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On the Reproductive Diapause in the Predatory Ladybird Cheilomenes Sexmaculata (Fabricius, 1781) (Coleoptera, Coccinellidae) S

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On the Reproductive Diapause in the Predatory Ladybird Cheilomenes Sexmaculata (Fabricius, 1781) (Coleoptera, Coccinellidae) S ISSN 0013-8738, Entomological Review, 2021, Vol. 101, No. 1, pp. 1–6. © The Author(s), 2021. This article is an open access publication. Russian Text © The Author(s), 2021, published in Entomologicheskoe Obozrenie, 2021, Vol. 100, No. 1, pp. 5–13. On the Reproductive Diapause in the Predatory Ladybird Cheilomenes sexmaculata (Fabricius, 1781) (Coleoptera, Coccinellidae) S. Ya. Reznika,b,*, A. N. Ovchinnikova,b, A. A. Ovchinnikovab, O. S. Bezman-Moseykob, and N. A. Belyakovaa a All-Russia Institute of Plant Protection, Russian Academy of Sciences, Pushkin, St. Petersburg, 196608 Russia b Zoological Institute, Russian Academy of Sciences, St. Petersburg, 199034 Russia *e-mail: [email protected] Received January 14, 2021; revised January 19, 2021; accepted January 19, 2021 Abstract—The ability to enter reproductive diapause was experimentally studied in females of the laboratory population of the predatory ladybird Cheilomenes sexmaculata originated from individuals collected in Nepal in a region of subtropical monsoon climate. The experiment included 12 regimes, i.e. combinations of 2 temperatures (20 and 24°C), 3 photoperiods (day lengths of 10, 12, and 14 h), and 2 diets (the green peach aphid Myzus persicae and eggs of the grain moth Sitotroga cerealella). Females with undeveloped ovaries and well developed fat body were considered as diapausing. The proportion of diapausing females was signifi cantly dependent only on the temperature being 0.8% at 24°С and 7.4% at 20°С. Although found in only a small fraction of the studied population, the ability to enter reproductive diapause (as suggested by literature data) was probably an important prerequisite for Ch. sex- maculata spread northwards to the temperate zone. Keywords: diapause, temperature, photoperiod, variation, Cheilomenes sexmaculata, Coccinellidae DOI: 10.1134/S0013873821010012 Facultative diapause anticipatory induced by envi- value of wintering adaptations is not as high as in the ronmental cue factors and ensuring survival during ad- temperate and arctic zones. Nevertheless, facultative verse periods is one of the most important seasonal ad- winter diapause induced by short day and low tempera- aptations of insects (Tauber et al., 1986; Danks, 2007; ture is also recorded for many subtropical insects, al- Tougeron, 2019). Winter diapause that is usually in- though it is not as deep and stable as in insects from the duced in insects of the temperate and arctic zones by temperate and arctic zones. Moreover, often not only short light day and / or low temperature results in a de- diapause intensity but also diapause frequency de- crease in metabolism intensity, in an arrest of develop- creases: even under the most “strong” combination of ment or reproduction, in an increase in cold resistance, diapause-inducing factors it is induced in only a small and in other changes which are necessary for successful proportion of individuals. It is well known that this indi- overwintering of most insect species. Therefore, the vidual variability in the ability to diapause is not only process of induction of winter diapause is strictly con- important for the population survival during the extreme trolled by natural selection ensuring precise adaptation seasons but also serves as an essential prerequisite for to the specifi city of the local climate (Danilevsky, 1961; the spreading to the regions with colder climate (Sau- Zaslavsky, 1984, 1996; Denlinger, 2002; Saunders et al., lich, 1999; Saulich and Volkovich, 2004). 2002; Saulich and Volkovich, 2004). In insects inhab- iting the subtropical zone, where the winter decrease in The object of our study, the predatory ladybird temperature and corresponding worsening of the envi- Cheilomenes sexmaculata (Menochilus sexmaculatus) ronmental conditions are poorly expressed, the selective (Fabri cius, 1781) (Coleoptera, Coccinellidae), is widely 1 2 REZNIK et al. distributed in the tropical and subtropical regions of and day length of 18 h. The experiments were conducted Southern Asia (Afghanistan, Pakistan, India, Indonesia, in Laboratory of Experimental Entomology (Zoological Philippines, etc.) and Australia (Iftikhar et al., 2018) and Institute RAS). Before the study the ladybirds were for at present is spreading northward up to central Japan 1 or 2 generations reared at a temperature of 24°С and (Kawakami et al., 2016, 2017). This widely distributed day length of 14 h; larvae and adults were fed on the polyphagous species is well known as an important green peach aphid Myzus persicae (Sulz.) reared on agent for biological control of various sucking insect bean Vicia faba L. seedlings. Larvae and pupae of indi- pests (Pandi et al., 2012; Iftikhar et al., 2018) and, there- viduals