Temperature dependent survivorship and development of Helicoverpa armigera (Hubner) (Lepidoptera-Noctuidae) on chickpea

doi:10.21203/rs.3.rs-4845823/v1

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Temperature dependent survivorship and development of Helicoverpa armigera (Hubner) (Lepidoptera-Noctuidae) on chickpea

https://doi.org/10.21203/rs.3.rs-4845823/v1

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Effect of constant temperatures (14°, 16°, 18°, 20°, 22°, 25°, 27°, 30°, 32°, 35° and 36°C) on demography and development of Helicoverpa armigera was evaluated under laboratory conditions (with 65% RH and 14L:10D h) on chickpea. Potential fecundity (pf) was significantly reduced to 86 females/female/generation at 35ºC compared to 532 at 27ºC. Intrinsic rate of increase (r_m) was minimum (0.0191 females/female/day) at 14ºC and maximum (0.0489) at 30ºC. Estimate of linear regression model showed that lower temperature threshold (T_min) of egg stage was 7.71ºC. Values of T_min for 1st, 2nd, 3rd, 4th, 5th and 6th instar were estimated as 4.97º, 10.52º, 4.67º, 4.44º, 5.74º and 4.19ºC, respectively. Total heat requirement for embryonic development was 74.07ºC-day. Degree day (DD) estimated by Arnold method showed that 542.75 DD was required by immature stage of H. armigera to complete its life cycle at 36ºC. Estimates of cubic polynomial model showed that lower temperature threshold (T_min) required for embryonic development was 8.47ºC and upper temperature threshold (T_max) was 38.83ºC. T_min required for development of 1st, 2nd, 3rd, 4th, 5th and 6th instar was 9.68º, 8.93º, 10.11º, 12.05º, 9.12º and 10.47ºC, respectively and T_max was 40.84º, 36.53º, 37.38º, 41.59º, 39.53º and 40.26ºC, respectively. It is concluded that pf was maximum at 27ºC while r_m at 30ºC. Development of H. armigera increased with increase in temperature and optimum development occurred at the range of 27º to 30ºC. Moreover, demographic parameters of H. armigera along with the thermal effect can be used to develop the models of population growth and prediction.

Development

Helicoverpa armigera

Demography

Thermal models

temperature

Helicoverpa armigera (Hubner) is a significant and highly adaptable pest that poses a serious threat to nearly 200 cultivated and wild plant species. It is a major hindrance to the production of various crops, including chickpeas, pigeon peas, chili peppers, tomatoes, okra, cotton, maize, sunflowers, tobacco, soybeans, and canola (Singh and Yadav 2009; Ahmad et al. 2014; Ahmad et al. 2015, Ahmad et al. 2017, Hugar et al. 2014; Abid et al. 2020; Reddy et al. 2022). This pest exhibits remarkable migratory behavior, exceptional survival and reproductive rates, multiple generations in a year, the ability to thrive on different host plants, and a strong capacity to develop resistance to insecticides (Wang et al. 2021). The impact of this pest on crop yields can be severe, with potential losses ranging from 95–100% in farmers' fields and pod damage caused by this pest can reach up to 100% (Singh and Yadav 2009; Ahmad et al. 2014; Kora and Teshome, 2021).

Helicoverpa armigera displays year-round activity and completes its life cycle in approximately 35–40 days, though the exact duration is contingent upon the host plants and the prevailing climatic conditions, (Vinutha et al. 2013). Temperature exerts a significant influence on the growth of arthropod populations, affecting their activity and seasonal dynamics, while also setting limits on various biological activities. This impact is evident in studies by Roy et al. (2002), Tochen et al. (2014), Hasan and Ansari, (2015), Labou et al. (2017), and Jung et al. (2023). Temperature plays a crucial role in determining the life cycle duration, fecundity, and survival of insect population (Howe 1967; Andrewartha 1970). Several models have been developed to elucidate the relationship between temperature and insect development (Kontodimas et al. 2004; Golizadeh et al. 2007; Aghdam et al. 2009; Jung et al. 2023). As development progresses, development rates become directly proportional to temperature and reach a point known as the "optimum temperature," (Allsopp et al. 1991). Beyond this optimum temperature, development rates sharply decline with further increases in temperature. Additionally, insect reproduction rates are temperature-dependent, typically up to a critical threshold (Dent, 1995), and the number of offspring produced tends to increase with rising temperatures (Mironidis and Savopoulou-Soultani 2008). However, high temperatures can lead to reduced fecundity. Helicoverpa species have the capacity to adapt to varying seasonal challenges for survival, including thermal stress, drought, food availability, cold conditions, and diseases, across a wide range of climatic zones, spanning from wet to dry, and tropical to cool temperate regions (Zohu et al. 2019). The regulation of diapause in H. armigera is primarily governed by environmental factors, with photoperiod and temperature serving as the main regulators (Jung et al. 2023).

