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. 2024 Mar 5;24(2):2. doi: 10.1093/jisesa/ieae025

Effects of photoperiod and temperature on the developmental duration and diapause in Dolycoris baccarum (Heteroptera: Pentatomidae) from Hohhot, Inner Mongolia, China

Ruilin Tian 1,2,✉, Zhanming Hou 3, Song Li 4,5, Hua Chai 6
Editor: John Ewer
PMCID: PMC10914362  PMID: 38442351

Abstract

The shield bug, Dolycoris baccarum (L.) (Heteroptera: Pentatomidae), is widely distributed across Asia and Europe. At high latitudes, it overwinters, as adult in diapause, which then becomes the insect source for the following year. To fully understand the developmental duration and diapause characteristics of D. baccarum, the effects of photoperiod and temperature were studied in a population from Hohhot, Inner Mongolia, China. The results indicated that the developmental duration was significantly prolonged at temperatures of 20 or 25 °C, with a prolonged light period; however, when the light period was prolonged to 16L:8D and 18L:6D, the developmental duration was shortened significantly. Furthermore, the developmental duration was also shortened significantly with increasing temperature, when the photoperiod was 12L:12D for short days and 16L:8D for long days. All individuals entered diapause under short-day conditions of 10L:14D and 12L:12D at a temperature of 20 °C; however, the diapause rate decreased significantly under 14L:10D and 16L:8D photoperiods, and the diapause rate decreased significantly at a temperature of 25 °C with prolonged photoperiod. Interestingly, when the photoperiod was fixed at 12L:12D, the diapause rates at different temperatures (20, 25, 28, and 30 °C) exceeded 95%; while the effect of temperature on diapauses was nonsignificant under this photoperiod, it was still sensitive to the photoperiod; at a photoperiod of 16L:8D, the effect of temperature on the diapause rate was noticeable, and the diapause rate decreased significantly with increasing temperature.

Keywords: Dolycoris baccarum, Pentatomidae, adult diapause, developmental duration

Introduction

Shield bugs (Heteroptera: Pentatomidae) are widely distributed in the Old World; most species of them are phytophagous, feeding on a variety of plants. Investigation on life history of shield bugs till now found that most species of them overwinter in diapause as adults (Hodek and Hodkova 1993, Šlachta et al. 2002, Santos et al. 2003, Robert et al. 2021). Dolycoris baccarum (L.) (Heteroptera: Pentatomidae) is widely distributed throughout the Asian and European continents, where it feeds on many species of plants and harms numerous crops, such as soybeans, cotton, sesame, carrots, burdock, wheat, tobacco, and rice (Fent and Aktaç 1999, Tsagkarakis et al. 2022). In China, it is widely distributed from provinces in the south to Inner Mongolia, Xinjiang, and Heilongjiang in the north (Sachurula et al. 2022).

In northern China, D. baccarum overwinter as adults in rock crevices or under the leaf litter. The overwintering generation of adults is viable only when it enters diapause; it reproduces the next generation in the following spring after the diapause has been terminated. Dolycoris baccarum is a widely distributed species, and the diapause conditions and developmental duration of geographical populations differ between various distribution areas.

Since the 1950s, European scholars have carried out research on the life history and environmental adaptation of European populations of D. baccarum, mainly examining populations found in the Czech Republic, Slovakia, Norway, and Russia (Hodek 1977, Conradi-Larsen and Sømme 1978, Hodek and Hodkova 1993). In the Krasnodar territory of Russia, multiple generations can be produced per year, while in Novosibirsk in Russia and southern Norway (which are both located at higher latitudes), only one generation is produced per year (Hodkova et al. 1989). Japanese scholars have studied the characteristics of the development and diapause of Hokkaido and Osaka populations (Nakamura 2003, Nakamura and Numata 2006). While D. baccarum is also widely distributed in China, the developmental duration and diapause characteristics of populations in various parts of China have not been comprehensively studied to date.

