Dropping behaviour of larvae of aphidophagous ladybirds and its effects on incidence of intraguild predation: interactions between the intraguild prey, Adalia bipunctata (L.) and Coccinella septempunctata (L.), and the intraguild predator, Harmonia axyridis Pallas

Abstract.  1. Two experiments were performed in the laboratory to assess the behaviour of dropping from a host plant as a defence against intraguild predation in aphidophagous ladybird larvae.
2. In the first experiment, encounters were observed on bean plants between fourth instars of the intraguild predator species, Harmonia axyridis , and first instars of two other ladybird species, Adalia bipunctata (L.) and Coccinella septempunctata (L.). The percentages of first instars of the latter two species that dropped from the plant in response to attack differed dramatically, with 47.5% of C. septempunctata first instars dropping vs. 0% of A. bipunctata .
3. In the second experiment, first instars of A. bipunctata or C. septempunctata and a fourth instar of H. axyridis were allowed to forage together on bean plants for 3 h. During this time, 44.3% of C. septempunctata larvae dropped from the plant, but less than 2% of A. bipunctata larvae did so. In contrast, 95.0% of A. bipunctata larvae fell victim to intraguild predation by H. axyridis vs. only 54.5% of C. septempunctata larvae.
4. The significance of dropping behaviour of ladybird larvae as a defence against intraguild predation, and the relationship of dropping behaviour to species-specific habitat affinity of ladybirds, is discussed.     

Interactions between introduced and native predatory ladybirds (Coleoptera, Coccinellidae): factors influencing the success of species introductions

Abstract.  1. Why some exotic species invade successfully while others do not is poorly understood. This study focuses on the inability of the exotic predatory ladybird Adalia bipunctata (L.) (Coleoptera, Coccinellidae) to establish and spread in Japan. In particular, this study considers the interactions between A. bipunctata and three native Japanese ladybird species, Harmonia axyridis Pallas, Coccinella septempunctata Linn., and Propylea japonica Mulsant.
2. The number of aphids occurring on the host plants declined dramatically over the course of larval development in the presence of H. axyridis or C. septempunctata . In contrast, many aphids remained at the end of the experiment when only A. bipunctata or P. japonica was present.
3. The survivorship of A. bipunctata from second instar to adult was significantly reduced in the presence of H. axyridis , but not in the presence of C. septempunctata or P. japonica . Most deaths were the result of intra-guild predation when H. axyridis or C. septempunctata larvae were present. Larvae of H. axyridis and C. septempunctata suffered very high mortality in this experiment, but survived better when co-occurring with A. bipunctata than when occurring only with conspecifics. In contrast, P. japonica survived better when occurring with conspecifics than with A. bipunctata .
4. The finding that larvae of the exotic species A. bipunctata died at high rates from intra-guild predation by the native Japanese ladybirds H. axyridis and C. septempunctata may bear on the question of why A. bipunctata has not established more successfully in Japan whereas H. axyridis and C. septempunctata have been very successful in establishing themselves in North America.     

Effect of cannibalism and predation on the larval performance of two ladybird beetles

The relative impact of cannibalism and predation on the development and survival of fourth instar larvae was assessed in two species of aphidophagous ladybird beetles, Coccinella septempunctata and Harmonia axyridis. The effect of eating aphids, conspecific larvae or heterospecific larvae on larval performance differed in the two species: aphids were the best food for C. septempunctata and survival of C. septempunctata larvae was significantly lower when offered heterospecific larvae rather than conspecific larvae or aphids as food, indicating that H. axyridis larvae were not suitable food for C. septempunctata. However, as the different foods did not affect the larval performance of H. axyridis, this species appears to be more polyphagous. Both intraguild predation by the aggressive larvae of H. axyridis and the polyphagous food habit of this species may account for its dominance in ladybird assemblages and its displacing other ladybird beetles in several places in the world.     