Life tables serve as a valuable tool for accurately assessing the impact of external factors on the growth, survival, reproduction, and intrinsic rate of increase within insect populations (Chi and Su (2006); Stark et al. (2007); Ahmad et al. 2015; Fathipour et al. 2020). The analysis of multiple sets of life table data can unveil critical mortality factors, pivotal life stages or periods, and contribute to a deeper understanding of insect population dynamics. Simultaneously, it can pinpoint the most opportune period for effective management practices, in line with the findings of Harcourt (1969) and Southwood (1978). Pioneering work in this area was conducted by Deevey (1947) on natural animal populations. The intrinsic rate of increase is widely recognized as a fundamental measure of fitness among insects (Birch, 1948; Stark and Banks, 2003; Stark et al. (2007); Ahmad et al. 2013, 2015, 2017). Furthermore, the constant temperature at which the intrinsic rate of increase reaches its maximum is defined as the "optimal" temperature for a particular insect species (Shi et al. 2012). Growing degree day (GDD) is a measure of the amount of heat that accumulates above a specified base temperature during a 24 h period and it is a valuable tool for predicting pest activity (Mathukumalli et al. 2016).

While a few studies have explored the influence of constant temperatures on the growth parameters of H. armigera (Qureshi et al. 1999; Jallow and Matsumura 2001; Bartekova and Praslicka 2006; Mironidis and Savopoulou-Soultani 2008; Mironidis and Savopoulou-Soultani, 2012). There is currently a gap in the literature concerning the effects of constant temperature on life table parameters and degree days requirements of H. armigera when reared on chickpeas as their primary food source. Therefore, there is a need for a comprehensive study of the life history and survival of H. armigera on chickpeas at various temperatures to establish the critical temperature thresholds for its survival.

Temperature in relation to development and population growth studies will certainly provide the essential information to predict the seasonal abundance of H. armigera and construction of demographic models. Present study aims to find out the effect of constant temperatures on development, mortality and demographic parameters of H. armigera. The findings will contribute to the better understanding of effects of minimum and maximum temperature on demography, development of threshold temperatures and heat unit requirements (degree-days) from application of linear and non-linear models of H. armigera on chickpea.

Collection and rearing of larvae of H. armigera:

Sixth instar larvae of H. armigera were gathered from the field where the chickpea was grown for the experimental purpose. They were individually housed in 100 ml plastic containers and provided with fresh green chickpea pods daily until they pupated. The environment was controlled at 27 ± 1°C, 75% relative humidity, and a light-dark cycle of 14:10 hours. Pupae were collected and kept in jars for adult emergence. Upon emergence, adults were sorted by sex and paired in 20x10 cm rearing glass jars covered with muslin textile. A cotton wool piece soaked in 10% honey solution served as food and was replaced daily. Fresh chickpea branches with leaves and pods were provided for oviposition, maintained with moist soil, aluminum foil, and thin polythene sheet. Eggs laid on leaves were transferred to separate jars for hatching, and neonates were then moved to fresh chickpea leaves and pods individually housed in 100 ml plastic containers from the second instar onwards to prevent cannibalism. Daily, fecal matter and dry leaves/pods were replaced with fresh food until pupation, ensuring the multiplication and maintenance of the H. armigera culture throughout the experimental period.

Effect of constant temperatures on life table of H. armigera:

A detailed life table for H. armigera was constructed across a wide temperature range (14°, 16°, 18°, 20°, 22°, 25°, 27°, 30°, 32°, 35° and 36 ± 1°C) under controlled conditions (75% RH, 14:10 L:D). Ten replicates of 100 eggs each were sourced from a stock culture and monitored daily for hatching and development. All the experiments were conducted in BOD (Biological Oxygen Demand) incubator in controlled manner. First instars were reared on chickpea leaves, while subsequent instars were housed individually on pods to prevent cannibalism. Mortality and survival rates were recorded daily for each stage, and pre-pupal, pupal, and adult emergence durations were documented. Adult sex identification relied on characteristic wing patterns: females with brownish/reddish-brown forewings and males with dull greenish/yellow/light brown forewings, along with specific hindwing markings.

Female fecundity and life indices:

Young adults, both male and female, obtained from the aforementioned life table experiment, were paired and placed in a glass jar measuring 20X15 cm. The batches of 10 pairs were created and replicated three times to assess fecundity. The adults were provided with a 10% honey solution on cotton wicks as their food, along with fresh branches of chickpea containing leaves and pods for egg-laying. The freshness of the branches was maintained by wrapping moist soil around them and covering them with aluminum foil secured with thin polythene sheets. Whenever a male died, a new male from the same temperature conditions was introduced into the glass jar. This ensured that each female had access to a male for mating throughout its lifetime. The number of eggs laid by each female was recorded daily after mating until the female die. The similar method was adopted in our previous studies (Ahmad et al. 2013; Ahmad and Ansari 2013; Ahmad et al. 2015; Ahmad et al. 2017).

Fecundity table is thus, constructed with the following assumptions; x = Pivotal age (days), I_x = Number of females alive at the beginning of age interval x (x-pivotal age) as a fraction of an initial population of one (Birch 1948). m_x = Average number of eggs laid per female in each age interval assuming 50:50 sex ratio and computed as or mean number female offspring produced in a unit time by a female aged (x), $\:mx\:=Nx/2$, where N_x = Total natality per female offspring in each age. Besides ‘m_x’ total number of female offspring in each age interval i.e. female eggs laid in age interval (x). The value of I_x.m_x was computed by multiplying the column I_x with m_x that gives the total number of female births (female eggs laid) in each age interval (pivotal age x). This is also termed as ‘Reproductive Expectation’ (R₀). Intrinsic rate of increase (r_m) is defined as the instantaneous rate of increase of a population in a unit time under a given set of ecological conditions (Birch, 1948). It can be calculated by using the equation, $\:\sum\:\text{e}(-rm.x)\:Ix.mx\:=\:1\:$(Birch, 1948; Stark and Banks, 2003; Ahmad et al. 2013; Ahmad and Ansari 2013; Ahmad et al. 2015; Ahmad et al. 2017).