which were used in the experiments were reared fore, the main aspects of its biology have been thor- under the same conditions. oughly studied (Campbell et al., 1980; Omkar et al., At the beginning of the experiment (no more than 2005; Pandi et al., 2012; Wang et al., 2013; Mirhosseini 24 h after emergence) Ch. sexmaculata adults were et al., 2015; Zhao et al., 2015; Singh et al., 2016; Iftikhar weighed on electronic scales with the accuracy of et al., 2018). In particular, it was shown that the time of 0.1 mg and then, in pairs (male and female), were placed female maturation depends not only on temperature, but in plastic Petri dishes 60 mm in diameter and 15 mm also on photoperiod (Wang et al., 2013). The day length high. Then all the dishes were evenly distributed also infl uences the mean rate of preimaginal develop- between 12 experimental treatments, i. e. combinations ment (Singh et al., 2016), but the ability to enter repro- of 2 temperatures (20 and 24°С), 3 photoperiods (day ductive diapause was not considered in these studies. lengths of 10, 12 and 14 h), and 2 diets: (1) larvae and Phenological observations of Ch. sexmaculata popula- adults of the green peach aphid on a bean seedling or tions conducted under natural conditions in Japan, near (2) frozen eggs of the grain moth Sitotroga cerealella the northern limit of the species range suggested that (Oliv.) (Lepidoptera, Gelechiidae) glued with a 30% adults overwintered in reproductive diapause (Kawakami water solution of sugar to a piece of hard paper and et al., 2016, 2017), although this was not verifi ed by spe- a plastic tube fi lled with water and plugged with a cotton cial laboratory experiments. Transfer to the short day ball. The relative air humidity was the same in all the conditions also did not induce diapause in ovipositing treatments of the experiment (about 70%); the food was females of the laboratory strain originated from individ- always provided in excess. All dishes were daily ob- uals collected in Pakistan (Campbell et al., 1980). served to record the beginning of oviposition. At the end We made an attempt to induce reproductive diapause of the experiment (10 days at 24°С and 15 days at 20°С) in females of the laboratory population of Ch. sexmacu- all the females were weighed again and then dissected. lata originated from individuals collected in Nepal in The age of females at dissection was calculated based on a region of the subtropical monsoon climate. the results of earlier studies: under the optimal condi- tions, by this time most individuals start to lay eggs MATERIALS AND METHODS (Campbell et al., 1980; Omkar et al., 2005; Wang et al., 2013; Mirhosseini et al., 2015; Zhao et al., 2015). The The experiments were conducted with the laboratory state of ovaries was evaluated with the simple scale: population of Ch. sexmaculata originated from 30 in- “developed” (follicles are wider than germarium; dividuals collected in May 2013 in Nepal, in the envi- mature oocytes are well visible) or “undeveloped” (only rons of Sauraha (27.5848°N, 84.5038°E, 189 m asl). germarium is visible, follicles are absent or barely Sauraha has a subtropical monsoon climate: the average noticeable); the fat body was also evaluated as “devel- temperatures of December–January and May–August oped” or “undeveloped.” are about 16 and 29°С, correspondingly; the dry season with the mean monthly precipitation of less than Thus, for each survived female, the state of the ova- 20 mm lasted from November to March (data from ries and of the fat body were determined. In addition, the https://ru.climate-data.org/). relative increase in weight was calculated by the for- mula D = (W2–W1) / W1, where W1 is the initial weight For several years the ladybirds were reared in Bio- of a female at the beginning of the experiment (just after control Laboratory of All-Russia Institute of Plant Pro- emergence) and W2 is its weight at the end of the exper- tection on the wheat aphid Schizaphis graminum Rond. iment (before dissection). Further, the age at the mo- (Hemiptera, Aphididae) at a temperature of 20–25°С ment of the beginning of oviposition was recorded for ENTOMOLOGICAL REVIEW Vol. 101 No. 1 2021 ON THE REPRODUCTIVE DIAPAUSE 3 each ovipositing female. In total, 249 females were used on the contrary, signifi cantly depended both on the tem- in the study (from 18 to 24 per each of the 12 experi- perature (5.9 ± 0.2 and 8.5 ± 0.3 days at 24 and 20°С, mental treatments). correspondingly) and on the diet (6.0 ± 0.2 and 9.3 ± 0.3 days with feeding on aphids and on grain moth eggs, Statistical treatment of the experimental results in- correspondingly) (Table 1). In particular, at 20°С ovipo- cluded multiple linear regression, probit analysis, sition was started by 86% of females with developed 2 Spearman rank correlation analysis, and χ test. For the ovaries and undeveloped fat body but only by 50% of descriptive statistics, the mean and standard error were females in which both ovaries and fat body were well used.
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