Locomotor Behavior of Flightless Harmonia axyridis Pallas (Col., Coccinellidae)

To improve the efficiency of the lady beetle H. axyridis as a biological control agent against aphids, a flightless population was obtained by feeding adults with a mutagen and selecting their progeny for nonflying but otherwise morphologically normal individuals. These flightless adults attempted to fly but immediately fell. They softened their fall by opening their elytrae and wings. The inability to fly could result from change in their flying behavior compared to control adults. The flight duration was very much shorter, and the wing beat frequency and, more particularly, the amplitude of the wing beats were clearly lower. More time was spent in the other components of the flight behavior such as wing rotation, wing immobility, and wing folding. The sequence of these patterns differed slightly, due mainly to change in their frequency. The locomotor behavior was not modified by the mutation, which affected only the wing muscles. Searching behavior of mutant adults differed from that of control adults only in that they took longer to encounter and ingest aphids. Nevertheless, the larval growth and reproductive rate remained unchanged. The behavioral and biological features of these flightless adults indicate that it should be possible to use them in biological control programs.     

A natural flightless mutation in the ladybird, Harmonia axyridis

A homozygous flightless strain, obtained by selection from a laboratory population of Harmonia axyridis Pallas (Coleoptera, Coccinellidae), has been reared under controlled conditions since 1982 after sampling in China. The adults of this flightless strain have normal elytra and wings but drop almost vertically when they attempt to fly. The origin of this mutation, whether laboratory or natural, is discussed. As the mutation does not affect the fitness of the beetles, this flightless strain can be used in biological control. Releasing flightless adults rather than larvae should provide the potential for more continuous control of aphids by both larvae and adults.     

Aphid consumption and residence time of larvae of flightless lady beetles, Harmonia axyridis (Coleoptera: Coccinellidae), on aphid-infested plants

A flightless strain of the lady beetle, Harmonia axyridis Pallas, has been established, by artificial selection, for effective biological control of aphids. However, this biological control technique is costly because of the high cost of production of the adults. It is, therefore, important to consider the utility of the larvae in biological control. This study examined the potential for larvae of the flightless strain to be used as biological control agents compared with those of the wild-type, in terms of how they behave on aphid-infested plants. We found no differences between the strains with regard to residence time and aphid consumption on the plant for the first, second, and fourth instars, and at low and high aphid densities. In contrast, however, aphid consumption by third-instar larvae of the flightless strain tended to be lower, although they remained on the plant longer than third-instar larvae of the wild-type. Consequently, our results suggest the flightless strain does not differ from the wild-type in its ability to control aphids across all larval stages, except for the third instars. On the basis of these results, and in conjunction with the results from previous studies, we discuss the appropriateness of different larval instars for release.     

Natural flightless morphs of the ladybird beetle Adalia bipunctata improve biological control of aphids on single plants

The challenge of using ladybird beetles for biological control of insect pests such as aphids is that the adult beetles tend to fly away from the host plants. Therefore, flightless ladybirds might improve biocontrol. There are several artificial ways to obtain flightless beetles, but it may be preferable to use natural variation in flight ability. We investigated, for the first time, biocontrol by inundative augmentation of natural flightless morphs of the ladybird beetle Adalia bipunctata. Microcosm experiments using single leaves with one of three species of aphid revealed no differences in consumption behavior between flightless and winged beetles. Monitoring for 48 h of single, caged pepper plants infested with aphids of Myzus persicae nicotianae or Aulacorthum solani showed that flightless beetles had a longer residence time on the plants than winged beetles. This only translated into significantly better biocontrol of M. persicae. Despite their difference in residence time, both beetle morphs reduced the population growth of A. solani. This is probably explained by the tendency of A. solani to drop from the plant upon disturbance, and we predict that flightless beetles may outperform winged ones in the long term. Overall, our results provide a proof of principle that natural flightless A. bipunctata can improve biocontrol of aphids by ladybird beetles. However, we recognize that the effect of biocontrol will vary with the species of aphid used and that further examination in long term and large scale experiments is required.     

