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Repeated short-term thermal stress and its impact on reproductive fitness in parthenium beetle, Zygogramma bicolorata (Coleoptera: Chrysomelidae)

Published online by Cambridge University Press:  02 December 2024

Arvind Kumar Patel,
Priyanka Yadav and
Bhupendra KumarOpen the ORCID record for Bhupendra Kumar[Opens in a new window]
Arvind Kumar Patel
Affiliation:
Department of Zoology, Banaras Hindu University, Varanasi, 221005, India
Priyanka Yadav
Affiliation:
Department of Zoology, Banaras Hindu University, Varanasi, 221005, India
Bhupendra Kumar*
Affiliation:
Department of Zoology, Banaras Hindu University, Varanasi, 221005, India
*
Corresponding author: Bhupendra Kumar; Email: bhupendrakumar@bhu.ac.in
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Abstract

Insects experience variable temperature conditions in their natural environment, making constant temperature conditions in studies unrealistic. To address this, we investigated the effects of repeated short-term heat stress (STH) and short-term cold stress (STC) conditions on the pre-oviposition, oviposition, and post-oviposition periods, as well as on fecundity and egg viability of the parthenium beetle, Zygogramma bicolorata Pallister (Coleoptera: Chrysomelidae). We found that pre-oviposition periods were shortest under STH conditions and at the optimal temperature and longest under STC conditions. Conversely, oviposition and post-oviposition periods were longest at the optimal temperature. Oviposition periods were shortest under STH, whereas post-oviposition periods were shortest under both STH and STC conditions. Age-specific fecundity trends were triangular, and egg-viability trends were plateau-shaped at all temperatures. Females subjected to STH conditions experienced the highest oviposition peaks early in their adult life. Conversely, lifetime fecundity and longevity were highest at the optimal temperature, whereas egg viability was maximal under STH conditions. Regardless of the temperature they were maintained at, middle-aged females exhibited the highest fecundity and egg viability. Based on these results, despite reducing overall fecundity and longevity, STH conditions enhanced daily oviposition in females, with the peak occurring early in adult life. Additionally, both STH and STC conditions increased percentage egg viability in parthenium beetles.

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Type
Research Paper
Information
The Canadian Entomologist , Volume 156 , 2024, e38
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Copyright
© The Author(s), 2024. Published by Cambridge University Press on behalf of Entomological Society of Canada

Introduction

Insects have evolved to thrive within specific habitats. The optimal performance of insects relies on a relatively narrow range of abiotic factors, such as temperature, relative humidity, and photoperiod (Terblanche Reference Terblanche2014; Singh et al. Reference Singh, Singh, Yadav, Giri and Verma2018). Temperature is the main abiotic factor that directly affects the ecology of insects (Bale et al. Reference Bale, Masters, Hodkinson, Awmack, Bezemer and Brown2002; Skendžić et al. Reference Skendžić, Zovko, Živković, Lešić and Lemić2021). Being ectothermic in nature, insects depend on external temperatures for growth, development, and survival (Denlinger and Lee Reference Denlinger and Lee2010; Sarmad et al. Reference Sarmad, Shakoor and Zaka2023). At the optimum temperature, insects not only complete their development most efficiently but also reproduce in the greatest numbers over a given period and achieve the highest survival rates over time (Deal Reference Deal1941; Davidson Reference Davidson1944). When exposed to stressful cold temperatures, insects undergo a range of physiological and biochemical changes that can negatively affect their reproductive rate, morphology, and biochemistry (González-Tokman et al. Reference González-Tokman, Córdoba-Aguilar, Dáttilo, Lira-Noriega, Sánchez-Guillén and Villalobos2020). Even brief exposure to stressful cold temperatures may reduce their rate of development, reproduction, and longevity considerably (Terada et al. Reference Terada, Matsumura and Miyatake2019; Wang et al. Reference Wang, Wang, Yu, Dang, Sun and Li2021). Similarly, under stressful hot temperatures, various physiological processes in insects, such as feeding rate, digestion, and nutrient absorption, are diminished (Yu et al. Reference Yu, Zhao, Zhou, Pan, Tian, Yin and Chen2022). Several insect life-history traits, such as foraging behaviour, mating, and voltinism, are expected to change as temperature increases above optimal (Clissold and Simpson Reference Clissold and Simpson2015; Mirth et al. Reference Mirth, Saunders and Amourda2021). Although high temperatures may tend to decrease insect body size, reproductive abilities, and life span, they also increase rates of growth and development (Denlinger and Yocum Reference Denlinger, Yocum, Hallman and Denlinger2019; Zhu et al. Reference Zhu, Wang and Ma2019).

