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.     

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.     

Intraguild interactions and aphid predators: biological efficiency of Harmonia axyridis and Episyrphus balteatus

Introductions of the harlequin ladybird Harmonia axyridis into Belgium for aphid biological control have been followed by declines in native aphid natural enemies. We first examined, in laboratory and field conditions, the impact of larval mobility of either H. axyridis or Episyrphus balteatus, the most abundant native hoverfly in central Europe, on aphid suppression. The hoverfly larvae consumed more aphids (Megoura viciae) in a short term, whereas the ladybird ones were more efficient in a long term. We second investigated the intraguild interactions between H. axyridis and E. balteatus larvae and adults. In larva pairings between the two species in laboratory microcosms containing aphid (M. viciae) infested broad bean (Vicia faba) plants, H. axyridis had an intraguild predation (IGP) advantage over the hoverfly. When conspecific larvae were paired together on aphid‐infested plants, no cannibalism between them was detected. The presence of either H. axyridis or E. balteatus larvae on aphid‐infested plants negatively influenced the ovipositional behaviour of H. axyridis and E. balteatus females; lower numbers of laid eggs were recorded compared to control treatment. Moreover, eggs laid by E. balteatus females were also dropped as victims of predation mainly by H. axyridis larvae. Our results suggest that while the exotic ladybird was more efficient in aphid biological control, larvae and eggs of the native hoverfly species face increased IGP by H. axyridis, which would contribute, as a consequence, to the decline in E. balteatus population following invasion.     

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.     

Vulnerability of larvae of two species of aphidophagous ladybirds, Adalia bipunctata Linnaeus and Harmonia axyridis Pallas, to cannibalism and intraguild predation

Vulnerability of larvae of two species of aphidophagous ladybirds, Adalia bipunctata Linnaeus and Harmonia axyridis Pallas, to cannibalism and intraguild predation was assessed in the laboratory. In the first experiment, a first instar of one of the two above species was kept with a fourth instar of the other species in a Petri dish. The number of times each first instar larva was encountered by the fourth instar larva and the fate of the first instar was determined over a period of 10 min. The fourth instar larvae captured and killed all the first instar larvae of their own species at the first encounter. However, when presented with fourth instar larvae of the other species the first instar larvae of A. bipunctata and H. axyridis were encountered 6.4 ± 1.3 ( n  = 10) and 19.4 ± 2.1 ( n  = 10), respectively. In this experiment no first instar larvae of H. axyridis , whereas all those of A. bipunctata , were killed.     

Suppression of aphids on strawberry by augmentative releases of larvae of the lacewing Chrysoperla carnea (Stephens)

In laboratory feeding experiments, larvae of Chrysoperla carnea consumed up to 790 Chaetosiphon fragaefolii during their development. In gauzehouse experiments, releases of C. carnea larvae significantly reduced numbers of C. fragaefolii on potted strawberry plants. In open field experiments numbers of C. fragaefolii were significantly reduced at release rates of eight chrysopid larvae per plant, but a release experiment on larger strawberry plants grown under protection did not give a significant reduction in aphid numbers, even at a release rate of 25 larvae per plant.     

Extrafloral nectar of Hibiscus cannabinus promotes adult populations of Harmonia axyridis

High numbers of Harmonia axyridis adults were observed even when aphid populations were low or absent in kenaf (Hibiscus cannabinus) fields. Compared to a control group given access to water alone or cotton aphids and water, longevity of H. axyridis adults provided with kenaf leaves containing extrafloral nectar significantly increased.     

The evolution of chemical defenses along invasion routes: Harmonia axyridis Pallas (Coccinellidae: Coleoptera) as a case study

The evolution of increased competitive ability (EICA) hypothesis (Blossey & Nötzold, 1995 ) postulates that escaping from coevolved enemies increases invaders fitness by energy reallocation from defenses and immunity to growth and reproduction. In this context, we evaluated the evidence of evolutionary change in invasive populations of Harmonia axyridis Pallas (Coccinellidae: Coleoptera). We measured egg defenses—cocktail of hydrocarbons on the egg's surface flagging egg toxicity and the concentration of the main alkaloid harmonine—in individuals from three populations along the invasion route (Japan: native, United States: introduced more than 30 years ago, South Africa: introduced in the early 2000s) in a common garden experiment. Our results support the EICA hypothesis: We found changes along the invasion route in the profiles of the hydrocarbons coating the eggs’ surface and a decrease in the concentration of harmonine in eggs from the most recent invasive South African population compared to the long established in the United States and the native Japanese ones.     