From the above data, Potential fecundity ($\:pf=\:mx$), intrinsic rate of natural increase (e^(−r_m^x).I_x.m_x = 1 (Birch 1948)); finite rate of increase (λ = Anti log_e r_m) were determined. Mean generation time (c) is the mean period over which offspring are produced and is estimated by the formula, c = I_x .m_x.X/I_x .m_x, while corrected generation time (τ) can be defined as the time from the birth of individuals to the birth of offspring and is determined by the formula, $\:\tau\:\:=\:\text{l}\text{o}\text{g}\text{e}\:\left(R0\right)/\:rm$. Doubling time (DT) is defined as the time required for the population to reimburse the loss and is calculated by the formula, DT = log_e 2/r_m.

Development of H. armigera at constant temperatures:

Eggs freshly laid from the stock culture were organized into batches of 100, with each batch replicated three times to yield a total of 300 eggs for each temperature ranging from 14°C to 36°C. The development time of eggs and successive instars (1st to 6th ), as well as pre-pupae and pupae, was recorded at each temperature. This experiment was repeated three times to ensure reliability. The duration of development for each stage was determined under constant temperature conditions. The rate of development per day was calculated by dividing the average development duration of all immature stages individually by one (1/d).

Linear Regression Model:

The impact of consistent temperatures on the development of H. armigera was examined by applying (i) linear regression and (ii) cubic polynomial fitting curves using Sigma Plot-Version 10 software. The rate of development, denoted as the inverse of the time needed to complete a life stage, was calculated as 1/d.

Linear regression equation was adopted to express the relationship between the temperature (T) and rate of development (D)

$$\:D\:=\:a\:+b\text{T}$$

………………………………………

Where, D = Development rate

Constants a and b were determined using the least squares method.

T = Temperature

The lower thermal threshold (T_min) was derived by substituting D = 0 into Eq. (1), resulting in

$$\:Tmin\:=\:-\:a/b$$

………………………….….…..….

Thermal constant was calculated by

$$\:K\:=\:1/b$$

………………………………………..

Means total quantity of thermal energy required to complete development

K = Thermal constant expressed in degree-days (Campbell et al. 1974)

b = Regression slope

The thermal units necessary for completing development were computed using Arnold's formula (Arnold, 1959, 1960):

$$\:DD\:=\:(\text{T}1\:\--\:{T}_{min}).D$$

……………………………

Where, DD = Degree days, D = Mean Development time, T₁ = Rearing temperature and T_min = Assumed minimum threshold temperature

Calculations and estimations were carried out using the software Microsoft Excel and Sigma Plot Version 10.

Cubic Polynomial Model:

Utilizing the linear model for calculating ambient temperature is not viable due to its monotonically increasing nature. Therefore, Harcourt and Yee (1982) demonstrated that a cubic curve can be fitted using the least squares method, assuming:

$$\:D\:=\:a\:+\:bT\:+c{T}^{2}\:+\:d{T}^{3}$$

…………..……….

Where, D = Development time, T = Temperature and the constants a, b, c and d, which were obtained from the normal equation of the least square method

To calculate the ambient temperature, we differentiate D √t*T and equate it to Zero (0)

i.e. $\:\text{d}D/\text{d}T=\:\text{b}+2cT+3d{T}^{2}=0$………………(6)

The ambient temperature is obtained by solving this quadratic equation and taking the larger of the two roots

If $\:{\alpha\:},\:{\beta\:}\:=\:\:-\:c\pm\:\surd\:\:{\text{c}}^{2}-3bd/3d,\:\:{T}_{opt}\:\:=\:{M}_{max}\:({\alpha\:},\:{\beta\:})\:$…………....(7)

The minimum threshold and maximum threshold temperatures are the minimum and the maximum roots representing the equation

$$\:a\:+\:bT\:+c{T}^{2}+\:d{T}^{3}\:=\:0\:$$

…………………....…

Statistical Analysis:

Bartlett’s test was employed to assess the homogeneity of all cumulative variances. Proportional binomial data underwent analysis using logistic regression within a generalized linear mixed models (GLMM) framework, specifically employing Pearson's chi-squared test. Subsequently, a one-way ANOVA was conducted. Statistical analysis of life indices and data from linear and polynomial cubic models was performed using repeated measures of the protected Fisher’s least significant difference (Tukey’s test, LSD) at a significance level of P < 0.05. The software utilized for these analyses included "MINITAB-16 for Windows" and "SigmaPlot version 10".