Earlier investigations have revealed that the impact of short-term high- or low-temperature stresses can have either positive or negative effects on insect reproduction and survival, depending on the intensity and duration of exposure to heat or cold, on the species, and on the life stage of the insect (Hoffmann et al. Reference Hoffmann, Sørensen and Loeschcke2003; Marshall and Sinclair Reference Marshall and Sinclair2012). Small changes in temperature conditions below or above optimal have been reported to increase (Economos and Lints Reference Economos and Lints1986; Sørensen et al. Reference Sørensen, Sarup, Kristensen, Loeschcke, Le Bourg and Rattan2008), decrease (Carroll and Quiring Reference Carroll and Quiring1993; Butler and Trumble Reference Butler and Trumble2010), or have no effect on (Kjærsgaard et al. Reference Kjærsgaard, Pertoldi, Loeschcke and Blanckenhorn2013) the life span of insects. Although short-term low-temperature exposure below optimal levels has been reported to improve reproductive abilities in insects (Renault Reference Renault2011), exposure to short-term high temperatures above optimal has been shown to negatively affect the oviposition period and fecundity of many insects (Ebrahimi et al. Reference Ebrahimi, Talebi and Fathipour2020; Liao et al. Reference Liao, Liu and Li2022). For example, the longevity, oviposition period, and fecundity of the cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae), decreased after the insect was exposed to short-term high temperatures ranging from 40 to 46.5 °C (Mironidis and Savopoulou-Soultani Reference Mironidis and Savopoulou-Soultani2010). Similarly, short intervals of temperatures of 36 °C or higher significantly reduced the survival rates, reproductive parameters, and longevity in adults of fungus gnat flies, Bradysia difformis (Frey) and Bradysia odoriphaga Yang and Zhang (Diptera: Sciaridae) (Zhu et al. Reference Zhu, Xue, Luo, Ji, Liu, Zhao and Sun2017).

Research by González-Tokman et al. (Reference González-Tokman, Córdoba-Aguilar, Dáttilo, Lira-Noriega, Sánchez-Guillén and Villalobos2020) has highlighted the swift and lethal impact of heat stress on insects. Interestingly, other studies have suggested that brief exposure to extreme temperatures can paradoxically enhance an organism’s heat tolerance (Hoffmann et al. Reference Hoffmann, Sørensen and Loeschcke2003) and can also confer resistance to cold temperatures (Kelty and Lee Reference Kelty and Lee2001; Worland and Convey Reference Worland and Convey2001). When faced with seasonal variations or conditions outside the optimal range, insects must either endure or evade stress, which can increase or decrease their fitness (Buckley et al. Reference Buckley, Arakaki, Cannistra, Kharouba and Kingsolver2017; Zeng et al. Reference Zeng, Lian, Jia, Liu, Wang and Yang2022). Throughout evolution, insects have evolved various behavioural and physiological responses to avoid high temperatures and other stress impairments. Most insect species are believed to employ a variety of behavioural, physiological, or genetic survival mechanisms to cope with thermal stress (Colinet et al. Reference Colinet, Sinclair, Vernon and Renault2015). For example, short-term exposure to high temperatures is thought to stimulate alterations in protein synthesis (Zeng et al. Reference Zeng, Zhu, Fu and Zhou2019), which leads to oxidative stress and increased levels of lipid peroxidation, along with enhanced antioxidant enzyme activity in insects (Zhu et al. Reference Zhu, Xue, Luo, Ji, Liu, Zhao and Sun2017). Strong evidence suggests that hormesis is a general adaptive response that often occurs as an overcompensation following the disruption of homeostasis and damage associated with low levels of stress (Calabrese Reference Calabrese2001). Stress at low doses or moderate levels therefore may contribute to fitness, whereas stress at high doses is largely detrimental (Cutler et al. Reference Cutler, Amichot, Benelli, Guedes, Qu and Rix2022).

In the present study, we investigated the effects of repeated short-term heat- and cold-stress conditions on the pre-oviposition, oviposition, and post-oviposition periods and on the fecundity, egg viability, and survival rates of females of the parthenium beetle, Zygogramma bicolorata Pallister (Coleoptera: Chrysomelidae). Previous studies have shown that the beetle’s optimal temperature range is 25–30 °C (Bhusal et al. Reference Bhusal, Ghimire, Patel, Bista, Upadhyay and Kumar2020; Patel et al. Reference Patel, Bhusal, Kumar and Kumar2020). Both the beetle’s fecundity and egg viability are significantly reduced by temperature variations below or above optimal (Omkar et al. Reference Omkar, Rastogi and Pandey2009). Although the majority of studies on this beetle have assessed its reproductive performance under constant optimal or sub-optimal temperature conditions (e.g., Omkar et al. Reference Omkar, Rastogi and Pandey2009; Patel et al. Reference Patel, Bhusal, Kumar and Kumar2020), no previous study has been conducted to determine the effect of fluctuating temperature conditions on the beetle’s reproductive parameters.

