A. N. Ovchinnikov

Weak photoperiodic response facilitates the biological invasion of the harlequin ladybird Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae)

Photoperiodic regulation of reproductive diapause in two invasive and two native populations of Harmonia axyridis and in one native population of Harmonia yedoensis was investigated in laboratory at 20°C, five photoperiods (day length of 10, 12, 14, 16 and 18 h) and two diets: (i) eggs of the Angoumois grain moth Sitotroga cerealella and (ii) the green peach aphid, Myzus persicae. Laboratory strains originated from native populations of H. axyridis from Irkutsk province of Siberia and H. yedoensis from South Korea showed a strong photoperiodic response: under short photoperiods (10–14 h and 10–12 h for H. axyridis and H. yedoensis, correspondingly), all females which fed on eggs and most of those fed on aphids did not start to lay eggs during 40 days after emergence, while under long photoperiods, all females fed on aphids and most of those fed on eggs oviposited. The photoperiodic response of H. axyridis from South Korea was less strong: on the both diets, the range of the photoperiodic response (the difference in the proportion of ovipositing females between the treatments with long and short days) was ca 40%. In the European (Czech Republic) and in the Caucasian (Sochi region, Russia) invasive populations of H. axyridis, the photoperiodic response was very weak: the proportion of females that started oviposition (when fed on aphids) or at least reproductive maturation (when fed on eggs) during 40 days after emergence was close to 100%, independently of the photoperiodic conditions. Obviously, instead of a rapid micro‐evolutionary adaptation of the critical day length to a new climate, the invasive populations of the harlequin ladybird decrease their dependence on photoperiod and thus the weak photoperiodic response of SE Asian population of H. axyridis can be considered as a pre‐adaptation further developed during the invasion.

Cumulative induction of diapause in successive generations of Trichogramma species (Hymenoptera, Trichogrammatidae)

The ability of two Trichogramma species (Trichogramma telengai Sor. and T. principium Sug. et Sor.) to accumulate the effect of the maternal photoperiodic response during 5 consecutive generations reared in the laboratory under the short day (12 h) conditions was investigated. Control individuals developed at the same temperature of 20°C, but under the long day (18 h) conditions. The tendency to diapause was estimated by the proportion of progeny that entered diapause under the short day conditions at the temperatures of 13, 14 and 15°C. Trichogramma principium manifested an evident transgenerational cumulative photoperiodic response: the development of 1, 2, and 3 consecutive generations under the short day conditions caused a gradual increase in the proportion of diapausing progeny. In T. telengai, the progeny of the females that developed under the short day conditions also entered diapause more often than the progeny of those that developed under the long day conditions, but the number of preceding generations which developed under short day had no effect on the tendency to diapause. This interspecific difference can be possibly explained by the different natural geographic ranges of the two studied species. Trichogramma principium occurs in Southern Europe, Southern Kazakhstan, and Central Asia where the autumnal decrease in temperature is very slow and thus two or even more generations can develop under the short day conditions, whereas T. telengai is distributed over Central and North-Western Europe and in Siberia, where the autumnal decrease in temperature is rather fast, the development of one more “autumnal” generation is risky, and thus even the first “short-day signal” induces a very strong tendency of the progeny to diapause.

Interspecific variation in photoperiodic effect on the rate of preimaginal development in Harmonia axyridis (Pallas) (Coleoptera, Coccinellidae)

The effects of day length on preimaginal development and reproductive maturation of females of laboratory strains which originated from two native: Irkutsk (Siberia, Russia) and Daegu (South Korea) and two invasive: Sochi (Caucasus, Russia) and Pardubice (Czechia) populations of Harmonia axyridis were investigated under the laboratory conditions. In all the 4 strains, the acceleration of development caused by the short day (all other conditions being equal) was relatively stronger in those larvae that later, at the adult stage, delayed reproductive maturation. This correlation can be considered as an indirect proof that both reactions are based on the common physiological mechanism. However, comparison of the parameters of photoperiodic responses showed that although the photoperiodic effect on reproductive maturation in individuals from Sochi and Pardubice invasive populations was relatively weak, the effect of day length on the rate of their preimaginal development was even somewhat stronger than that of individuals from Irkutsk and Daegu native populations. This uncorrelated interpopulation variation of the quantitative and qualitative photoperiodic responses suggests that in spite of the common physiological mechanism, the responses influencing preimaginal development and reproductive maturation of H. axyridis are to a certain extent independent and thus the evolution of their parameters (in particular, adaptation to new climate conditions) occurs independently.