Based on the successful rearing of D. baccarum in an incubator and by controlling the photoperiod, temperature, and other conditions, the developmental duration and the diapause characteristics of a D. baccarum population from Hohhot, Inner Mongolia, China, were examined to study the effects of photoperiod and temperature on the developmental duration and diapause of D. baccarum. This study provides not only basic data on the D. baccarum distribution at high latitudes but also a theoretical basis for predicting the occurrence of D. baccarum in this area.

Materials and Methods

Insects for Experiments

In May 2021, adults of D. baccarum were collected from Daqing Mountain (111.2°E, 40.7°N) in Hohhot, Inner Mongolia, China, and were incubated in an illuminated incubator (Boxun BXG-250, Boxun Medical Biological Instrument Corp., Shanghai, China) under a temperature condition of 25 ± 0.7 °C and a 16L:8D light cycle. The adults were fed with raw peanuts and distilled water absorbed by absorbent cotton (Sachurula et al. 2022). After spawning, egg masses were collected for experiments. The eggs were hatched and reared individually in single feeding bottles (transparent plastic bottles with a diameter:height ratio of 3.5:3.5 cm). Their instar was determined according to the width of the pronotum and their molting (Sachurula et al. 2022).

Effects of the Photoperiod on the Developmental Duration

In order to observe the developmental duration, the temperature was set to 20 ± 0.5 °C combined with 4 types of photoperiods: 10L:14D, 12L:12D, 14L:10D, and 16L:8D; the temperature was set to 25 ± 0.7 °C combined with 6 types of photoperiods: 12L:12D, 13L:11D, 14L:10D, 15L:9D, 16L:8D, and 18L:6D. For each temperature and corresponding light treatment condition, no less than 40 eggs that were laid on the same day were taken and transferred into single feeding bottles for individual feeding after hatching. The developmental duration of each stage from egg hatching to adult insect was recorded, and males and females were identified after they became adults. Each treatment was repeated three times, and individuals that died during the nymphal stage were excluded from the statistical analysis. Considering that 25 °C is close to the summer temperature in the examined region, the long-day photoperiod setting was used for 2 more cycles than under 20 °C.

Effects of Temperature on the Developmental Duration

The photoperiod and temperature condition were set as follows: 2 patterns of photoperiod like 12L:12D and 16L:8D combined, respectively, with 4 kinds of temperatures like 20 ± 0.5, 25 ± 0.7, 28 ± 0.7, and 30 ± 0.9 °C for each pattern of photoperiod. Under each combination of photoperiod and temperature conditions, no less than 40 eggs were taken and transferred into single feeding bottles for individual feeding after hatching. The developmental duration of each developmental stage (from egg hatching to adult insect) was recorded, and males and females were identified after they became adults. Each treatment was repeated 3 times.

Effects of Photoperiod on Diapause

Temperatures were set to 20 and 25 °C, and different photoperiods from short day to long day were set for each temperature. Four types of photoperiods (10L:14D, 12L:12D, 14L:10D, and 16L:8D) were set at 20 °C, and 6 types of photoperiods (12L:12D, 13L:11D, 14L:10D, 15L:9D, 16L:8D, and 18L:6D) were set at 25 °C. No less than 40 eggs produced on the same day were taken for each combination, and individual feeding was carried out after hatching. Males and females were identified within 30 days after maturation, following the methods described by Hodek (1971, 1977). The method of Nakamura and Numata (2006) was used to identify whether the adult had entered diapause or not. Each treatment was repeated 3 times, and individuals that had died during the nymphal stage were excluded from statistical analysis.

Effects of Temperature on Diapause

Photoperiods were set to 12L:12D and 16L:8D, and different temperatures (20 ± 0.5, 25 ± 0.7, 28 ± 0.7, and 30 ± 0.9 °C) were set for each photoperiodic condition. The method was the same as the experiment mentioned above. Each treatment was repeated 3 times.

Statistical Analysis

One-way analysis of variance (calculated in SPSS 20.0) was used for the analysis of variance, and Tukey tests were used to test the significance. Multiple comparison analysis was carried out to compare the level of differences among all treatments.