Because insects do not always encounter optimal temperature throughout their life, their performance under changing temperature conditions cannot be predicted accurately when provided with a constant temperature under laboratory conditions (Worner Reference Worner1992). For the present study, we hypothesised that repeated short-term thermal stress conditions would reduce the reproductive parameters and decrease the survival rate of the beetle. The results of the study will improve our understanding of the short- and long-term adaptation abilities of insects for reproductive fitness and survival under global climate change scenarios.

Materials and methods

Insect species

In our study, we used Z. bicolorata as our experimental model. This beetle is an effective biocontrol agent for Parthenium hysterophorus Linnaeus (Asteraceae), an alien invasive herbaceous weed with pantropic distribution. The weed adversely affects grazing land productivity and native biodiversity and causes naso-branchial allergy in humans. Zygogramma bicolorata was first introduced to Australia from Mexico in 1980 (McFadyen and McClay Reference McFadyen and McClay1981). Parthenium weed control efforts in India using this beetle were initiated in 1983 (Jayanth and Nagarkatti Reference Jayanth and Nagarkatti1987). Feeding by Z. bicolorata negatively affects P. hysterophorus under field conditions (Dhileepan et al. Reference Dhileepan, Setter and Mcfadyen2000), prompting great interest in the use of this beetle for biological control of P. hysterophorus (Patel et al. Reference Patel, Bhusal, Kumar and Kumar2020).

Insect rearing

Adult males and females (n = 50: ♀ = 22; ♂ = 28) of Z. bicolorata were collected from agricultural fields of Varanasi, India (25° 20’ N, 83° 0’ E) during October–November and randomly paired in plastic Petri dishes (140-mm diameter × 16-mm height; Tarsons, India) under constant abiotic conditions (27 ± 2 °C; 65 ± 5% relative humidity; 12:12 light:dark photoperiod) in a biological oxygen demand incubator (NSW 152, New Delhi, India). The adult beetles received fresh P. hysterophorus leaves daily. The beetles were allowed to mate, and eggs (observable through the naked eye) were collected every 24 hours. The eggs (n = 400) were kept in the incubators under the above-mentioned abiotic conditions and were observed for hatching, and the requisite stages were reared with a daily replenished supply of fresh P. hysterophorus leaves. First-generation (F1) adult male (n = 150) and female (n = 150) beetles were separated, based on the posterior margin of their last visible abdominal ventrite, which is whole in females. In males, the tip of the posterior margin is slightly serrated, and their last abdominal ventrite has a faint depression at the centre (Patel et al. Reference Patel, Bhusal, Kumar and Kumar2020). The F1 adults were used for further experimentation.

Heat and cold treatments followed by the recovery phase

To induce heat or cold stress in Z. bicolorata adults, exposing them to a range of temperatures that ensures their survival while inducing a certain level of stress is crucial. When working with brief exposures to extreme temperatures, it is essential to consider the variability in the insect’s response and to adjust the temperature accordingly (Goller and Esch Reference Goller and Esch1990). In Indian agroecosystems, the temperature range of 25–30 °C is considered optimal for Z. bicolorata (Patel et al. Reference Patel, Bhusal, Kumar and Kumar2020): we therefore selected 27 ± 2 °C as the optimal temperature for our experiments. Larvae of Z. bicolorata do not complete their development at temperatures below 15 °C, and at temperatures above 40 °C, both larvae and adults exhibit frequent mortality (Chidawanyika et al. Reference Chidawanyika, Nyamukondiwa, Strathie and Fischer2017; Patel et al. Reference Patel, Bhusal, Kumar and Kumar2020). We therefore opted for a temperature range of 10 ± 2 °C as the cold stress temperature and 42 ± 2 °C as the heat stress temperature in the present study.

Considering the above conditions, the newly emerged F1 adults of Z. bicolorata reared at 27 ± 2 °C (control, or optimal temperature) were divided into three groups, each consisting of 40 mating pairs. During every 24-hour period, adult males and females of group A (one male and one female in each Petri dish) were exposed to a temperature of 42 ± 2 °C (heat stress group), whereas pairs of group B were exposed to a temperature of 10 ± 2 °C (cold stress group) in the biological oxygen demand incubators for one hour. Subsequently, for the next 23 hours, the adults (kept as one mating pair per Petri dish) of both groups were returned to the optimal temperature of 27 ± 2 °C and were fed fresh P. hysterophorus leaves daily. This process was repeated daily for the next 10 days. However, beginning on the eleventh day and continuing until the end of their lifespans, the mating pairs of both group A and group B were kept under the optimal temperature to allow recovery from the earlier temperature stress.