Genetics and selective breeding of variation in wing truncation in a flightless aphid control agent

Augmentative biological control by predaceous ladybird beetles can be improved by using flightless morphs, which have longer residence times on the host plants. The two‐spot ladybird beetle, Adalia bipunctata (L.) (Coleoptera: Coccinellidae), is used for the biological control of aphids in greenhouses and on urban trees. Flightlessness due to truncated wings occurs at very low frequency in some natural populations of A. bipunctata. Pure‐breeding strains of this 'wingless' genotype of A. bipunctata can easily be obtained in the laboratory. Such strains have not been commercialized yet due to concerns about their reduced fitness compared to wild‐type strains, which renders mass production more expensive. Wingless strains exhibit, however, wide intra‐population phenotypic variation in the extent of wing truncation which is related to fitness traits. We here use classical quantitative genetic techniques to study the heritability and genetic architecture of variation in wing truncation in a wingless strain of A. bipunctata. Split‐families reared at one of two temperatures revealed strong family‐by‐temperature interaction: heritability was estimated as 0.64 ± 0.09 at 19 °C and 0.29 ± 0.06 at 29 °C. Artificial selection in opposite directions at 21 °C demonstrated that the degree of wing truncation can be altered within a few generations resulting in wingless phenotypes without any wing tissue (realized h² = 0.72), as well as those with minimal truncations (realized h² = 0.61) in two replicates. The latter lines produced more than twice as many individuals. This indicates that selective breeding of wing truncation may be exploited to improve mass rearing of flightless strains of A. bipunctata for commercial biological control. Our work illustrates that cryptic variation can also be a source for the selective breeding of natural enemies.     

An artificial non-flying mutation to improve the efficiency of the ladybird Harmonia axyridis in biological control of aphids

The use of coccinellids in the biological control of aphids is restricted to the release of larvae because adults tend to fly away. Non-flying adults may stay longer in one place and so they and their progeny could give longer term protection to plants. This work is an attempt to produce a non-flying population by the use of a chemical mutagen and selection of adults with wing malformations through their subsequent generations. These adults are characterized by open elytra and extended wings. Some general features of this mutation were disclosed. The mutation is either unexpressed or results in malformed wings. It also seems recessive and lethal when homozygous. The adults with the mutation suffered a high level of mortality and a drastic reduction in reproductive capacity that prevents their mass rearing for biological control. This study revealed a negative relationship between wing malformations and reproductive capacity. Nevertheless, when adults with the mutation were released in greenhouses containing cucumbers infested with the aphid Aphis gossypii, they remained on the plants in higher numbers and laid eggs over a longer period of time than the control adults but their progeny were less numerous.     

Releases of a natural flightless strain of the ladybird beetle Adalia bipunctata reduce aphid-born honeydew beneath urban lime trees

Aphids can cause major environmental problems in urban areas. One important problem is the annual outbreaks of lime aphid, Eucallipterus tiliae (L.) (Hemiptera: Aphididae), which spoil the surroundings of lime trees by depositing honeydew. To date no environmentally friendly method has been demonstrated to yield effective control of lime aphids. Attempts are made in some cities to control lime aphids by releasing larvae of the native two-spot ladybird beetle, Adalia bipunctata (L.) (Coleoptera: Coccinellidae). However, it is known that adult ladybird beetles disperse soon after release, and there is little indication they provide control of the aphids. Here, we demonstrate experimentally that releases of a flightless strain of A. bipunctata, obtained from natural variation in wing length, can reduce the impact of honeydew from lime aphid outbreaks on two species of lime in an urban environment. Both larvae and adult beetles were released, and we discuss the contribution of the flightless adults to the decline in honeydew.     