Voracity and feeding preferences of two aphidophagous coccinellids on Aphis citricola and Tetranychus urticae

Voracity and feeding preferences of adult Coccinella septempunctata L. and Harmonia axyridis Pallas (Coleoptera: Coccinellidae, tribe Coccinellini) were evaluated in the laboratory on a common prey, the spirea aphid, Aphis citricola van der Goot (Homoptera: Aphididae), and on the twospotted spider mite, Tetranychus urticae Koch (Acarina: Tetranychidae), a prey previously unrecorded for these two predators. The experiments were carried out in the laboratory on apple saplings (Malus domestica Borkhausen). Adult males and females of H. axyridis consumed significantly more mites than adults of C. septempunctata. For H. axyridis, males consumed 41.3 spider mites in 24 h and females 48.4, whereas for C. septempunctata males consumed 14.1 prey and females 15.2. The consumption of spirea aphids by the males was similar for the two species. Consumption by the females was significantly greater for H. axyridis (46.5) than for C. septempunctata (22.2). The two coccinellids showed a significant preference for A. citricola in the presence of T. urticae. This preference was more pronounced for C. septempunctata. The total number of prey consumed and the percentage of exploited biomass decreased significantly for C. septempunctata and stayed relatively constant for H. axyridis as the number of mites increased in the prey ratio. Our results suggest that T. urticae is only an alternative prey for both predators, and that H. axyridis should be more efficient than C. septempunctata in a prey assemblage with aphids and mites.     

Intraguild predation behaviour of ladybirds in semi-field experiments explains invasion success of Harmonia axyridis

Harmonia axyridis has been introduced as a biological control agent in Europe and the USA. Since its introduction, it has established and spread, and it is now regarded as an invasive alien species. It has been suggested that intraguild predation is especially important for the invasion success of H. axyridis. The aim of this study was to compare the intraguild predation behaviour of three ladybird species (Coccinella septempunctata, Adalia bipunctata, and H. axyridis). Predation behaviour was investigated in semi-field experiments on small lime trees (Tilia platyphyllos). Two fourth-instar larvae placed on a tree rarely made contact during 3-hour observations. When placed together on a single leaf in 23%-43% of the observations at least one contact was made. Of those contacts 0%-27% resulted in an attack. Harmonia axyridis attacked mostly heterospecifics, while A. bipunctata and C. septempunctata attacked heterospecifics as often as conspecifics. In comparison with A. bipunctata and C. septempunctata, H. axyridis was the most successful intraguild predator as it won 86% and 44% of heterospecific battles against A. bipunctata and C. septempunctata respectively, whilst A. bipunctata won none of the heterospecific battles and C. septempunctata won only the heterospecific battles against A. bipunctata. Coccinella septempunctata dropped from a leaf earlier and more often than the other two species but was in some cases able to return to the tree, especially under cloudy conditions. The frequency with which a species dropped did not depend on the species the larva was paired with. The results of these semi-field experiments confirm that H. axyridis is a strong intraguild predator as a consequence of its aggressiveness and good defence against predation from heterospecific species. The fact that H. axyridis is such a strong intraguild predator helps to explain its successful establishment as invasive alien species in Europe and the USA.     

Relationships Between Attack and Escape Rates, Cannibalism, and Intraguild Predation in Larvae of Two Predatory Ladybirds

We compared incidences of cannibalism and intraguild (IG) predation (IGP) and quantified attack and escape rates—mechanisms which possibly account for the difference in incidences of these interactions—in laboratory experiments with Harmonia axyridis and Coccinella septempunctata. There was a tendency for H. axyridis to act as an IG predator and C. septempunctata as an IG prey. Cannibalism was also often observed in both species. The incidences of both IGP and cannibalism were different between the species. The average attack rates of C. septempunctata were less than 20%, but those of the more aggressive H. axyridis exceeded 50%. Larvae of both species attacked conspecifics and heterospecifics H. axyridis larvae successfully escaped when attacked by both conspecifics and by heterospecifics, while larvae of C. septempunctata escaped from attacks of conspecifics but not from those of heterospecifics. Thus the aggressive behavior of H. axyridis, in particular, of the third and fourth instars, negatively affects the larval survival of C. septempunctata. It may contribute to the dominance of H. axyridis in ladybird assemblages and its displacement of other ladybird species in several places in the world.     

Toxicity of plant essential oil vapours to aphid pests and their coccinellid predators

The comparative toxicity of five essential oil vapours was tested against four aphid species, the black bean aphid Aphis fabae, the pea aphid Acyrthosiphon pisum, the chrysanthemum aphid Macrosiphoniella sanborni, the green peach aphid Myzus persicae and on two of the most common coccinellid predators, the seven-spotted ladybird Coccinella septempunctata and the two-spotted ladybird Adalia bipunctata. All essential oils were highly toxic to the aphid species tested with LC₅₀ and LC₉₉ values ranging between 0.17 and 1.92 and 0.44 and 4.83 µL/L air, respectively, depending on the aphid species and on the essential oil. Coccinellid predators were also highly susceptible to the essential oil vapours and the selective toxicity ratio varied depending on aphid species, coccinellid predator and essential oil. The possibilities for the utililization of essential oils as aphicides, especially in IPM programmes in glasshouses are discussed with regard to the present findings.     