The control group (consisting of 40 mating pairs) remained at the optimal temperature (27 ± 2 °C) from the day of their emergence throughout their lifespan.

Reproductive and survival parameters of females

Fecundity and egg viability serve as crucial fitness indicators for Z. bicolorata adults (Omkar and Afaq Reference Omkar and Afaq2013; Patel et al. Reference Patel, Bhusal, Kumar and Kumar2020). Omkar et al. (Reference Omkar, Rastogi and Pandey2009) reported previously that the egg viability of the beetle is between 65 and 68% at temperatures of 25–30 °C. In the present study, once females began laying eggs in both the experimental and control groups, 20 mating pairs from each group were selected to assess their reproductive and survival parameters. Each mating pair was placed in a plastic Petri dish with fresh P. hysterophorus leaves that were replenished daily. The Petri dishes were checked daily for egg-laying by the females, and eggs laid were examined daily for hatching. The number of eggs laid by the female each day was recorded to determine the daily fecundity (= daily oviposition) parameter. Lifetime fecundity for each female was calculated as the cumulative number of eggs laid by a female over its entire lifespan (Sampaio et al. Reference Sampaio, Batista and Marchioro2024). Eggs were considered viable if larvae hatched, and the numbers of viable eggs were recorded. Daily egg viability (%) was calculated as the percentage of hatched eggs to the total number of eggs laid by the female per day. Lifetime egg viability (%) for each female was calculated as the percentage of hatched eggs to the total number of eggs laid by the female during her lifetime.

Ovipositing females within each experimental and control group were categorised into three age groups – young (less than 25 days), middle aged (25–50 days), and old (more than 50 days). This age-based categorisation of Z. bicolorata females aligns with the approach used by Pandey and Omkar (Reference Pandey and Omkar2013) in their experiments. We quantified the pre-oviposition period (the time between reaching adulthood and the onset of oviposition), oviposition period, and post-oviposition period (the time between the last egg laid and death), following Rahmani et al.’s (Reference Rahmani, Fathipour and Kamali2009) methodology. We also assessed the survivability of the females within the mating pairs according to experimental and control group.

Statistical analyses

We assessed the homogeneity of group variances in the experimental data using Levene’s test and checked for normality through the Kolmogorov–Smirnov test. To analyse the pre-oviposition, oviposition, and post-oviposition periods (the dependent variables) of the females, we conducted one-way analysis of variance, followed by Tukey’s comparison of means, with the different treatment conditions (short-term cold stress, short-term heat stress, or optimal condition) as independent variables. The daily fecundity and egg viability parameters (dependent variables) underwent analysis of co-variance (generalised mixed linear model), followed by Tukey’s post-hoc comparison of means. In these latter post-hoc analyses, treatment condition served as an independent random variable, and the age of the females was a covariate.

The lifetime-fecundity and egg-viability parameters for each age group (young, middle aged, or old) under the three experimental conditions were analysed using repeated measures analysis of variance (two-way). The independent variables in these analyses were treatment condition and age group, whereas lifetime fecundity and lifetime egg viability were dependent variables. Bonferroni’s multiple comparison of means was conducted after the analysis of variance. Before analysis of co-variance or repeated measures analysis of variance, all percent data on egg viability underwent arcsine square-root transformation. Graphs of age-based fecundity and egg viability were extrapolated using polynomial regression equations. The statistical analysis was performed using MINITAB 18 (MINITAB Inc., University Park, Pennsylvania, United States of America).

To analyse survival, we employed the Kaplan–Meier estimator with the log-rank (Mantel–Cox) test amongst the groups (cold stress, heat stress, or optimal condition). We investigated the chance of survival in a population by following 20 females from each group. The data were analysed using GraphPad Prism 8.4.2 (GraphPad Software Inc., La Jolla, California, United States of America).

Results

The one-way analysis of variance revealed that the pre-oviposition, oviposition, and post-oviposition periods of Z. bicolorata females were affected significantly by the different treatment conditions (F = 67.19, P < 0.0001, df = 2). Comparison of means further indicated that the pre-oviposition periods were shortest when females experienced either repeated short-term heat stress (STH) conditions or were kept at the optimal temperature. In contrast, the pre-oviposition periods were longest when females experienced repeated short-term cold stress (STC) conditions. Although the oviposition periods were shortest under STH conditions, the post-oviposition periods were the shortest under both STH and STC conditions. Both the oviposition and post-oviposition periods were the longest at the optimal temperature (Fig. 1).

Figure 1.