Fecundity of H. armigera varied significantly (P<0.05) at constant temperatures (Fig-1). Mating took place following emergence of adults and females initiated egg laying after a pre-oviposition period of 4 days at 14ºC and 20ºC, 3 days at 18ºC and 22ºC, 2 days at other temperatures, and 1 day at 35ºC. The oviposition period was extended to 9 days at 16ºC but shortened to 3 days at 36ºC. Post-oviposition lasted for 5 days at 14ºC and 18ºC, and 1 day at 22ºC and 27ºC. Peak egg laying occurred on the 75.5th day of the pivotal age at 14ºC and the 24.5th day at 36ºC. Following the peak, egg laying decreased with age across all temperatures. H. armigera females laid a significantly higher number of eggs at 27ºC compared to other temperatures (P<0.05). The daily fecundity rate (mx) increased with age, peaked, and then gradually decreased until the female's death. At 30ºC, the daily fecundity rate was greater (158 females/day) on the 6th day after emergence compared to 57 females/day on the 7th day at 14ºC and 58 females/day on the 5th day at 36ºC. Female longevity was 14 days at 16ºC and 7 days at 36ºC.Life indices of H. armigera were significantly (P<0.05) affected at constant temperatures (Table-1). Potential fecundity (pf) was significantly (P<0.05) reduced to 86 females/female/generation at 35ºC compared to 532 at 27ºC (Bartlett’s K² =77.45; df =10; F= 443.6, P= 0.002, LSD= 22.4). It was increased from 14º to 27ºC and then decreased up to 35ºC. Net reproductive rate (R₀) was significantly higher (138.1 females/female/generation) at 30ºC than to 38.59 at 14ºC and greatly (Bartlett’s K² =77.45; df =10; F= 194.6, P< 0.001, LSD= 6.3) reduced to 2.98 females/female/generation at 36ºC. Intrinsic rate of increase (r_m) was significantly (F= 67.2, P= 0.003, LSD= 0.0032) differed at constant temperatures and smallest value (0.0191 females day^-1) occurred at 14ºC and highest (0.0489 females day^-1) at 30ºC. The intrinsic rate of increase (r_m) rose as the temperature increased from 14ºC to 30ºC and subsequently declined at 36ºC. At 30ºC, a total of 1.119 females/female/day were born, while a significantly lower birth rate (λ) of 1.044 females/female/day was observed at 14ºC. There was no significant difference in birth rate observed between temperatures ranging from 22ºC to 36ºC. The duration required by H. armigera to complete one generation (c) was significantly reduced (23.5 days) at 36ºC, while it was extended to 82.5 days at 14ºC, as indicated by a significant difference (P<0.001). The corrected generation time (τ) followed a similar pattern at constant temperatures. H. armigera took a longer time (15.7 days) to double its population at 14ºC, whereas 6.15 days were required at 30ºC, followed by 7.3 days at 36ºC. The multiplication rate was higher at 27ºC, 30ºC, and 32ºC compared to other tested temperatures. Mortality across different instars was observed to be unpredictable at constant temperatures (Fig-2), with higher mortality rates in early instars at both higher and lower temperature ranges compared to late instars.

The findings from Table-2 demonstrated that constant temperatures had a significant effect (P<0.05) on the larval development of H. armigera. Immature development consistently decreased with increasing temperatures from 14ºC to 36ºC, with no development observed at 37ºC. The incubation period was 6.2 days at 14ºC, while it decreased to 2.1 days at 36ºC. The duration of the 1^st instar was significantly prolonged to 4.9 days at 14ºC and shortened to 2.1 days at 36ºC, with no significant difference observed between 25ºC and 30ºC. The duration of the 2nd instar was 5.1 days at 14ºC and 1.1 days at 36ºC, with no observed effect on the duration of the 2^nd instar at 18ºC and 20ºC (3.9 days). The pre-pupal period was 5.5 days at 14ºC and significantly shortened to 1.6 days at 36ºC, with no significant difference observed between 14ºC and 20ºC, 22ºC and 30ºC, and 32ºC and 36ºC. The pupal period was significantly (P<0.05) prolonged to 32.5 days at 14ºC and reduced to 6.0 days at 36ºC. Overall, the development of the immature stage (egg to pupa) was significantly prolonged to 75.9 days at 14ºC and shortened to 18.6 days at 36ºC.

The data of “development per day” was used in linear regression analysis (D=a+bt) in relation to constant temperatures (Table-3). Regression data differed significantly at various probability levels. Values of R² are also differed significantly for various developmental stages (F = 51.61; R² = 0.9515; P = 0.0001^*Eggs; F = 16.00; R² = 0.8911; P = 0.0031^{*1st instar}; F = 40.64; R² = 0.9187; P = 0.0001^{*2nd instar}; F = 16.76; R² = 0.9507; P = 0.0027^{*3rd instar}; F = 29.16; R² = 0.9642; P = 0.0004^{*4th instar}; F = 26.73; R² = 0.9481; P = 0.0006^{*5th instar}; F = 40.98; R² = 0.8988; P = 0.0001^{*6th instar}; F = 107.7; R² = 0.9229; P = 0.0001^*Pre-pupa; F = 579.9; R² = 0.9847; P = 0.0004^*Pupa). Lower temperature threshold (T_min) of egg stage was computed as 7.71ºC. Values of T_min for 1^st, 2^nd, 3^rd, 4^th, 5^th and 6^th instar were estimated as 4.97º, 10.52º, 4.67º, 4.44º, 5.74º and 4.19ºC, respectively. T_min for pre-pupal and pupal stages were 8.41º and 8.42ºC, respectively. Similarly, T_min for overall immature development of H. armigera was 6.82ºC. Therefore, result showed that all stages of H. armigera may be available in the field condition with a range of 4º to 10.52ºC.

Thermal constant (K) is often called as ºC-day is calculated by method of Campbell et al. (1974) and differed significantly at constant temperatures (F = 329.58; df = 9,99; P < 0.05) (Table 4). Total heat requirement for embryonic development was 74.07ºC-day. The 1^st, 2^nd, 3^rd, 4^th, 5^th and 6^th instars required 48.07, 34.60, 58.48, 68.02, 38.46, and 58.82ºC-day, respectively. However, the values of thermal constant required for the development of 3^rd and 6^th instars were not significantly different. Development of pre-pupa and pupa required 40.32 and 161.29ºC-day, respectively. It showed that pupa required maximum heat for its development compared to other stages of H. armigera. Moreover, 588.24ºC-day was required for the development of H armigera.