The influence of density-dependent factors on larval development in native and invasive populations of Harmonia axyridis (Pall.) (Coleoptera, Coccinellidae)

Effects of the number of larvae per Petri dish (1, 5, and 10) on the preimaginal development of individuals of the native (Irkutsk, southern Siberia) and invasive (Sochi, the Northern Caucasus) populations of the multicolored Asian ladybird Harmonia axyridis were investigated in the laboratory. The experiments were conducted under short (12 h) and long (18 h) day conditions; the larvae were fed on the green peach aphid Myzus persicae or on the eggs of the grain moth Sitotroga cerealella. An increase in the number of larvae developed in one Petri dish resulted in a significant decrease in the rate of development in individuals from both populations which fed on aphids. Survival decreased with an increase in the number of larvae developed in one Petri dish fed on both prey species, but only in larvae from the invasive population of H. axyridis. The weight of emerging adults decreased with the number of larvae per dish in individuals from both study populations, but only when fed on aphids. These data suggest that the influence of density-dependent factors on the development of H. axyridis depends significantly on larval prey species. In addition, larvae from the invasive population have somewhat more aggressive interactions with competitors, this possibly having been one of the prerequisites for invasion.

Costs and benefits of interlarval cannibalism in Harmonia axyridis

Cannibalism, which is rather common in ladybirds, has been usually studied at the individual level: benefits of cannibalism for cannibals were estimated. Our study was conducted at the group level: we evaluated the overall effect of interlarval cannibalism on a group of Harmonia axyridis larvae of the fourth instar deprived of food, including both cannibals and their victims. Experiments showed that the probability of pupation in larvae which were kept individually was significantly higher than in larvae kept in groups of five, other conditions being the same. The proportion of samples in which at least one of five individuals pupated among the larvae kept individually was also higher than among those kept in groups suggesting that the eventual benefit of cannibalism was outweighed by the negative impact of aggressive interlarval interactions. The mean and minimum survival time in samples where none of five larvae pupated were longer when larvae were kept individually than when larvae were kept in groups. However, the maximum survival time (the survival time of the last larva in a sample) increased when larvae were kept in groups, which was the only one benefit of cannibalism found in our study. Under natural conditions, the possible adaptive value of this effect is that in the absence of natural prey, longer larval survival time proportionally increases the possibility of finding a new prey patch thereby ensuring survival of the population.

The Influence of Diet and Population Density on Maturation of Females from Native and Invasive Populations of the Multicolored Asian Ladybird Harmonia axyridis (Pallas) (Coleoptera, Coccinellidae)

Population density can influence insect reproduction both directly and indirectly causing quantitative and qualitative changes in the feeding regime. We investigated the impact of diet and population density on reproductive maturation of females from native (Irkutsk) and invasive (Sochi) populations of the multicolored Asian ladybird Harmonia axyridis. During the study the beetles fed either on the green peach aphid, Myzus persicae, or on less suitable factitious food (eggs of the grain moth Sitotroga cerealella). Population density was determined by the number of females and males placed in a standard Petri dish. The experiments showed that feeding on the grain moth eggs (other conditions being equal) delayed maturation and increased the tendency to enter reproductive diapause in females from the native but not from the invasive population of H. axyridis. In addition, the preoviposition period increased with the number of females but decreased with the number of males in a dish, although these effects were observed only in individuals from the invasive population and their strength depended on the food of the beetles. Earlier we have demonstrated that the impact of the density-dependent factors on the larvae of the invasive population of H. axyridis was stronger than that on the larvae of the native population because the larvae of the invasive population have somewhat more aggressive interactions with competitors. In the present study, similar differences were revealed between females of these populations.

On the photoperiodic induction of diapause in first generation hybrids of Harmonia axyridis (Pall.) (Coleoptera, Coccinellidae)

Ladybirds Harmonia axyridis (Pallas) belonging to the autochthonous and invasive populations from Irkutsk and Sochi that differed in the photoperiodic induction of diapause were crossed in laboratory conditions. The individuals from the Irkutsk population show a strong induction of diapause under short day conditions, while individuals from the Sochi population exhibit very weak photoperiodic induction of diapause. The F1 hybrids obtained from reciprocal crosses demonstrated a photoperiodic reaction similar to that of the parental individuals of the Irkutsk population. The obtained data suggest that the strong photoperiodic induction of diapause is dominant and the effects of male and female genotypes on progeny phenotype are equal.