Results

Effects of the Photoperiod on the Developmental Duration

The insects grew and developed normally under a temperature of 20 °C and photoperiods of 10L:14D, 12L:12D, 14L:10D, and 16L:8D. As the photoperiod changed from short day to long day, the developmental duration tended to be prolonged (F = 4.781; df = 3, df = 193; P = 0.003 [♀] and F = 5.85; df = 3; df = 163, P = 0.001 [♂]) (Fig. 1). Under a temperature of 25 °C and photoperiods of 12L:12D, 13L:11D, 14L:10D, and 15L:9D, the developmental duration was prolonged with extended light exposure (F = 15.315; df = 5, df = 304; P = 0.001 [♀] and F = 8.723; df = 5; df = 247, P = 0.001 [♂]); when the photoperiod was extended to 16L:8D and 18L:6D, the developmental duration presented a shortening trend (Fig. 1).

Fig. 1.

Fig. 1.

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Developmental duration of Dolycoris baccarum at different photoperiods under 20 and 25 °C. Data show means ± SE. Different letters indicate significant differences (P < 0.01). 20 °C: 10L:14D, n = 48 ♀, 43 ♂; 12L:12D, n = 46 ♀, 45 ♂; 14L:10D, n = 60 ♀, 36 ♂; 16L:8D, n = 42 ♀, 42 ♂. 25 °C: 12L:12D, n = 53 ♀, 42 ♂; 13L:11D, n = 50 ♀, 45 ♂; 14L:10D, n = 44 ♀, 40 ♂; 15L:9D, n = 55 ♀, 47 ♂; 16L:8D, n = 54 ♀, 36 ♂; 18L:6D, n = 54 ♀, 42 ♂.

Effects of the Temperature on the Developmental Duration

Under photoperiods of 12L:12D and 16L:8D, with increasing temperature, the developmental duration of each instar was significantly shortened (12L: F = 2,457.692; df = 3, df = 205; P = 0.001 [♀] and F = 2,556.018; df = 3; df = 180, P = 0.001 [♂]; 16L: F = 7,929.023; df = 3, df = 198; P = 0.001 [♀] and F = 4,183.620; df = 3; df = 185, P = 0.001 [♂]) (Fig. 2).

Fig. 2.

Fig. 2.

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Developmental duration of Dolycoris baccarum at different temperatures under 12L:12D and 16L:8D. Data show means ± SE. The different letters indicate significant differences (P < 0.01). 12L:12D: 20 °C, n = 46 ♀, 45 ♂; 25 °C, n = 53 ♀, 42 ♂; 28 °C, n = 58 ♀, 57 ♂; 30 °C, n = 51 ♀, 39 ♂. 16L:8D: 20 °C, n = 42 ♀, 42 ♂; 25 °C, n = 54 ♀, 36 ♂; 28 °C, n = 52 ♀, 63 ♂; 30 °C, n = 53 ♀, 47 ♂.

Effects of Photoperiod on Diapause

The diapause rate was 100% at 20 °C and under short-day photoperiods of 10L:14D and 12L:12D. When the photoperiod was set to 14L:10D and 16L:8D, the diapause rate decreased significantly, which was more evident under prolonged photoperiods (F = 103.291; df = 3, df = 8; P = 0.001 [♀] and F = 187.494; df = 3; df = 8, P = 0.01 [♂]) (Fig. 3).

Fig. 3.

Fig. 3.

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The effect of photoperiod on diapause induction in Dolycoris baccarum under 20 and 25 °C. Data show means ± SE. Different letters indicate the significance of the diapause rate under different photoperiods (P < 0.01). 20 °C: 10L:14D, n = 48 ♀, 43 ♂; 12L:12D, n = 46 ♀, 45 ♂; 14L:10D, n = 60 ♀, 36 ♂; 16L:8D, n = 42 ♀, 42 ♂. 25 °C: 12L:12D, n = 53 ♀, 42 ♂; 13L:11D, n = 50 ♀, 45 ♂; 14L:10D, n = 44 ♀, 40 ♂; 15L:9D, n = 55 ♀, 47 ♂; 16L:8D, n = 54 ♀, 36 ♂; 18L:6D, n = 54 ♀, 42 ♂.