Entomopathogenic fungi stimulate transgenerational wing induction in pea aphids,Acyrthosiphon pisum (Hemiptera: Aphididae)

1. Aphid natural enemies include not only predators and parasitoids but also pathogens, of which fungi are the most studied for biological control. While wing formation in aphids is induced by abiotic conditions, it is also affected by biotic interactions with their arthropod natural enemies. Wing induction via interactions with arthropod natural enemies is mediated by the increase in their physical contact when alarmed (pseudo‐crowding). Pathogenic fungi do not trigger this alarm behaviour in aphids and, therefore, no pseudo‐crowding occurs. 2. We hypothesise that, while pathogenic fungi will stimulate maternally induced wing formation, the mechanism is different and is influenced by pathogen specificity. We tested this hypothesis using two entomopathogenic fungi, Pandora neoaphidis and Beauveria bassiana, an aphid specialist and a generalist respectively, on the pea aphid, Acyrthosiphon pisum Harris. 3. We first demonstrate that pea aphids infected with either pathogen and maintained in groups on broad bean plants produced a higher proportion of winged morphs than uninfected control aphids. We then show that, when maintained in isolation, aphids infected with either pathogen also produced higher proportions of winged offspring than control aphids. There was no difference between P. neoaphidis and B. bassiana in their effects on wing induction in either experiment. 4. Unlike the effect of predators and parasitoids on pea aphid wing induction, the effect of pathogens is independent of physical contact with other aphids, suggesting that physiological cues induce wing formation in infected aphids. It is possible that aphids benefit from wing induction by escaping infected patches whilst pathogens may benefit through dispersion. Possible mechanisms of wing induction are discussed.     

Control of Myzus persicae and Lipaphis erysimi (Hemiptera: Aphididae) by adults and larvae of a flightless strain of Harmonia axyridis (Coleoptera: Coccinellidae) on non-heading Brassica cultivars in the greenhouse

The green peach aphid [Myzus persicae (Sulzer)] and turnip aphid [Lipaphis erysimi (Kaltenbach)] are economically important pests with a worldwide distribution. We have evaluated the efficacy of releasing adults and larvae of a flightless strain of the multicolored Asian lady beetle (Harmonia axyridis Pallas) as a control measure against these aphids on plants of non-heading Brassica cultivars. Both adults and larvae of H. axyridis were observed to be effective biocontrol agents, markedly decreasing the numbers of aphids. The residence duration of adults was longer than that of larvae. The proportion of non-marketable plants damaged by aphids was lower in plots into which either adults or adults and larvae of H. axyridis had been released. These results suggest that both adults and larvae of this flightless strain of H. axyridis are effective in controlling aphids on plants of non-heading Brassica cultivars.     

Suppression of aphids by augmentative release of larvae of flightless Harmonia axyridis

The release of the larvae of flightless ladybird beetles could extend the duration of effective control because of the longer presence of adult stages, and the per individual production cost for juvenile stages is lower than that for adult stages. A preliminary release experiment was conducted to assess the effectiveness in controlling two aphid species, Aphis gossypii and Aulacorthum solani, using second instars of a flightless strain of Harmonia axyridis. The number of A. gossypii was suppressed in greenhouses that contained the flightless strain compared with greenhouses that contained the wild‐type strain. In one of two replicates, more flightless adults were observed on the plants for longer than wild‐type adults. However, it was not clear whether the extension of the residence period contributed to the effectiveness in controlling aphids directly, because the population of ladybirds in the greenhouses consisted of both larvae and adults during parts of the experimental period. In flightless H. axyridis, the release of larvae was more effective in suppressing A. solani than the release of adults. These results suggest that it may be more effective to release larvae of flightless H. axyridis than wild‐type larvae or flightless adults.     