Degree day was estimated by the method of Arnold (1959, 1960). Results (Table-4) showed that degree day (DD) requirement was increased with increasing the temperatures from 14º to 36ºC for eggs and larval development and fluctuated after 22ºC. Development of egg was prolonged at 14ºC; therefore, degree day requirement was less than those eggs which were developed fast at 36ºC. The DD required for egg stage was 39.0 at 14ºC and 59.41 at 36ºC. A total of 542.75 DD was required by immature stage of H. armigera to complete its life cycle at 36ºC. Degree requirement was increased with increasing temperature from 14º to 22ºC then decreased with further increasing temperature from 25º to 27ºC.

Cubic polynomial model was used to determine maximum and minimum threshold temperatures. Estimates of development rate were determined at constant temperatures by fitting in polynomial equation and computed R² and RSS which are presented in Table-5. Lower temperature threshold (T_min) required for embryonic development was 8.47ºC and upper temperature threshold (T_max) was 38.83ºC. T_min required for development of 1^st, 2^nd, 3^rd, 4^th, 5^th and 6^th instar was 9.68º, 8.93º, 10.11º, 12.05º, 9.12º and 10.47ºC, respectively and T_max was 40.84º, 36.53º, 37.38º, 41.59º, 39.53º and 40.26ºC, respectively. The values of T_min for pre-pupa and pupa was 7.31º and 10.9ºC and T_max was 36.03º and 37.11ºC, respectively. Results showed that ambient temperature (T_opt) for development of different stages of H. armigera was within the range of 26.21º to 31.16ºC. Ambient temperature for egg development was 30.36ºC and for 1^st, 2^nd, 3^rd, 4^th, 5^th, 6^th instar, pre-pupa and pupa was 31.16º, 27.60º, 27.27º, 29.24º, 30.21º, 29.79ºC, 28.72º and 26.21ºC, respectively. However, fractional variation has occurred in T_optof 2^nd & 3^rd instars and 4^th & 6^th instars.

The relationship between temperature and developmental rate is critical for understanding and predicting the development time of insect pests. This understanding is invaluable for pest management programs, which aim to control pest populations efficiently and reduce the damage they cause to crops and ecosystems (Roy et al. 2002; Hasan and Ansari, 2015; Bapatla et al. 2022; Du Plessis et al. 2020). In our study, we observed that H. armigera can only develop within a specific temperature range, from 14° to 36°C. Outside this range, development ceases entirely. This indicates that temperature is a limiting factor for the survival and development of this species. Further research supports this finding, showing that both low and high temperatures significantly hinder the development of H. armigera. Specifically, it cannot develop from egg to adult outside the range of 13.3–32.5°C (Jallow and Matsumura 2001; Jung et al. 2023). Du Plessis et al. (2020) investigated the developmental rate of another pest, Spodoptera frugiperda, and found that it increases linearly with rising temperatures within the range of 18 to 30°C. They also noted that larval survival was highest between 26 and 30°C, indicating an optimal temperature range for both development and survival. Similarly, Mironidis and Soultani (2008) studied the survival of another insect species over a wide constant thermal range of 15°-27.5°C and found that survival rates remained stable within this range. However, survival decreased sharply below 15°C, reaching zero at 12.5°C. At the higher end of the spectrum, survival also dropped quickly above 28°C, with no survival at 40°C. This demonstrates the narrow thermal tolerance for survival outside optimal temperatures. Our research further revealed that the survival rate of both male and female H. armigera declined with increased exposure to high temperatures. Specifically, the time required to achieve 50% and 90% mortality of the adult population decreased rapidly as the temperature rose from 40° to 46.5°C (Mironidis and Soultani 2010). This indicates that higher temperatures can be lethal over shorter exposure periods. Moreover, we found that the overall development time of immature H. armigera stages varied significantly with temperature. At 14ºC, development took 75.9 days, while at 36ºC, it was reduced to 18.6 days. This demonstrates that higher temperatures accelerate development, up to a certain point. Additionally, Shah et al. (2013) reported that the egg development period for H. armigera was shortest at 3 days when temperatures were 35±1°C, and longest at 4.5 days at 27±1°C. Similarly, the larval period was shortest at 13 days at 35±1°C, and longest at 18 days at 27±1°C. This further emphasizes that development rates are highly temperature-dependent, with faster development occurring at higher temperatures within the optimal range. Understanding the relationship between temperature and developmental rate is essential for predicting pest development and implementing effective pest management strategies. By knowing the temperature ranges that facilitate or inhibit pest development, agricultural practices can be better tailored to control pest populations, potentially through environmental manipulations or timing of interventions.

We found that the maximum numbers of eggs laid by a female were counted at 27°C and minimum at 35°C (Table 1). Potential fecundity was highest at 27°C but reproductive rate was greater at 30°C than to other tested temperatures on H. armigera. Our results were as par with that of Mironidis and Soultani (2008) found that maximum numbers eggs of H. armigera were laid at 25°C and minimum at 35°C. Noor-ul-Ane et al. (2018) found that maximum fecundity of H. armigera was 973 eggs per female at 25°C decreasing to 72 eggs per female at 37.5°C. Mohite et al. (2011) also reported that fecundity of H. armigera was positively correlated with temperature. Maximum oviposition occurred between 25° and 27°C, however, 30°C or higher was detrimental.