Effects of repeated short-term cold stress (STC), repeated short-term heat stress (STH), and optimal temperature (control) on pre-oviposition, oviposition, and post-oviposition periods of Zygogramma bicolorata. Values are mean ± standard error; small letters represent comparison of means amongst the three temperature conditions.

Analysis of co-variance values further revealed significant effects of the different treatment conditions and the age (covariate) of females on daily fecundity (F = 10.56, P < 0.0001, df = 2 and F = 2645.51, P < 0.0001, df =1, respectively) and daily egg viability (F = 6.01, P = 0.002, df = 2 and F = 791.30, P < 0.0001, df =1, respectively). Comparison of means further revealed that the daily fecundity and daily egg viability of females increased with age, reaching a peak and thereafter declining as the females further aged (Fig. 2). Figure 2A illustrates the age-specific fecundity plots of Z. bicolorata females under varying thermal stress conditions. The polynomial-regression graph depicts trends in peak oviposition and the day of peak oviposition across thermal-stress and optimal conditions. Under both thermal-stress conditions and optimal temperatures, age-specific fecundity trends (eggs per day versus age) exhibited a triangular pattern. Females kept under optimal and STH conditions started ovipositing on day 7. These females also experienced their oviposition peaks at early ages (between 15 and 25 days after emergence). In contrast, females kept under STC conditions began ovipositing on day 11. These females achieved their oviposition peaks during their middle age (between 25 and 35 days). The peaks of oviposition were relatively higher in females that experienced STH conditions compared to females that had been maintained at optimal temperatures; females kept under STC conditions showed the lowest oviposition peaks.

Figure 2.

Effects of repeated short-term cold stress (STC), repeated short-term heat stress (STH), and optimal temperature (control) on A, age-specific fecundity and B, age-specific egg viability of Zygogramma bicolorata. Values are mean ± standard error; the lines based on polynomial regression analysis show triangular/plateau-shaped patterns.

The polynomial-regression graphs for age-specific egg viability exhibited plateau-shaped patterns, with the peak in egg-viability occurring at early ages (15–25 days after emergence) under both optimal and STH conditions and at middle age (30–40 days after emergence) under STC conditions (Fig. 2B).

Two-way repeated measures analysis of variance further revealed nonsignificant effects of the different treatment conditions on the females’ lifetime fecundity (F = 0.80, P = 0.509, df = 2) and lifetime egg viability (F = 0.19, P = 0.834, df = 2). However, both age and the interaction between the two independent factors significantly influenced lifetime fecundity (F = 38.01, P = 0.002, df = 2 and F = 45.33, P < 0.0001, df = 4) and lifetime egg viability (F = 22.18, P = 0.007, df = 2 and F = 17.28, P < 0.0001, df = 4). Despite being maintained at the optimal temperature or kept under repeated thermal-stress conditions, middle-aged Z. bicolorata females exhibited the highest lifetime fecundity and egg viability parameters, followed by young females. Old females had the lowest lifetime fecundity and egg viability parameters when kept regardless of treatment condition or control (Fig. 3). However, amongst the three temperature conditions, life-time fecundity was highest in females maintained at the optimal temperature and lowest in females subjected to STH conditions. In contrast, life-time egg viability was highest in females subjected to either STH or STC and lowest in females maintained at the optimal temperature (Fig. 4A).

Figure 3.

Effects of repeated short-term cold stress (STC), repeated short-term heat stress (STH), and optimal temperature (control) on A, lifetime fecundity and B, lifetime egg viability of young, middle-aged, and old females of Zygogramma bicolorata. Values are mean ± standard error; small letters represent comparison of means amongst the three age groups per temperature condition.

Figure 4.

Effects of repeated short-term cold stress (STC), repeated short-term heat stress (STH), and optimal temperature (control) on A, lifetime fecundity and lifetime egg viability, and B, female survival curves of Zygogramma bicolorata adults. Values are mean ± standard error; small letters represent comparison of means amongst the three temperature conditions.

Thermal-stress conditions significantly decreased females’ longevity compared to that of females maintained at the optimal temperature (Fig. 4B). Survival curve comparisons using the log-rank (Mantel–Cox) test (χ2 = 26.60, P < 0.0001, df = 2) and the Gehan–Breslow–Wilcoxon test (χ2 = 12.76, P = 0.0017, df = 2) revealed a significant effect of repeated thermal stress conditions on female survival. Maximum survival was recorded in females that had been maintained at the optimal temperature (∼131 days), with females kept under STC conditions and those kept under STH conditions surviving for approximately 107 days and approximately 82 days, respectively, in comparison.