Musculature of the Ovipositor of Timia erythrocephala Wiedemann, 1824 (Diptera, Ulidiidae)

The structure of the ovipositor sclerites and musculature was investigated in Timia erythrocephala Wiedemann, 1824 (Ulidiidae), whose larvae are saprophagous. The ovipositor musculature of this species is compared with that of the previously investigated Tephritidae. Based on morphological analysis, characters common to Ulidiidae and primitive Tephritidae and supposedly plesiomorphic for Tephritidae are revealed. Abdominal segment VII in Timia is compact and consists of tergite and stemite VII fused into a syntergostemite with a visible suture. The preserved suture between the stemite and tergite of segment VII should be regarded as an intermediate state in the process of syntergostemite formation in tephritoid flies, which was completed already in Lenitovena.

Color polymorphism, development, and reproductive diapause of the multicolored Asian ladybird Harmonia axyridis (Pallas) (Coleoptera, Coccinellidae) females

Preimaginal development and maturation of females of two laboratory strains originated from two populations of the multicolored Asian ladybird Harmonia axyridis were investigated under laboratory conditions. Females of the autochthonous population from Irkutsk (Siberia) enter diapause under the short day conditions, whereas in females of the invasive population from Sochi (the Caucasus) photoperiodic induction of diapause is weak. The two populations also differ in the proportions of morphs: the population from Sochi is represented only by the morph succinea, whereas the population from Irkutsk is represented by the morphs succinea и axyridis with the predominance of the last one, which in our study was separated into two phenotypes, differed in the degree of melanization. Rearing of adults under the short day (12 h) conditions induced reproductive diapause in females of all the studied morphs and phenotypes of the Irkutsk population, whereas under the long day (18 h) conditions females of the morph succinea showed a slightly lower tendency to diapause. Evidently, the interpopulation differences in the responses regulating the seasonal cycle of the multicolored Asian ladybird are determined by genes that are not involved (or almost not involved) in the determination of the color polymorphism. The interpopulation differences in size and weight were quite substantial, whereas the differences between morphs and phenotypes were statistically significant in only some of our experiments. In combination with the literature data, these results suggest that the genes determining the color polymorphism in H. axyridis may have a pleiotropic effect on other traits including important eco-physiological parameters but this effect is relatively weak and manifests itself only against a particular genetic background and / or under particular environmental conditions.

Dynamics of the Photo-Trophic Termination of Reproductive Diapause in Females of the Multicolored Asian Ladybird Harmonia axyridis (Pallas) (Coleoptera, Coccinellidae)

Females of certain aphidophagous ladybirds in the absence of natural protein food (aphids) enter reproductive diapause. Reactivation of diapausing beetles is possible only after consuming the food which is suitable for oogenesis of females and development of larvae. The influence of diet and photoperiod on the dynamics of weight and on the rate of reproductive maturation of reactivating females of Harmonia axyridis was studied under laboratory conditions. The experiments were conducted at combinations of two day lengths (12 and 18 h) with 6 trophic regimes with the following mean numbers of daily consumed aphids: 0 (aphids were absent over the whole experiment), 0.1 (1 aphid was provided every 10 days), 0.5 (1 aphid every second day), 1 (1 aphid every day), 10 (10 aphids every day), and 50 (about 50 aphids every day). Judging from the state of ovarian development estimated by dissection 20 days after the beginning of the experiment, the threshold of the trophic termination of reproductive diapause under the long day conditions lies between the regimes of 0.1 and 0.5 aphids per day, which is approximately equal to the earlier investigated threshold of the trophic induction of diapause. Short day slowed reactivation and has increased the threshold of the trophic response up to 1-10 aphids per day. Based on these data, we conclude that under natural conditions females which entered reproductive diapause because of the absence of aphids are capable of reactivation in the presence of even a minimal amount of natural protein food. Moreover, in spring and summer (when the probability of the increase in aphid abundance is relatively high) reactivation starts at lower prey population density than in autumn, when the appearance of the stable aphid colony (which is necessary to complete the development of the emerged larvae) is less probable.