Nitrogen fertiliser affects the functional response and prey consumption of Harmonia axyridis (Coleoptera: Coccinellidae) feeding on cereal aphids

Predator–prey interactions are influenced by nitrogen availability. Wheat (Triticum aestivum cv. Solstice) plants were provided with four levels of nitrogen and examined the responses of coccinellid predator, Harmonia axyridis to cereal aphids, Rhopalosiphum padi and Sitobion avenae. Increased nitrogen application improved nitrogen contents of the plants and also the body weight of cereal aphids feeding on them. In no‐choice feeding trials, H. axyridis consumed more aphids on low fertilised plants, suggesting a compensatory consumption to overcome reduced biomass (lower aphid size). Total biomass devoured by H. axyridis on all nitrogen fertiliser treatments was not statistically different. Logistic regression analysis of the proportion of prey consumed demonstrated that all developmental stages (larval and adult) of H. axyridis exhibited the type II functional response on all nitrogen fertiliser treatments. The rate of successful search (a′) of third and fourth instars and adults were the same across all fertiliser treatments suggesting that nitrogen fertilisation did not affect a′. Maximum handling time for the first instars of H. axyridis on R. padi (3.81 h^?1) and S. avenae (4.59 h^?1) was on the highest nitrogen treatment while minimum handling time was for the adults of H. axyridis on R. padi (0.20 h^?1) and S. avenae (0.20 h^?1) on the lowest nitrogen treatment. Handling time varied at varying fertiliser treatments within all instars and affected the predator's efficiency. The functional response curve, rate of successful search and handling time provide the information needed to understand the predator–prey interaction between H. axyridis and these cereals aphids. This could lead to the development of a better strategy for the biological control of R. padi and S. avenae at any particular level of nitrogen fertiliser regime in the field crops.     

Pre-release packing and chilling reduce host-searching ability of the parasitoid Diachasmimorpha longicaudata used in the augmentative control of tephritid flies

Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae) is a solitary parasitoid used in augmentative releases to control Tephritidae (Diptera) fruit flies of economic importance. Pre-release process includes packing adult parasitoids in cages at high densities and expose them to a temperature of 2 ± 2 °C during 105 min. In this process, females’ antennae may be damaged resulting in a reduction in their host-searching ability and fecundity. Here we measured, for five consecutive days after chilling, the searching ability and fecundity of parasitoids with damaged (D) and undamaged (ND) antennae compared with parasitoids that were not chilled. Female individual responses to fruit infested by Anastrepha spp. was determined in an olfactometer. Latency in the response and latency in making a choice were recorded. Additionally, groups of 30 females were used to measure their ability to find hosts in infested fruit in the laboratory. Fecundity was determined by using artificial oviposition units with Anastrepha ludens (Loew) larvae. In the olfactometer test, ND had lower response than control females during the 1st and 2nd days after chilling. However, no difference in the response was observed between ND and D and the control females on the 5th day. Additionally, chilled females showed a longer latency of response to infested fruit than females of the control treatment when tested in groups. However, after a 24–48 h period, no difference between D and ND and control females was observed. Our results showed similar searching ability and fecundity among parasitoids of the three tested conditions at individual and at group levels. We conclude that pre-release chilling reduces female searching ability only for the first 1–2 days after chilling.     