美国杏李园瓢虫群落组成及生态位

对美国杏李园中瓢虫的种群动态和生态位进行研究,结果表明,异色瓢虫、龟纹瓢虫、多异瓢虫为优势种群,黑缘红瓢虫、红点唇瓢虫、七星瓢虫、马铃薯瓢虫、深点食螨瓢虫、二星瓢虫种群密度长时间处于稳定状态。马铃薯瓢虫占据生态位最宽,对美国杏李树危害时间较长。红点唇瓢虫和七星瓢虫的生态位重叠较高,出现频率高。在瓢虫类天敌中,生态位宽度越宽的种类往往数量较低,且持续时间较长,对害虫种群的控制程度较低,生态位宽度较低的种类出现时间较短,短时间内种群数量较高,可以控制害虫种群数量。     

厦门园林植物有益瓢虫调查研究

据调查,厦门市园林植物共有瓢虫33种,隶属于22属。其优势种群为七星瓢虫(Coccinella septempunctata)、小红瓢虫(Rodolia pumila)、大红瓢虫(R. rufopilosa)、稻红瓢虫(Micraspis discolor)、异色瓢虫(Harmonia axyridis)、二星瓢虫(Adalia bipunctata)。文中提出保护与利用有益瓢虫的措施。     

Intraguild predation of the aphid pathogenic fungus Pandora neoaphidis by the invasive coccinellid Harmonia axyridis

Abstract.  1. The ladybird Harmonia axyridis is an invasive alien species in many countries and is predicted to have a negative impact on native biodiversity. However, little is known on the status of this aphidophage as an intraguild predator of natural enemies of aphids such as insect-pathogenic fungi.
2. The study assessed the predation of the aphid-specific pathogenic fungus Pandora neoaphidis by adult and larval H. axyridis collected from the U.K. (an invasive population) and Japan (a native population) relative to that of the ladybird Coccinella septempunctata (native to the U.K.) and the non-U.K. C. septempunctata subspecies brucki that were either starved or unstarved.
3. Overall, predation of uninfected aphids was greater than infected aphids and, when given a choice, a preference for aphids was shown. However, the extent of this preference was dependent on the species and origin of the coccinellid. Harmonia axyridis (U.K.) consumed the greatest quantity of fungal cadavers and showed little preference for uninfected aphids over infected aphids. In contrast, C. septempunctata rarely consumed infected aphids. Life stage had no direct effects on predation but starved coccinellids consumed more uninfected aphids than infected aphids.
4.  Harmonia axyridis (U.K.) is a stronger intraguild predator of P. neoaphidis cadavers than the native species C. septempunctata and, therefore, may have an impact on the occurrence and persistence of P. neoaphidis . The differences in intraguild predation by H. axyridis collected in the U.K. and those from Japan suggests that individuals that invaded the U.K. could have a different genetic profile to those in its native range.     

Differences between the 7-spot and 2-spot ladybird beetles (Coccinellidae) in their toxic effects on a bird predator

Abstract. 1. Experiments with nestling blue tits Parus caeruleus L. examined the effects of feeding them 7-spot ladybird Coccinella septempunctata (L.), 2-spot ladybird Adalia bipunctata (L.) or controls Tenebrio sp.
2. A feeding rate of 51/3 7-spot ladybirds per day 'killed' nestlings within 2 days. Three of six nestlings fed at half this rate survived 4 days. In contrast, all experimental birds survived sixty-four 2-spot ladybirds fed over 4 days (equivalent by weight to the high 7-spot diet).
3. Nestlings fed 7-spot ladybirds also grew more slowly than birds fed 2-spot ladybirds. The latter birds showed no difference in weight gain from the controls although they begged more strongly for food.
4. Cadavers of birds fed 7-spot ladybirds showed evidence of severe liver damage.
5. The results indicate a substantial difference between the ladybird species in their toxicity to nestling blue tits. They support the hypothesis that 2-spot ladybirds are largely-edible, polymorphic Batesian mimics of well-protected, monomorphic species such as the 7-spot ladybird.     