At 25 °C, the diapause rate decreased significantly with prolonged photoperiod (F = 31.367; df = 5, df = 12; P = 0.01 [♀] and F = 56.861; df = 5; df = 12, P = 0.001 [♂]). The diapause rate was high under the short-day condition of 12L:12D, but it was very low under the long-day condition of 18L:6D (Fig. 3). This result differed from that of the 12L:12D light cycle at 20 °C, as some individuals were still not in diapause at 25 °C.

Effects of Temperature on Diapause

Under the short-day condition of 12L:12D, the diapause rate at 20 °C reached 100%; while the diapause rates at other temperatures were also very high, no significant differences were found compared with that observed at 20 °C (F = 0.626; df = 3, df = 8; P = 0.618 [♀] and F = 0.336; df = 3; df = 8, P = 0.8 [♂]) (Fig. 4). This result indicates that the effect of temperature on diapause correlated with the photoperiod; under the short-day condition of 12L:12D, the increase of temperature had no apparent effect on diapause inhibition.

Fig. 4.

Fig. 4.

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The effect of temperature on diapause induction of Dolycoris baccarum under 12L:12D and 16L:8D. Data show means ± SE. Different letters indicate the significance of the diapause rate under different photoperiods (P < 0.01). 12L:12D: 20 °C, n = 46 ♀, 45 ♂; 25 °C, n = 53 ♀, 42 ♂; 28 °C, n = 58 ♀, 57 ♂; 30 °C, n = 51 ♀, 39 ♂. 16L:8D: 20 °C, n = 42 ♀, 42 ♂; 25 °C, n = 54 ♀, 36 ♂; 28 °C, n = 52 ♀, 63 ♂; 30 °C, n = 53 ♀, 47 ♂.

Under the long-day condition of 16L:8D, the diapause rate decreased significantly with increasing temperature (F = 38.440; df = 3, df = 8; P = 0.001 [♀] and F = 9.076; df = 3; df = 8, P = 0.006 [♂]) (Fig. 4). This result indicates that under the long-day condition of 16L:8D, the increase in temperature inhibited diapause and resulted in a significant decrease of the diapause rate. The results showed that the effect of temperature on diapause was related to the photoperiod.

Discussion

Effects of Photoperiod and Temperature on the Developmental Duration of D. baccarum

At 25 °C, differences were found in the developmental duration under different photoperiods. When the photoperiod was extended from 12L:12D to 15L:9D, the developmental duration was gradually extended, but when the photoperiod was extended to 16L:8D, the developmental period began to show a shortening trend (Fig. 1). The characteristics of the developmental duration of D. baccarum from Hohhot at 25 °C under different photoperiods were similar to those of the Osaka population and the Hokkaido population in Japan; the development period under a medium photoperiod was longer than that under both shorter and longer photoperiods (Nakamura and Numata 2006). The same phenomenon was also reported in the stinkbug, Pyrrhocoris apterus (L.) (Heteroptera: Pyrrhocoridae) (Numata et al. 1993). This phenomenon suggests that under higher temperature conditions in summer, the relationship between the developmental duration and the photoperiod of D. baccarum is determined by the critical photoperiod for diapause; the developmental duration is longer when the photoperiod nears critical conditions (Nakamura and Numata, 2006).

When the photoperiod was extended from short-day to long-day conditions, the developmental duration tended to be prolonged under each photoperiod at 20 °C (Fig. 1). No significant change in the developmental duration was found between shorter photoperiods of 10L:14D and 12L:12D, but a lengthening trend was observed at 14L:10D and 16L:8D, which differed from the trend under 25 °C. The occurrence of such a trend may be related to the high diapause rate at 20 °C. To identify the reason for this result, further research is needed.