Intrinsic rate of increase is the only biological index that summarizes physiological qualities of an insect relative to its capacity of increase (Stark and Banks 2003; Stark et al. 2007; Ahmad et al. 2013, 2015). It provides an effective summary of insect life history traits as well as a good indicator of temperature at which growth of a population is most favourable. We found that intrinsic rate of increase was highest at 30°C, and lowest at 14°C and significantly differed at 27° and 30°C. However, the r_m is greater at 30°C than to 27°C but potential fecundity and reproductive rate was highest at 27°C compared to other temperatures tested. According to the studies of Mironidis, (2014) the intrinsic rates of increase were positive, indicating that H. armigera could be anticipated to either persist or proliferate in numbers within the temperature range of approximately 17.5 to 32.5 °C, with the peak value occurring around the mean temperature of 27.5 °C. H. armigera demonstrates survival, development, and reproduction across a broad spectrum of fluctuating temperatures, albeit with varying degrees of success at different mean temperatures due to diurnal variations. Mironidis and Soultani (2008) reported that intrinsic rate of increase was highest at 27.5°C, at both constant and corresponding alternating temperature regimes. They also showed that extreme temperatures had negative effect on life table parameters of H. armigera. The value of r_m and 𝜆 were higher at 27°C and 30°C compared to other temperatures because development of immature was fast and high rate of offspring production per day of Zygogramma bicolorata on Parthenium hysterophorus (Hasan and Ansari 2015).

Linear models, such as degree-day models, are widely used to predict the thermal responses of insects (Rebaudo & Rabhi, 2018; Schmalensee et al., 2021). However, both theoretical and empirical data indicate that biological thermal reaction norms are generally not linear. In the present study, it is estimated by linear regression equation that lower temperature threshold (T_min) for embryonic development was 7.71°C, while different larval instars can be able to develop between 4.19° to 10.52°C (Table 3). However, T_min was estimated to be 6.82°C for development of immature stages of H. armigera. The value of T_min was highest for second instar which means that among all the immatures, second instar larvae require more heat to complete its development. Qureshi et al. (1999) reported that development threshold temperature for egg, larva and pupa of H. armigera was 10.8°, 13.6° and 14.6°C, respectively. Furthermore, the effective sums for development were 45.5, 200.0 and 142.9 degree day, respectively. Developmental threshold of 10.5°, 11.3° and 13.8°C was estimated for egg, larval and pupal stages of H. armigera, respectively (Jallow and Matsumura 2001). These variations could be due to the change in the geographical distribution and the food source of H. armigera.

Thermal constant (ºC-day) is the amount of heat that each species required to complete its life cycle or part of it, regardless of temperature to which it is expressed. It is estimated in the present study that the thermal constant was 74.07°C-day for embryonic development which is greater than each larval stage of H. armigera whereas, pupal stage required 161.29°C-day for its development. A total of 588.24°C-day required for development of immature stage. Degree day (DD) required for development of egg at 14°C was 39.88 DD, while it was 62.76 DD at 35°C in the present study (Table 4). Jallow and Matsumura (2001) also reported that a thermal constant of 51 DD was required for development of eggs and 215.5 DD for larval stages. The DD required for egg stage was 39.99 at 14ºC and 59.41 DD at 36ºC and 542.78 DD was required for development of immature. While, Bartekova and Praslicka (2006) reported the thermal constant for development of eggs, larvae and pupae were 64.1, 344.8 and 222.2 DD, respectively. Lower thermal threshold for total development of H. armigera was 11.5°C with a thermal constant of 625.0 DD (Bartekova and Praslicka, 2006). Mohite et al. (2011) reported that a mean thermal constant (DD) of 45.53, 195.98, 142.62 and 81.53 above estimated lower threshold temperature was required for incubation of eggs, larval, pupal development and oviposition period, respectively. A limited number of degree-days in autumn season prevented part of population of H. armigera from developing to diapausing pupal stage. Emergence of 10, 25, 50, 75, and 90% of adults required 153, 199, 252, 303, and 347 DD, respectively (Mironidis et al. 2010). When temperature goes beyond the optimal, degree-day models cannot be applied, and are, in fact, unsuitable for predicting insect development.

The estimated optimum temperature (T_opt) was 30.36°C for egg development, while 27° to 32°C for larval development in the present study. However, development of pupa was fast at 26.21°C. The T_opt for total immature development was estimated to be 27.81°C. Upper thermal threshold (T_max) of egg was 38.83°C and 4^th instar can be able to tolerate up to 41.59°C compared to other instars. The value of T_max of immature of H. armigera was ranged between 35.31° to 41.59ºC. Estimated T_minby application of Linear Regression and Cubic Polynomial Models were found to be variable for different stages of immature. The value of T_min for second instar was highest if calculated with linear regression curve fitting model which proves that the lower threshold temperature required by second instar of H. armigera is high as compared to other instars. Optimal developmental temperatures estimated for eggs, larvae, pupae, and total immature stages were 34.84º, 34.22º, 35.37º, and 34.61ºC, respectively under constant temperatures (Mironidis and Soultani 2008). They also reported that upper developmental thresholds (T_max) for each immature stage and for the total immature stage were estimated between 39.11º and 43.54ºC. In the present study, T_max ranged from 35.31° to 41.59ºC. Finally, the information generated from the present study is useful in developing new models in order to forecast population dynamics of H. armigera which will be helpful tools for its management. It is necessary that ecological factors which have profound effect on the performance of H. armigera in the field conditions be further investigated in order to impose them in the management programs.