Differential photoperiodic responses in genetically identical winged and wingless pea aphids, Acyrthosiphon pisum, and the effect of day length on wing development

Abstract. Winged and wingless individuals of a pink clone of the pea aphid, Acyrthosiphon pisum (Harris), showed differences in the response curves for photoperiodic induction of both males and sexual females (oviparae). The critical night length (CNL) for ovipara induction in winged aphids was 0.75 h shorter than in wingless aphids, whereas the CNL for male induction in winged aphids was 1.0h longer than in wingless aphids. This means that in winged aphids the CNL for male induction in winged aphids was 0.5 h longer than that for ovipara induction, while in wingless aphids the CNL for male induction was 1.0–1.5 h shorter than that for ovipara induction, and also the shapes of the curves differed.
Winged aphids were produced by wingless mothers which were crowded as young adults. However, when young adults were crowded in long nights, winged aphids were not produced, and the CNL for wing inhibition was between 9.5 and 10h. This effect of photoperiod on wing induction was maternal.     

Juvenile hormone titres and winged offspring production do not correlate in the pea aphid, Acyrthosiphon pisum

Pea aphids, Acyrthosiphon pisum, reproduce parthenogenetically and are wing-dimorphic such that offspring can develop into winged (alate) or unwinged (apterous) adults. Alate induction is maternal and offspring phenotype is entirely determined by changes in the physiology and environment of the mother. Juvenile hormones (JHs) have been implicated in playing a role in wing differentiation in aphids, however until recently, methods were not available to accurately quantify these insect hormones in small insects such as aphids. Using a novel LC-MS approach we were able to quantify JH III in pea aphids that were either producing a high proportion of winged morphs among their offspring or mainly unwinged offspring. We measured JH III titres by pooling the hemolymph of 12 or fewer individuals (1 μL hemolymph) treated identically. Levels of JH ranged from 30 to 163 pg/μL. While aphids in the two treatments strongly differed in the proportion of winged morphs among their offspring, their JH III titres did not differ significantly. There was also no correlation between JH III titre and the proportion of winged offspring in induced aphids. This supports earlier findings that wing dimorphism in aphids may be regulated by other physiological mechanisms.     

Walking activity of flightless Harmonia axyridis (Coleoptera: Coccinellidae) as a biological control agent

The use of flightless strains of the multicolored Asian lady beetle, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), established via artificial selection, can be highly effective as a biological control agent for aphids. However, flightless H. axyridis must depend on walking for dispersion. Therefore, data on the walking activity levels in flightless strains are important for the development of effective methods when releasing these agents in the field. Results of measurement of walking activity levels using an infrared actograph showed that walking activity levels during the daytime (but not nighttime) in both sexes of pure flightless strains tended to be lower than those of control strains. We also found that walking activity levels during the daytime for the F1 generation of hybrid strains, produced by reciprocal crossing between two pure flightless strains, were approximately equal to those of pure strains; the reduction in walking activity levels was not recovered by hybrid vigor. Our results indicate that the reduction in walking activity levels in the pure flightless strains was not caused merely by inbreeding depression stemming from the artificial selection process. Instead, potentially flight ability and walking activity levels in this species may be controlled by the pleiotropic effect of a gene.     

Control of Aphis gossypii and Myzus persicae (Hemiptera: Aphididae) by a flightless strain of Harmonia axyridis (Coleoptera: Coccinellidae) on green pepper plants in open fields

The cotton aphid Aphis gossypii Glover and the green peach aphid Myzus persicae (Sulzer) are economically important pests with a worldwide distribution. We evaluated the efficacy of releasing a flightless adult strain of the multicolored Asian lady beetle Harmonia axyridis (Pallas) as a control measure against these aphids on green pepper plants in open fields. Flightless H. axyridis adults were observed on the green pepper plants in the releasing plots throughout the experimental period and were found to be effective biocontrol agents, markedly decreasing the numbers of aphids. These results suggest that adults of this flightless strain of H. axyridis are effective in controlling aphids on green pepper plants in open fields.     