Environmental Temperature Significantly Affects the Developmental Duration

Temperature significantly affects the developmental duration of D. baccarum. At the 4 temperatures with photoperiods of 12L:12D and 16L:8D, the developmental duration of the D. baccarum population from Hohhot was significantly shortened with increasing temperature (Fig. 2). This result indicates that temperature had a significant effect on the developmental duration and an increase in temperature resulted in accelerated development of D. baccarum. The breeding period of D. baccarum in Hohhot lasts from May to September. During these 5 months, the temperature is above 25 °C and the changes in photoperiod are 14L-15L, 15L, 15L-16L, 15L, and 15L-14L, respectively; starting from late September, the photoperiod will shorten to less than 14L. In this research, at a temperature of 25 °C, the developmental durations under photoperiods of 12L:12D and 16L:8D were similar, but the diapause rate under a photoperiod of 12L:12D was extraordinarily high (Fig. 3). This result suggests that a temperature above 25 °C and a longer photoperiod are suitable conditions for the normal development of D. baccarum in Hohhot.

Effects of the Photoperiod on the Diapause Rate of D. baccarum

While many environmental factors affect diapause in insects, temperature and photoperiod are the main factors (Tauber and Tauber 1973, Saunders 2020). Variations of the photoperiod are most apparent at high latitudes; therefore, the photoperiod is the most significant of all environmental factors affecting insect development (Meuti and Denlinger 2013, Saunders 2020). The diapause rate of the D. baccarum population from Hohhot varied significantly under different photoperiods (Fig. 3). Under the short-day condition of 12L:12D, almost all individuals entered diapause regardless of temperature. However, under the long-day condition of 16L:8D, the diapause rate decreased significantly. These results indicated that the diapause rate of D. baccarum was higher under the short-day period than under the long-day period. In high latitudes, with the alternation of seasons, the change of photoperiod is apparent. Dolycoris baccarum grows and reproduces normally under long-day conditions and enters diapause under short-day conditions.

Because of differences in geographical latitude, the photoperiod differs between different insect distribution areas, which is an important reason why the same species can show different growth and development characteristics in different distribution areas. Changes in photoperiod are the signals that induce diapause in insects (Beck 1989).

In this research, at 20 °C, the diapause rates under photoperiods of 10L:14D, 12L:12D, and 14L:10D exceeded 50%, while the diapause rate under 16L:8D did not reach 50%. This difference indicates that the critical photoperiod for diapause is likely shorter than 16 h. According to the diapause rate under each photoperiod at 25 °C, the light duration of the critical photoperiod for diapause was analyzed using regression analysis. The results showed that the critical photoperiod for diapause was 14.6 h (y = 1.1925x2 − 49.259x + 516.41, R2 = 0.975) for females and 14.1 h (y = 2.1474x2 − 78.292x + 725.8, R2 = 0.986) for males. Considering the results on the effect of the photoperiod on the developmental duration in this research (Fig. 1), the results of this analysis indicate that the developmental duration was the longest under 15L:9D at 25 °C. Therefore, the hypothesis is proposed that adult insects in diapause have the longest developmental duration under the critical photoperiod for diapause. Furthermore, this study showed that the critical photoperiod for diapause of the Hohhot population was between that of the Osaka population (13–14 h) and the Hokkaido population (15–16 h) of Japan (Nakamura and Numata 2006). This result is consistent with the latitude of Hohhot, which ranges between that of the above 2 places in Japan. These results showed that the critical photoperiods for diapause of the same insect species in different geographic distribution areas can be significantly different (Umeya and Yamada 1973, Rae and Death 1991, Fowler et al. 2015). With increasing latitude, the critical photoperiod for diapause of D. baccarum is prolonged. The differences in different geographical populations reacting to photoperiodic changes are the result of the long-term adaptation of these populations to the living environment in their distribution area. Populations in different distribution areas have different biogeographical histories, and thus have evolved unique survival strategies (Danks 1987, 2007).