Competing Interest:

The authors declare no conflict of interest.

Fundings:

No funding was obtained for this study.

Author Contribution

SA perform the experiments and wrote the manuscript

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Table 1. Effect of constant temperature on life indices of H. armigera

T (ºC)	pf	*R_o*	*r_m*	λ	c	Τ	DT
14	149±5.5g	38.59±2.1f	0.0191±2.6 e-4j	1.044±0.32b	82.5±3.5a	83.0±2.6a	15.7±1.2a
16	234±6.3f	50.47±1.6e	0.0224±2.4 e-4i	1.052±0.13b	66.7±1.6b	75.9±1.6b	13.4±1.0b
18	157±10.5g	31.44±2.5g	0.0226±2.5 e-4i	1.053±0.16b	59.4±2.6c	66.2±1.8c	13.3±0.6b
20	292±2,5e	68.44±2.3d	0.0300±3.4 e-4h	1.071±0.36b	56.3±2.3c	61.1±2.4c	10.0±0.7c
22	342±33.7d	78.44±1.7c	0.0357±1.8 e-4g	1.085±0.36a	48.4±1.8d	53.0±2.8d	8.4±0.3d
25	429±22.6c	70.38±1.6d	0.0393±2.7 e-4e	1.094±0.47a	42.0±1.7e	47.0±0.8e	7.6±0.8d
27	532±21.6a	98.94±1.5b	0.0475±9.1 e-4b	1.115±0.03a	38.7±1.0f	42.0±1.5e	6.3±0.8e
30	503±26.3b	138.1±3.7a	0.0489±1.6 e-4a	1.119±0.06a	36.2±1.3f	40.0±1.3f	6.1±0.2e
32	243±9.4f	70.32±2.8d	0.0455±1.3 e-4c	1.110±0.16a	34.2±1.8f	37.9±1.7f	6.6±0.6e
35	86±8.3h	17.13±1.6h	0.0390±1.5 e-4f	1.093±0.18a	25.9±1.5g	29.6±0.5g	7.7±0.4f
36	90±4.7h	2.98±0.1i	0.0408±2.4 e-4d	1.098±0.05a	23.5±0.5g	27.0±0.7g	7.3±0.7f

Within column, means followed by different letters are significantly different according to Tukey HSD (P < 0.05) (± SD).

Whereas, pf = potential fecundity, R_o = Net Reproductive rate, r_m = intrinsic rate of increase, λ = Finite rate of increase, c = mean length of generation time, τ = corrected generation time and DT = doubling time

Table 2. Effect of constant temperature on the development of H. armigera (Days±SE)

T (°C)	Egg	L₁	L₂	L₃	L₄	L₅	L₆	PP	P	Total
14	6.2±0.6a	4.9±0.4a	5.5±0.3a	5.1±0.5a	5.2±0.4a	5.3±0.3a	5.6±0.2a	5.5±0.3a	32.6±2.3a	75.9±2.6a
16	4.2±0.2b	4.5±0.3a	4.7±0.2a	4.8±0.2a	4.3±0.4b	4.8±0.2b	4.6±0.1a	4.4±0.1a	24.5±1.3b	60.8±2.8b
18	4.2±0.2b	4.3±0.2a	3.9±0.5b	3.3±0.2c	3.9±0.1b	4.3±0.3b	4.2±0.3a	4.7±0.3a	18.8±0.8c	51.6±1.5c
20	3.6±0.3c	3.7±0.5b	3.9±0.5b	3.9±0.1b	3.8±0.3b	4.0±0.1b	4.0±0.1b	3.5±0.4a	15.5±0.3d	45.9±1.6d
22	3.3±0.4c	2.4±0.2c	3.5±0.3b	3.6±0.2b	3.6±0.1b	3.8±0.2b	3.3±0.3b	3.7±0.2b	12.6±0.7e	39.8±1.4e
25	2.3±0.5d	2.1±0.1c	3.2±0.2b	3.6±0.3b	3.4±0.1b	3.3±0.4c	2.3±0.2c	2.6±0.3b	9.0±0.5f	31.8±1.2f
27	3.1±0.2c	2.1±0.1c	2.2±0.1c	3.2±0.1c	2.2±0.3c	2.1±0.1d	3.3±0.1b	2.1±0.1b	8.2±0.5f	28.5±1.3f
30	2.1±0.1d	2.2±0.2c	2.3±0.3c	3.1±0.1c	3.2±0.2b	2.4±0.2c	2.6±0.1c	2.1±0.1b	7.2±0.2g	27.2±1.6g
32	2.2±0.3d	2.3±0.2c	2.1±0.1c	2.2±0.2d	2.3±0.3c	3.1±0.1c	2.3±0.1c	1.6±0.2c	7.1±0.5g	25.2±1.9g
35	2.3±0.2d	1.1±0.1d	1.2±0.3d	2.3±0.2d	2.3±0.1c	1.7±0.1d	2.1±0.2c	1.3±0.1c	6.3±0.8g	20.6±0.8h
36	2.1±0.1d	2.1±0.2c	1.1±0.1d	1.3±0.2e	1.6±0.2c	1.3±0.1d	1.5±0.2d	1.6±0.1c	6.0±0.3g	18.6±0.9h
37	NCD (Not Completely Developed)

Within column, means followed by different letters are significantly different according to Tukey HSD (P < 0.05) (± SD).