Discussion

Insects usually encounter various abiotic challenges to survival and reproduction, with temperature being among the major abiotic factors that cause physiological changes (Jia et al. Reference Jia, Dou, Hu and Wang2011). Although fitness encompasses both survival and reproduction, reproductive success is almost as important as individual survival is within insect populations (Marshall and Sinclair Reference Marshall and Sinclair2012). Compensatory mechanisms can restore all functions throughout the lifespan of insects, provided that stressful conditions are not encountered during the earlier life stages (Zhang et al. Reference Zhang, Chang, Hoffmann, Zhang and Ma2015). In the present study, Darwinian fitness is affected by both repeated short-term cold-stress conditions and repeated short-term heat-stress conditions. Pre-oviposition periods were shortest and oviposition and post-oviposition periods were longest when Z. bicolorata females were maintained at the optimal temperature. A reason why the shorter pre-oviposition periods occurred at the optimal temperature may have been because the warmer conditions might accelerate gonadal maturation in Z. bicolorata females. Rapid maturation leads to earlier egg-laying and prolonged oviposition periods (Omkar et al. Reference Omkar, Rastogi and Pandey2009; Saha et al. Reference Saha, Bangadkar and Raja2015; Bali et al. Reference Bali, Gupta, Pervez, Guroo, Gupta and Gani2022). In addition, the beetles’ overall health at the optimal temperature may contribute to a longer post-oviposition period. Our findings are consistent with those of Pervez and Omkar (Reference Pervez and Omkar2004), Jalali et al. (Reference Jalali, Tirry and De Clercq2009), Sarkar and Barik (Reference Sarkar and Barik2017), Lee et al. (Reference Lee, Baek, Kang, Lee, Lee and Lee2018), and Huang et al. (Reference Huang, Gu, Peng, Tao, Chen and Zhang2020) in other insect species.

The shortened pre-oviposition, oviposition, and post-oviposition periods observed in the present study under repeated short-term heat-stress conditions may reflect the adverse effects of high temperatures on gonadal maturation (Wang et al. Reference Wang, Gordon and Rainwater2008). Paul and Keshan (Reference Paul and Keshan2016), Huang et al. (Reference Huang, Gu, Peng, Tao, Chen and Zhang2020), and Sales et al. (Reference Sales, Vasudeva and Gage2021) reported suppression of ovarian maturation and impaired development of gonads at high temperatures in insects in their studies. The extended pre-oviposition periods observed in the present study when females were subjected to repeated short-term cold-stress conditions may be attributed to the reduced metabolic activity at lower temperatures, which could result in slower gonad maturation (Yu et al. Reference Yu, Zhao, Zhou, Pan, Tian, Yin and Chen2022). Previous studies have described a linear relationship between temperature and the rate of gonadal maturation in insects (Phoofolo et al. Reference Phoofolo, Obrycki and Krafsur1995; Nobuhiro Reference Nobuhiro2002; Blanckenhorn and Henseler Reference Blanckenhorn and Henseler2005). The shortened post-oviposition periods observed in the present study in females under repeated short-term cold-stress conditions are consistent with the findings of Augustine and Shera (Reference Augustine and Shera2024) for Fulgoraecia melanoleuca (Fletcher) (Lepidoptera: Epipyropidae). Contrary to our findings, Omkar et al. (Reference Omkar, Rastogi and Pandey2009) and Glatz et al. (Reference Glatz, Du Plessis and Van den Berg2017) reported increased post-oviposition periods under cold-stress conditions in females of Z. bicolorata and Busseola fusca (Lepidoptera: Noctuidae), respectively. However, Bali et al. (Reference Bali, Gupta, Pervez, Guroo, Gupta and Gani2022) reported no variations in the post-oviposition periods of field-collected Z. bicolorata females from the colder and hotter regions of the Indian subcontinent.

In the present study, age-specific fecundity curves exhibited a triangular shape and age-specific egg viability curves displayed a plateau shape under varying temperature conditions. Both daily fecundity and egg viability of females increased with age, reaching a peak or slope, and subsequently declined with further advancement in age. The reduced fecundity and egg viability observed in females during their very early ages may be attributed to the process of attaining sexual maturity. However, the increased fecundity observed with age, from early to middle ages, can likely be attributed to a higher number of mature ova compared to females in their later stages of life (Obata Reference Obata1988). The decline in egg production in later stages of life may be associated with reduced food consumption and nutrient assimilation, as well as decreased speed of locomotion and fertility (Dixon and Agarwala Reference Dixon and Agarwala2002). Our present results align with those reported earlier in coccinellid beetles (Omkar et al. Reference Omkar, Singh, Pervez and Mishra2004; Pervez et al. Reference Pervez, Omkar and Richmond2004; Jafari et al. Reference Jafari, Aghdam, Zamani, Goldasteh, Soleyman-Nejadian and Schausberger2023). Omkar et al. (Reference Omkar, Pandey, Rastogi and Mishra2010) and Sampaio et al. (Reference Sampaio, Batista and Marchioro2024) also reported triangular and temperature-dependent age-specific fecundity curves in chrysomelid beetles (Coleoptera: Chrysomelidae) and southern armyworms (Lepidoptera: Noctuidae), respectively.