Singing on the wings! Male wing fanning performances affect female willingness to copulate in the aphid parasitoid Lysiphlebus testaceipes (Hymenoptera: Braconidae: Aphidiinae)

Lysiphlebus testaceipes (Hymenoptera: Braconidae: Aphidiinae) is a generalist endoparasitoid attacking more than 100 aphid species. In L. testaceipes, wing fanning is a main male courtship display evoked by a female‐borne sex pheromone. However, no information is available on the characteristics and behavioral role of male fanning during courtship in this parasitoid. Here, the courtship behavior of a wild strain of L. testaceipes was quantified and the male wing fanning performances were analyzed through high‐speed video recordings and examined in relation to mating success. Courtship sequence of wild L. testaceipes did not substantially differ from that previously reported for other populations mass reared on aphids. We observed that the male courtship duration did not affect mating success. However, video analysis revealed that the males producing high‐frequency fanning signals achieved higher mating success over those that display low‐frequency fanning. Wing fanning before successful and unsuccessful courtship differed in amplitude of wing movements and alignment toward the mate, highlighting that frontal courtship positively influence the female mating decisions. This study increases knowledge on sexual behavior in a key parasitoid of aphids, highlighting the importance of wing fanning among the range of sensory modalities used in the sexual communication of L. testaceipes. From a practical point of view, this information is useful in L. testaceipes‐based biocontrol strategies, since it can help to establish parameters for quality checking of mass‐reared wasps over time.     

昆虫翅型分化的调控及翅多型性的进化

翅多型现象普遍存在于各昆虫类群,一些学者就昆虫翅多型进行了大量的研究工作。根据昆虫翅型的分化,可划分为长翅型和短翅型,长翅型具飞行能力,而短翅型不能飞行。一些昆虫种类,如蚜虫,出现无翅个体,被称为无翅型。除飞行能力外,长翅型和短翅型在行为、生理等方面也存在差异。文章主要就环境因素对翅型分化的影响、翅多型的内分泌控制机理、翅多型的遗传机制及其进化等作一概述。     

FLIGHTLESSNESS IN STEAMER-DUCKS (ANATIDAE: TACHYERES): ITS MORPHOLOGICAL BASES AND PROBABLE EVOLUTION

Flightlessness in Tachyeres is caused by wing-loadings in excess of 2.5 g·cm^–2, which result from the large body size and small wing areas of the flightless species. Reduced wing areas of flightless species are related to absolutely shorter remiges, and to relatively or absolutely shortened wing bones, although these reductions differ among species. Reduced lengths of the ulna, radius, and carpometacarpus are associated most strongly with flightlessness. Pectoral muscles and the associated sternal keel are well developed in all species of Tachyeres, largely because of the use of wings in “steaming,” an important locomotor behavior. Relative size of these muscles was greatest in largely flighted T. patachonicus; however, sexual dimorphism in wing-loadings results in flightlessness in some males of this species. Proportions in the wing skeleton, intraspecific allometry, and limited data on growth indicate that the relatively short wing bones and remiges of flightless Tachyeres are produced developmentally by a delay in the growth of wing components, and that this heterochrony may underlie, in part, skeletal sexual dimorphism. Increased body size in flightless steamer-ducks is advantageous in territorial defense of food resources and young, and perhaps diving in cold, turbulent water; reductions in wing area probably reflect refinements for wing-assisted locomotion and combat. Flightlessness in steamer-ducks is not related to relaxed predation pressure, but instead was permitted selectively by the year-round habitability of the southern South American coasts. These conditions not only permitted the success of the three flightless species of Tachyeres, but at present may be moving marine populations of T. patachonicus toward flightlessness.     