Effect of floral and extrafloral resources on predation of Aphis spiraecola by Harmonia axyridis on Apple

Flowering companion plants and plants producing extrafloral nectar are being proposed to enhance biological control in apple (Malus domestica Borkh.) orchards. This experiment evaluated the impact of floral and extrafloral resources on predation of spirea aphid (Aphis spiraecola Patch) on apple by adult Harmonia axyridis (Pallas) under greenhouse conditions. Predation of spirea aphids was not affected by the presence of flowering buckwheat (Fagopyrum esculentum) as compared with either buckwheat with flowers removed or an uninfested apple shoot. However, there was a significant reduction in predation of spirea aphids on an apple shoot in the presence of a peach shoot with extrafloral nectar glands compared with either a peach shoot of the same cultivar without nectar glands or an uninfested apple shoot. These findings demonstrate that alternative food resources potentially could interfere with rates of biological control and, therefore, need to be carefully evaluated before incorporating in an orchard design. More studies are needed to adequately gauge the net effects of adding floral or extrafloral resources in orchards for conservation biological control.     

Ecology and biological control application of multicoloured Asian ladybird, Harmonia axyridis: A review

The ecology of and biological control by multicoloured Asian ladybird beetle, Harmonia axyridis (Pallas) are reviewed. Our emphasis is on assembling and interpreting information on general characteristics, invasion and establishment, sexual activity, foraging and predation, development, survival and reproduction, predator-predator interactions, natural enemies, biocontrol, non-target effects and status of H. axyridis as a pest of fruits. Colonization of H. axyridis for aphid biocontrol in the USA have been successful in terms of its establishment, but its abundance is turning out to be a nuisance to humans. Its harmful non-target impact on beneficial organisms, humans and native species is becoming a debatable issue. The question on its present position, whether it is a biocontrol agent or pest, is a critical issue and discussed. Inferences from the empirical data are made and new avenues for future research are suggested.     

Improvement of quality control methods for augmentative releases of the fruit fly parasitoids,Diachasmimorpha longicaudata and Psyttalia fletcheri (Hymenoptera: Braconidae)

Criteria were established to improve quality control methods for augmentative releases of the opiine parasitoids, Diachasmimorpha longicaudata (Ashmead) and Psyttalia fletcheri (Silvestri). These included correlating puparial weight with adult emergence and sex ratio at the Honolulu rearing facility, and determining the effect of air shipments and field releases on parasitoid emergence and subsequent mortality. There was a positive relationship between the weight of 7–10‐day‐old host puparia and percentage of emergence for both D. longicaudata and P. fletcheri. Standardization of shipping methods included placement of ice blocks in the top levels of the ice chests, prompt shipment and pick‐up of samples, and cooling of puparia before shipment to minimize metabolic heat generated in the samples, and to delay emergence of samples. Before standardization, emergence losses of up to 58% were observed for D. longicaudata and 18% for P. fletcheri. When shipping methods were standardized, emergence was no longer reduced. In addition, low emergence rates were associated with reduced flight propensity of D. longicaudata (R_s = ‐ 0.45 at Kilauea and ‐ 0.54 at Kealia). At the two release sites, 88–95% of adult D. longicaudata that did not escape the release containers were males.     

异色瓢虫生物生态学研究进展

原产于亚洲的异色瓢虫[Harmonia axyridis Pallas(Coleoptera:Coccinellidae)]是最重要的捕食性瓢虫种类之一,被广泛应用于农林业害虫的生物防治.本文综合分析了国内外近几十年对异色瓢虫的研究成果,对其重要的生物学及生态学特性进行了归纳,主要涉及生活史、繁殖行为及策略、捕食行为和自残行为等,分析了相关研究对其应用前景的影响.基于异色瓢虫的人工饲养、农药交互作用以及入侵生态影响等的总结,提出了预防异色瓢虫造成生态不平衡的具体措施.     