Ladybird population dynamics in potato: comparison of native species with an invasive species, Harmonia axyridis

Following the detection of the harlequin ladybird, Harmonia axyridis, in 2003 in potato crops in Belgium, a study was carried out between 2004 and 2006 on the phenology of this species compared to native species in potato. The results confirmed the success of H. axyridis, with high population levels in 2004 and 2005. In 2006, aphid populations were very low and no H. axyridis larvae were sampled in potato, but the indigenous species Coccinella septempunctata and Propylea quatuordecimpunctata were detected. A species by species comparison of the date of first larvae detection, the larvae population peak, and the difference between this peak and the aphid population peak was performed. Results showed a clear correlation between C. septempunctata and P. quatuordecimpunctata and potato aphids, with a delay of 3.5 and 6.5 days between the aphid and ladybird population peaks for the two native species. H. axyridis arrived 7–8 days after the two indigenous species and the larval peak population occurred 15.8 days after the aphid population peak. This meant that H. axyridis had to complete its larval development with very low aphid populations or even with no aphids at all. The reason for its late arrival and the possible food resources used by H. axyridis larvae are discussed.     

The role of vision and color in the close proximity foraging behavior of four coccinellid species

The role of vision and color in close-proximity foraging behavior was investigated for four species of lady beetles: Coccinella septempunctata, Hippodamia convergens, Harmonia axyridis, and Coleomegilla maculata. The effect of light level and color cues on consumption rates varied among the four predator species. The consumption rates of these predators on the pea aphid Acyrthosiphon pisum (Harris) was measured under light and dark conditions. C. septempunctata,H. convergens, and Ha. axyridis consumed significantly more aphids in the light than in the dark, while the consumption rate of Col. maculata was not affected by light level. Foraging ability was also measured on red and green color morphs of the pea aphid on red, green, and white backgrounds. C. septempunctata consumed significantly more of the aphid morph that contrasted with the background color, and showed no difference between morphs on the white background. H. axyridis consumed significantly more red morph aphids regardless of background. The remaining two species showed no difference in consumption rates on the two color morphs. The variation in the use of visual cues demonstrates how different species of predators can exhibit different foraging behaviors when searching for the same prey. Received: 4 August 1997 / Accepted: 3 February 1998     

Predation and avoidance behaviour in aphid‐ladybird interactions of native and invasive ladybirds in Europe

1. While detrimental effects of invasive predators on native species are well documented, we often lack a mechanistic understanding of the invasion success. Lack of prey avoidance behaviour can lead to higher consumption rates by invasive predators compared to native predators. This competitive advantage is expected to contribute to the invasion success of non‐native predators.
2. We compared aphid consumption and cue avoidance behaviour of aphids between four native ladybird species (Coccinella septempunctata, Adalia bipunctata, Propylea quatuordecimpunctata, and Hippodamia variegata) and the invasive Asian ladybird Harmonia axyridis.
3. The invasive H. axyridis and the native C. septempunctata consumed more aphids than the three smaller native ladybird species. In line with our expectations, aphids avoided leaves bearing cues of most native ladybird species but not of the invasive H. axyridis.
4. Our results indicate that body size rather than ladybird origin determined aphid predation rates. The lack of aphid avoidance behaviour towards cues of H. axyridis indicates that they were not able to recognise the chemical cues of the invasive predator.
5. Relatively large body size and the absence of cue avoidance in aphids might benefit the invasive H. axyridis, particularly in comparison to smaller native ladybird species. The absence of avoidance behaviour in aphids might lead to even higher predation rates of H. axyridis under more natural conditions.