The occurrence of peak oviposition at an early age in females subjected to repeated short-term heat stress conditions suggests that heat stress may induce adults to lay eggs as early as possible to avoid adverse effects later in life (Javoiš and Tammaru Reference Javoiš and Tammaru2004; Xing et al. Reference Xing, Hoffmann, Zhao and Ma2019). We also observed the peak of oviposition occurring early in adult life when females were maintained at the optimal temperature, which aligns with the findings of Omkar et al. (Reference Omkar, Rastogi and Pandey2009) in Z. bicolorata. In coccinellid beetles, Pervez and Omkar (Reference Pervez and Omkar2004) reported the peak of oviposition occurring early in adult life with increasing temperature, while also noting the highest rate of oviposition at the optimal temperature. However, females subjected to repeated short-term cold stress conditions achieved their oviposition peaks at middle-ages, possibly due to their long pre-oviposition periods resulting from the slower maturation of gonads at colder temperatures (Blanckenhorn and Henseler Reference Blanckenhorn and Henseler2005).

In the present study, the increased fecundity in middle-aged females may be attributed to a higher number of mature ova compared to younger and older females (Obata Reference Obata1988). Young males likely transfer significantly lower quantities of sperm, and old males possibly transfer less sperm than males of middle-ages (Hale et al. Reference Hale, Elgar and Jones2008). Moreover, the lower fecundity of older females may be due to the onset of senescence (Moore and Moore Reference Moore and Moore2001), causing a reduction in oogenesis. Our present results are consistent with those reported earlier in chrysomelid beetles (Omkar et al. Reference Omkar, Pandey, Rastogi and Mishra2010; Pandey and Omkar Reference Pandey and Omkar2013) and coccinellid beetles (Pervez et al. Reference Pervez, Omkar and Richmond2004; Omkar et al. Reference Omkar, Singh and Singh2006; Singh and Omkar Reference Singh and Omkar2009).

The reduced lifetime fecundity observed in females exposed to repeated short-term thermal stress in the present study is likely due to several factors: (1) low oogenesis rates at low temperatures (Huey et al. Reference Huey, Wakefield and Gilchrist1995); (2) fewer ovarioles at high temperatures (Mironidis and Savopoulou-Soultani Reference Mironidis and Savopoulou-Soultani2010); (3) less efficient food use (Veeravel and Baskaran Reference Veeravel and Baskaran1997); and (4) a potential trade-off between temperature acclimation and reproductive output (Xing and Zhao Reference Xing and Zhao2022). In addition, the shortened oviposition period and increased energy expenditure from elevated heat-shock protein expression under heat stress (Huang et al. Reference Huang, Chen and Kang2007; Tomanek and Zuzow Reference Tomanek and Zuzow2010; Gu et al. Reference Gu, Li, Wang and Liu2019; Xing and Zhao Reference Xing and Zhao2022) may have further contributed to the reduced overall fecundity that we observed. Our results closely agree with the findings of Marshall and Sinclair (Reference Marshall and Sinclair2010), who observed decreased fecundity in the common fruitfly, Drosophila melanogaster Meigen (Diptera: Drosophilidae), after repeated exposure to thermal-stress conditions.

The increased lifetime egg viability that we observed under repeated thermal stress conditions compared to the optimal temperature may be a strategy employed by females to accelerate spawning under adverse conditions, thereby maximising fitness before further deterioration and preventing damage later in the life cycle (Xing and Zhao Reference Xing and Zhao2022). In Bicyclus anynana butterflies (Lepidoptera: Nymphalidae), eggs produced at lower temperatures showed greater viability than those produced under the optimal temperature (Fischer et al. Reference Fischer, Eenhoorn, Bot, Brakefield and Zwaan2003). Contrary to our findings, many previous studies have reported decreased egg viability of females under thermal-stress conditions (Baur et al. Reference Baur, Jagusch, Michalak, Koppik and Berger2022; Ormanoğlu et al. Reference Ormanoğlu, Baliota, Rumbos and Athanassiou2023; Vasudeva Reference Vasudeva2023; Huang et al. Reference Huang, McPherson, Jiggins and Montejo-Kovacevich2024).