Antennal sensory organs and glands of the harlequin ladybird,Harmonia axyridis

Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) is a sub‐cosmopolitan species. Native to Asia, it has been released during the 20th century for classical and augmentative biological control of several herbivorous insects, mostly aphids and coccids. Despite its recognized positive impact on biological control, H. axyridis is now considered among the most dangerous invasive species in Europe and in most places where it has established. This is mostly due to its ability to reduce the populations of native predatory species of the same trophic guild. When exploring a new area, H. axyridis adults use semiochemical cues to acquire information about the habitat. Presumably, these cues are perceived by the sensilla located on the antennae. Surprisingly, in spite of the huge literature existing on H. axyridis, the antennal sensory organs have been poorly characterized. Here, we used scanning and transmission electron microscopy (SEM, TEM) techniques to study H. axyridis antennae, with focus on the various types of sensilla and their distribution in male and female individuals. The presence of various classes of antennal sensilla belonging to the main types described in insects (chemoreceptors, mechanoreceptors, and thermo‐hygroreceptors) was highlighted, as well as the widespread presence of antennal glands. The investigations showed some peculiar characteristics not known in Coccinellidae, such as the concentration of sensory structures at the level of the distal part of the apical antennomere and the discovery of antennal glands associated with it. No sexual dimorphism was revealed, neither for the general structure of the antenna (similar number of antennomeres and presence of modifications), nor for the total length and width of the antenna, the relative size of the antennomeres, the types of antennal sensilla, of their distribution and abundance. The potential relevance of these sensory structures and antennal glands, reported for the first time in Coccinellidae, is discussed in the context of intra‐ and interspecific communication.     

Dispersion of flightless adults of the Asian lady beetle, Harmonia axyridis, in greenhouses containing cucumbers infested with the aphid Aphis gossypii: effect of the presence of conspecific larvae

Nezara viridula (L.) (Heteroptera: Pentatomidae) recently expanded its distribution range in Japan and reached Osaka. In the southern temperate zone, the species overwinters in the adult stage and reproductive diapause is associated with a body colour change from green to russet. In Osaka, the reproductive diapause is only induced in September–October and nymphs from late egg masses are destined to die during winter. However, the fate of adults emerging late in the season remained unknown. Survival, body colour change, and post‐diapause reproduction were studied under quasi‐natural conditions in Osaka in 1999–2000 in those adults that attained adulthood as late as in November. Two experimental cohorts were used: in the Outdoor cohort, insects were reared outdoors starting in their second instar (28 September); in the Laboratory cohort, nymphs and subsequently adults were reared from the same day under diapause‐inducing conditions (L10:D14 at 25 °C), then acclimatized (5 days at 20 °C and 5 days at 15 °C; L10:D14) and transferred outdoors on 1 December. Adults in both cohorts did not reproduce in autumn and survived the winter with a low mortality. More than 20% of adults in the Outdoor cohort failed to change body colour from green to russet during winter, apparently because of the low ambient temperature, suggesting that the environmental conditions required for colour change do not completely coincide with those required for diapause induction, and that the colour of the adults is not always a reliable indicator of diapause in this species. After overwintering, females from the Outdoor cohort produced significantly fewer egg masses and eggs and had a significantly shorter period of oviposition than females that entered diapause under short‐day conditions in the Laboratory cohort. Thus, if progeny from the late egg masses attain adulthood late in the autumn, these adults have high chances of successful overwintering, but their reproductive output after the winter diapause is significantly reduced.     

Effects of augmentative releases of eggs and larvae of the ladybird beetle, Adalia bipunctata, on the abundance of the rosy apple aphid, Dysaphis plantaginea, in organic apple orchards

The impact of augmentative releases of larvae and eggs of the indigenous ladybird beetle Adalia bipunctata (L.) (Coleoptera: Coccinellidae) against the rosy apple aphid Dysaphis plantaginea Pass. (Homoptera: Aphididae), a major pest insect on apple trees, was assessed in field experiments in Switzerland, during 1997. In a first experiment, eggs and larvae were released on 3-year old apple trees infested with five aphids at four different predator-prey ratios (0:5, 1:5, 1:1, 5:1). In a second experiment, eggs and larvae were released at a predator-prey ratio of 5:1 on branches of apple trees naturally infested with aphids. In both experiments, the interaction with ants was taken into account and the releases were done at two different times in spring. The results showed that an augmentative release of larvae significantly prevented the build-up of colonies of D. plantaginea. Significant reductions in aphid numbers were recorded at the two highest predator-prey ratios, 1:1 and 5:1. Larvae were efficient just before flowering of apple trees at a time when growers normally have to spray their trees. On trees where ants were present the larvae of A. bipunctata were significantly less efficient. Effects of eggs of A. bipunctata, however, were less reliable. At the first date of release (5 April), they did not hatch, probably as a consequence of bad weather conditions.     