Effects of Temperature on the Induction of Diapause in D. baccarum

Under the short-day photoperiod of 12L:12D, the diapause rates at 20, 25, 28, and 30 °C of D. baccarum from Hohhot were all close to 100% (Fig. 4), indicating that the effect of temperature on diapause under the short-day condition was not apparent. However, under the long-day photoperiod of 16L:8D, the diapause rate decreased significantly with increasing temperature (Fig. 4), indicating that the higher temperature inhibited diapause and the lower temperature promoted diapause.

Temperature plays a significant role in the diapause process of insects, especially in tropical and subtropical regions with low latitudes, where the photoperiodic changes are not apparent, and the temperature usually triggers insects to enter diapause. Research on Colaphellus bowingi Baly (Coleoptera: Chrysomelidae) showed that adults enter diapause at a temperature of ≤20 °C and that temperature was the main environmental factor triggering diapause (Xue et al. 2002). However, in temperate regions at high latitudes, temperature is usually a diapause cofactor that acts in concert with the photoperiod (Danks 2007, Zhuo et al. 2011, Chen et al. 2015, Saunders 2020). For certain insects, both temperature and photoperiod are the main factors that induce diapause (Fatemeh and Saeid 2018). With regard to D. baccarum from Hohhot, the results of this study showed that the temperature was not the main diapause-inducing factor under the short-day condition of 12L:12D; however, under the long-day condition of 16L:8D, temperature significantly affected diapause, according to the following logic: the higher the temperature, the lower the diapause rate.

The observation found that D. baccarum from Hohhot began to enter their retreat site for overwintering in October. They usually did not like to choose the warm place that human lived as their overwintering site. At the end of March and beginning of April of the next year, they recovered and left their overwintering site and laid eggs for reproduction in about May (unpublished data).

It should be noted that in this research, once the conditions such as photoperiod and temperature were set, they were not changed thereafter. However, natural conditions change considerably, and the temperature during the day and night of 1 day will always be different from those on a different day, especially after late September, when the differences between day and night temperatures are large in Hohhot. Therefore, it is necessary to study the developmental duration and diapause induction under conditions where both photoperiod and temperature are varied. In addition, in this research, diapause was induced from eggs to the adult stage under set conditions. However, it remains unclear which developmental stage of D. baccarum is actually sensitive to the induction of diapause by temperature and photoperiod. Therefore, further research is required.

Acknowledgments

The authors express their thanks to Professor Qiang Liu, Tianjin Normal University, for critical reading of the manuscript and useful suggestions.

Contributor Information

Ruilin Tian, College of Life Science and Technology, Inner Mongolia Normal University, Hohhot 010022, China; Key Laboratory of Biodiversity Conservation and Sustainable Utilization in Mongolian Plateau for College and University of Inner Mongolia Autonomous Region, Hohhot 010022, China.

Zhanming Hou, College of Life Science and Technology, Inner Mongolia Normal University, Hohhot 010022, China.

Song Li, College of Life Science and Technology, Inner Mongolia Normal University, Hohhot 010022, China; Key Laboratory of Biodiversity Conservation and Sustainable Utilization in Mongolian Plateau for College and University of Inner Mongolia Autonomous Region, Hohhot 010022, China.

Hua Chai, College of Life Science and Technology, Inner Mongolia Normal University, Hohhot 010022, China.

Funding

This study was financially supported by the Natural Science Foundation of Inner Mongolia, China (no. 2020MS03016) and the Fundamental Research Funds for the Inner Mongolia Normal University (no. 2022JBTD010).

Author Contributions

Rui Tian (Conceptualization [Equal], Methodology [Equal], Writing—review & editing [Equal]), Zhan Hou (Methodology [Equal], Supervision [Equal], Writing—review & editing [Equal]), Song Li (Data curation [Equal], Investigation [Equal], Resources [Equal]), and Hua Chai (Investigation [Equal], Writing—original draft [Equal])

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