In the present study, the shortest lifespan of females was observed in females subjected to repeated short-term heat-stress conditions, followed by females subjected to repeated short-term cold-stress conditions. In unfavourable-temperature environments, insects allocate high levels of energy to metabolism, reproduction, and other life activities, resulting in decreased adult longevity (Jervis et al. Reference Jervis, Boggs and Ferns2005). Increased lipid peroxidation and, consequently, extended periods of high metabolic rates under thermal-stress conditions may lead to early death in females due to energy depletion (Storey and Storey Reference Storey and Storey2004). Our present results align with those of Li et al. (Reference Li, Li, Guo and Shang2021), who found that short-term heat-stress conditions negatively affected the fecundity, oviposition period, and longevity of adult females of Neoseiulus barkeri (Acari: Phytoseiidae). Similarly, the survival rate, longevity, and reproduction of adult Myzus persicae (Hemiptera: Aphididae) decreased after exposure to short-term high temperatures (Fan et al. Reference Fan, Chen, Sun, Tang, Wang, Ren and Wang2014). Similarly, the oviposition periods and longevity of Bactrocera tau (Diptera: Tephritidae) females were shortened after exposure to short-term high-temperature conditions (Huang et al. Reference Huang, Gu, Peng, Tao, Chen and Zhang2020).

In summary, the present study reveals how variable temperatures impact Z. bicolorata, a biocontrol agent for parthenium weed. Repeated short-term thermal stress can enhance egg viability but may lead to earlier and higher oviposition peaks. In contrast, optimal temperatures maximise female fecundity and longevity. The findings highlight the need to consider temperature variability in biocontrol research. Maintaining optimal temperatures is key for long-term biocontrol effectiveness, and fluctuating conditions can be used to boost short-term reproductive output. Future research should simulate natural temperature fluctuations, investigate stress adaptation across generations, and assess how reproductive timing influences biocontrol effectiveness. Predictive models and field trials should incorporate these variables to maximise biocontrol strategies. In addition, we suggest that future studies also explore how body size, temperature, and age relate to egg viability and reproductive success.

The present study’s findings also suggest that thermal stress, whether below or above the optimal range and even if such stress occurs only for a short time or occasionally, can significantly modulate the reproductive performance of insects and their ability to survive. Averaging daily temperatures may not adequately account for these effects because average performance over a range of temperatures may differ from performance at the average temperature within that range (Jensen’s inequality function; Jensen Reference Jensen1906; Martin and Huey Reference Martin and Huey2008). Although why modulation in reproductive output occurs after exposure to stressful temperatures is reasonably understandable, whether these distinct processes exhibit varying thresholds or reactions to these temperature stresses remains uncertain. The mechanisms underlying increased reproductive investment under fluctuating temperatures may be simple or may involve complex signalling pathways (Terblanche et al. Reference Terblanche, Nyamukondiwa and Kleynhans2010). These unknowns also should be prioritised as a subject for future research.

Acknowledgements

The authors thank UGC-CAS and DST-FIST supported Department of Zoology, Banaras Hindu University, Varanasi for laboratory facilities. Arvind Kumar Patel acknowledges CSIR, New Delhi, for JRF and SRF Fellowships. Bhupendra Kumar acknowledges IoE-Incentive (Phase-IV) and Trans-disciplinary grants, Banaras Hindu University, for financial assistance.

Competing interests

The authors declare that they have no competing interests.

Footnotes

Subject editor: Katie Marshall

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Figure 1.Effects of repeated short-term cold stress (STC), repeated short-term heat stress (STH), and optimal temperature (control) on pre-oviposition, oviposition, and post-oviposition periods of Zygogramma bicolorata. Values are mean ± standard error; small letters represent comparison of means amongst the three temperature conditions.

Figure 1

Figure 2.Effects of repeated short-term cold stress (STC), repeated short-term heat stress (STH), and optimal temperature (control) on A, age-specific fecundity and B, age-specific egg viability of Zygogramma bicolorata. Values are mean ± standard error; the lines based on polynomial regression analysis show triangular/plateau-shaped patterns.

Figure 2

Figure 3.Effects of repeated short-term cold stress (STC), repeated short-term heat stress (STH), and optimal temperature (control) on A, lifetime fecundity and B, lifetime egg viability of young, middle-aged, and old females of Zygogramma bicolorata. Values are mean ± standard error; small letters represent comparison of means amongst the three age groups per temperature condition.

Figure 3

Figure 4.Effects of repeated short-term cold stress (STC), repeated short-term heat stress (STH), and optimal temperature (control) on A, lifetime fecundity and lifetime egg viability, and B, female survival curves of Zygogramma bicolorata adults. Values are mean ± standard error; small letters represent comparison of means amongst the three temperature conditions.