Predation and functional response of the multi-coloured Asian ladybeetle Harmonia axyridis on the adult Asian citrus psyllid Diaphorina citri

Diaphorina citri (Hemiptera: Liviidae) is a vector for the citrus Huanglongbing greening disease, which can reduce crop yields. Harmonia axyridis (Coleoptera: Coccinellidae) is known to prey on D. citri nymphs; we investigated the predation capacity and functional response of H. axyridis on adult D. citri. H. axyridis larvae exhibited Holling’s type II functional response to different densities of adult D. citri. For second, third and fourth instar H. axyridis larvae, the successful attack rates were 0.75?±?0.22, 1.06?±?0.11, and 1.04?±?0.26, respectively; the handling times were 18.08?±?5.37, 0.45?±?0.07, and 0.24?±?0.07?h, respectively; and the estimated maximum predation rates were 4, 54, and 102, respectively. Fourth instar larvae had the lowest handling time. Adult H. axyridis consumed more D. citri adults maintained at 15–20°C than at 30–35°C, with an optimal temperature of 17.28°C. More adults were consumed during the day than at night, with peak consumption between 12:00 and 14:00?h, not differing significantly differ between predator genders. Adult H. axyridis reared on the aphid Acyrthosiphon pisum were tested for D. citri predation; these H. axyridis had successful attack rates, handling times, and estimated maximal predation rates of 0.66?±?0.18, 0.82?±?0.26?h, and 29, respectively. Conversely, those fed and tested on D. citri had corresponding rates of 0.99?±?0.17, 0.38?±?0.12?h, and 63, respectively. Significant H. axyridis predation on adult D. citri indicated its enhanced role in suppressing both nymph and adult D. citri.     

Density dependence and the augmentative release of egg parasitoids against graminaceous stalk borers

Abstract. 1. The augmentative release of Trichogranznza species for the biological control of graminaceous stalkborers is reviewed.
2. Previous experiments indicate strong density dependence acting on the early larval stages of the sorghum stalkborer ( Chilo partellus ). These data are described by a simple model for density dependence, whose properties are briefly described.
3. The effects upon the total mortality of different levels of egg parasitism are discussed when combined with density dependent larval losses that vary from under- to over-compensating.     

Toxicity of the aphid Aulacorthum magnoliae to the predator Harmonia axyridis (Coleoptera: Coccinellidae) and genetic variance in the assimilation of the toxic aphids in H. axyridis larvae

Larvae of the ladybird Harmonia axyridis are reported to suffer high mortality when they are fed with the aphid Aulacorthum magnoliae associated with the elder Sambucus sieboldiana. In the present study we first examined whether aphid toxicity to H. axyridis was altered when the aphids were reared on different host plants, and second whether some ladybird families could adapt specially to the toxic aphids. Ladybird larvae from each egg batch were divided into two groups; one group was fed with A. magnoliae reared on potato, and the other group was fed with A. magnoliae reared on elder. The ladybird larvae fed with elder aphids suffered significantly higher mortality and grew more slowly than did larvae fed with potato aphids. This result indicates that A. magnoliae aphids absorbed toxic substances or their precursors from S. sieboldiana. We suggest that host association of A. magnoliae with the primary host plant S. sieboldiana has been maintained because of the advantage of deterring predation. Significant and positive correlation was detected across H. axyridis sib families between the mean weight of larvae fed with elder aphids and the mean weight of larvae fed with potato aphids. The hypothesis that some ladybird families adapt specially to the toxic aphids was not supported. However, the available evidence showed that a large amount of genetic variance in performance is maintained in a wild population of the ladybird H. axyridis.