Whereas, L1, L2, L3, L4, L5, L6, PP and P are duration of I, II, III, IV, V, VI, Pre-pupa and Pupa respectively.

Table 3. Estimates of linear regression curve fitting on the development of H. armigera

Stages	a	b	df	F	P	R²	*RSS*	*T_min* (°C)	K*
Egg	-0.1041	0.0135	9,11	51.61	0.0001	0.9515±0.002b	0.0018	7.71	74.07±1.3c
L1	-0.1033	0.0208	9.11	16.00	0.0031	0.8911±0.003d	0.0145	4.97	48.08±0.7f
L2	-0.3041	0.0289	9,11	40.64	0.0001	0.9187±0.001c	0.0083	10.52	34.60±0.9 h
L3	-0.0798	0.0171	9,11	16.76	0.0027	0.9507±0.001b	0.0212	4.67	58.47±0.7e
L4	-0.0654	0.0147	9.11	29.16	0.0004	0.9642±0.004a	0.0021	4.45	68.03±1.1d
L5	-0.1492	0.026	9,11	26.73	0.0006	0.9481±0.002b	0.0103	5.74	38.46±0.4g
L6	-0.0713	0.017	9,11	40.98	0.0001	0.8988±0.002d	0.0301	4.19	58.82±0.7e
PP	-0.2086	0.0248	9.11	107.70	0.0001	0.9229±0.005c	0.0301	8.41	40.32±1.1g
P	-0.0547	0.0062	9,11	579.90	0.0001	0.9847±0.007a	0.0004	8.82	161.29±2.0b
IS	-0.0116	0.0017	9,11	404.11	0.0001	0.9782±0.004a	0.0000372	6.82	588.24±3.7a

* Thermal constant

Within column, means followed by different letters are significantly different according to Tukey HSD (P < 0.05) (± SD).

Table 4. Degree days (Arnold method) for development of H. armigera at constant temperatures

T (°C)	Egg	L1	L2	L3	L4	L5	L6	PP	P	IS
14	39.00	44.25	19.14	51.32	49.66	43.78	54.94	30.75	168.87	544.96
16	34.82	49.64	25.76	53.25	49.67	49.25	54.33	33.40	175.91	558.14
18	43.22	56.03	29.17	51.99	52.85	52.72	58.00	45.07	172.58	576.89
20	44.24	55.61	36.97	59.79	59.09	57.04	63.24	40.57	173.29	604.96
22	47.16	40.87	40.18	60.66	63.18	61.79	58.77	50.28	166.07	604.16
25	39.77	42.06	46.34	65.06	69.87	63.56	47.86	43.13	145.62	578.12
27	59.80	46.26	36.26	49.13	49.61	44.65	75.27	39.04	149.08	575.13
30	46.81	55.07	44.80	58.26	81.76	58.22	67.11	45.34	152.50	630.50
32	53.44	62.17	45.11	57.39	63.37	81.41	63.96	37.74	164.58	634.54
35	62.77	33.03	29.38	36.40	70.27	49.74	64.70	34.57	164.93	580.51
36	59.41	65.16	28.03	34.46	50.48	39.34	47.72	44.14	163.08	542.75

Whereas, L1, L2, L3, L4, L5, L6, PP, P and IS are I, II, III, IV, V, VI larval instar, pre-pupa, pupa and immature stages respectively.

Table 5. Estimates of cubic polynomial curve (D = a + bt + cT2 + dT3) and threshold temperatures

Stages	F	P	df	R²	*RSS*	*T_min* (°C)	*T_opt*	*T_max*
Egg	18.46	0.0001	7,11	0.9878a	0.0014	8.47	30.36	38.83
L1	4.15	0.0451	7,11	0.8975e	0.0112	9.68	31.16	40.84
L2	71.36	0.0001	7,11	0.9683b	0.0189	8.93	27.60	36.53
L3	13.40	0.0027	7,11	0.9229d	0.0387	10.11	27.27	37.38
L4	10.15	0.0064	7,11	0.9132d	0.0309	12.05	29.54	41.59
L5	13.03	0.0030	7,11	0.9482c	0.0502	9.12	30.21	39.33
L6	16.56	0.0015	7,11	0.8966e	0.0254	10.47	29.79	40.26
PP	38.36	0.0001	7,11	0.9427c	0.0224	7.31	28.72	36.03
P	361.72	0.0001	7,11	0.9937a	0.0002	10.9	26.21	37.11
IS	211.45	0.0001	7.11	0.9891a	0.000019	7.5	27.81	35.31

Within column, means followed by different letters are significantly different according to Tukey HSD (P < 0.05).

Whereas, T_min, T_opt and T_max are the lower thermal threshold, optimum temperature and maximum thermal threshold respectively. (Values of constants, a, b, c and d are calculated by least square method).

No competing interests reported.

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Temperature dependent survivorship and development of Helicoverpa armigera (Hubner) (Lepidoptera-Noctuidae) on chickpea

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Abstract

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Introduction

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Female fecundity and life indices:

Linear Regression Model:

Cubic Polynomial Model:

Statistical Analysis:

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