微波辐射对桃蚜生长发育和繁殖的影响

【目的】研究筛选对桃蚜Myzus persicae有致死作用的安全微波频率和照射时长,以为探究新型物理防蚜技术,弥补化学防治上的缺陷提供参考依据。【方法】在暗箱中,应用微波发射仪分别发射1375, 2 750, 5 500和11 000 MHz 4个不同频率的微波照射桃蚜1日龄无翅成蚜,每个频率的照射时长分别为15, 30, 60和120 s;照射后在人工气候箱中饲养,分别于照射后8, 24, 48和72 h观察其生长发育及繁殖状况,统计桃蚜死亡率、繁殖力(累计产蚜量)及子代有翅蚜率。【结果】4个不同频率的微波分别在4个不同照射时长下,对桃蚜1日龄无翅成蚜的死亡率、繁殖力和子代翅型分化都有不同程度的影响。照射后72 h, 5 500 MHz微波照射时间为15 s时对桃蚜1日龄无翅成蚜的致死作用最强,死亡率达到55.00%,在照射时间为30和120 s时可抑制子代桃蚜向有翅蚜的分化。2 750 MHz微波照射30和60 s时促进桃蚜1日龄成蚜繁殖,照射30 s时繁殖力最强,而照射15和120 s时却表现为抑制繁殖,且2 750 MHz微波照射30 s能抑制子代桃蚜向有翅蚜分化。【结论】微波辐射能够影响桃蚜1日龄成蚜的存活、繁殖和子代翅型分化。本研究初步筛选出了对桃蚜1日龄无翅成蚜有致死作用的微波频率和照射时长。     

The interplay between density- and trait-mediated effects in predator-prey interactions: a case study in aphid wing polymorphism

Natural enemies not only influence prey density but they can also cause the modification of traits in their victims. While such non-lethal effects can be very important for the dynamic and structure of prey populations, little is known about their interaction with the density-mediated effects of natural enemies. We investigated the relationship between predation rate, prey density and trait modification in two aphid-aphid predator interactions. Pea aphids (Acyrthosiphon pisum, Harris) have been shown to produce winged dispersal morphs in response to the presence of ladybirds or parasitoid natural enemies. This trait modification influences the ability of aphids to disperse and to colonise new habitats, and hence has a bearing on the population dynamics of the prey. In two experiments we examined wing induction in pea aphids as a function of the rate of predation when hoverfly larvae (Episyrphus balteatus) and lacewing larvae (Chrysoperla carnea) were allowed to forage in pea aphid colonies. Both hoverfly and lacewing larvae caused a significant increase in the percentage of winged morphs among offspring compared to control treatments, emphasising that wing induction in the presence of natural enemies is a general response in pea aphids. The percentage of winged offspring was, however, dependent on the rate of predation, with a small effect of predation on aphid wing induction at very high and very low predation rates, and a strong response of aphids at medium predation rates. Aphid wing induction was influenced by the interplay between predation rate and the resultant prey density. Our results suggests that density-mediated and trait-mediated effects of natural enemies are closely connected to each other and jointly determine the effect of natural enemies on prey population dynamics.     

Adult Coccinellid Activity and Predation on Aphids in Spring Cereals

Improved understanding of coccinellid activity and predation on aphids in the field could clarify their potential in aphid biological control. Our objective was to determine the influence of abiotic and biotic factors on activity and predation by adults of three coccinellid species (Hippodamia convergens Guerin-Meneville, H. tredecimpunctata tibialis (Say), and Coleomegilla maculata DeGeer) in spring cereal fields. The proportion of time coccinellids spent searching was correlated with air temperature, aphid density, and time of day. The relationship between searching and these variables differed among species. Mean walking speed ranged from 66.4 cm/min for C. maculata to 83.2 cm/min for H. tredecimpunctata and increased with temperature for all species. The frequency of short flights (<2 m) by beetles increased with temperature and decreased with increasing aphid density for all species, but the relationship of short flight frequency to these variables differed among species. The frequency of long flights (>2 m) was similar for all species and influenced by temperature and calendar date. The frequencies with which aphids were encountered and eaten were correlated with aphid density and temperature for H. convergens and H. tredecimpunctata. Despite over 250 h spent observing adult coccinellid behavior in the field, predation data were insufficient to develop a useful predation model.