     

七星瓢虫和异色瓢虫3变种成虫触角感器扫描电镜观察

七星瓢虫和异色瓢虫触角上分布粗大的毛状感器和短小的锥状感器。毛状感器分布于各个亚节,锥状感器主要密布于鞭节的末节端部。化感器的数量大小中顺序：七星瓢虫＞异色瓢虫显明变种＞异色瓢虫二斑变型和十九斑变种。     

Fungal plant endosymbionts alter life history and reproductive success of aphid predators

Endosymbionts occur in most plant species and may affect interactions among herbivores and their predators through the production of toxic alkaloids. Here, we ask whether effects of mycotoxins produced by the symbiosis of the fungal endophyte Neotyphodium lolii and the grass Lolium perenne are transmitted to the aphidophagous ladybird Coccinella septempunctata when feeding on cereal aphids Rhopalosiphum padi on infected plants. The larval development of coccinellids was extended, while their survival was reduced when feeding exclusively on aphids from infected plants. Ladybirds developing on aphids from infected plants showed reduced fecundity and impaired reproductive performance. Body size and symmetries of ladybird adults were not affected by the endophytes. Consistently strong, negative effects of endophytes on the lifetime performance of ladybirds indicates that mycotoxins are transmitted along food chains, causing significant damage for top predators. Such cascading effects will influence the population dynamics of aphid predators in the long term and could feedback to the primary plant producers.     

A comparative study on effects of normal versus elevated temperatures during preimaginal and young adult period on body weight and fat body content of mature Coccinella septempunctata and Harmonia axyridis (Coleoptera: Coccinellidae)

Two climate chamber experiments were performed to simulate the effects of global warming on life table parameters of coccinellids. We investigated the effects of two daily temperature profiles during preimaginal development (larval and pupal) and the young adult period (first 10 d) on body weight and fat body content of adult Coccinella septempunctata L. and Harmonia axyridis (Pallas) fed English grain aphids [Sitobion avenae (F.)] ad libitum: 1) normal, i.e., current daily temperatures in central Europe (T0: mean, 17.8°C; maximum, 21.8°C; minimum, 13.4°C) and 2) increased by 3K (T3: mean, 20.8°C; maximum, 25.5°C; minimum, 15.7°C). The first experiment was performed at the same temperatures (T0 or T3) during both periods to establish the responses of the two species to temperature. The second was conducted to identify the period (preimaginal or adult) in which the responses occurred and to confirm the results of the first experiment. Compared with normal temperatures (T0), elevated temperatures (T3) resulted in significant decreases in preimaginal development time and increases in aphid consumption rates in both species. C. septempunctata (10-d-old adults) had the highest weights when reared at T3, H. axyridis at T0. C. septempunctata was significantly heavier than H. axyridis in most cases, particularly in females. The body fat content of C. septempunctata was higher than that of H. axyridis at T0 and T3 temperatures. At T3 temperatures, fat accumulation in C. septempunctata increased, whereas that in H. axyridis remained relatively low. Body weight and fat body content of 10-d-old adults of both species seemed to be determined by temperature conditions during preimaginal development.     

Effect of emigration on cannibalism and intraguild predation in aphidophagous ladybirds

Abstract.  1. The incidence and timing of emigration, cannibalism, and intraguild predation of larvae of three aphidophagous ladybirds (Coleoptera: Coccinellidae), Harmonia axyridis Pallas, Coccinella septempunctata brucki Mulsant, and Propylea japonica Mulsant, relative to the presence of prey was determined in the laboratory in single- and mixed-species populations.
2. In single-species populations, 80% of the larvae of C. s. brucki emigrated prior to the extinction of the aphid population and no larvae were lost due to cannibalism; however > 80% of the larvae of the other two species were still present when the aphid became extinct and the losses due to cannibalism for H. axyridis and P. japonica were 25% and 14% respectively. Finally, 28% of the P. japonica larvae completed their development, whereas no larvae of the other two species became adult.
3. In mixed-species populations, mortality of P. japonica attributable to cannibalism or intraguild predation increased greatly to 60%, whereas that of the other two species remained about the same. Consequently, survival of H. axyridis larvae improved and survival of P. japonica worsened; however the survival of C. s. brucki larvae was not affected by the other two species. Early emigration by C. s. brucki larvae may have enabled them to escape intraguild predation by H. axyridis in this system.     

Response of coccinellid larvae to conspecific and heterospecific larval tracks: a mechanism that reduces cannibalism and intraguild predation

Cannibalism, where one species feeds on individuals of its own species, and intraguild predation (IGP), where a predator feeds on other predatory species, can both pose significant threats to natural enemies and interfere with their biological control of pests. Behavioral mechanisms to avoid these threats, however, could help maintain superior pest control. Here, we ask whether larvae of Coccinella septempunctata (Coleoptera: Coccinellidae) and Harmonia axyridis (Coleoptera: Coccinellidae) respond to larval tracks deposited by the other and whether this behavioral response reduces the threat of cannibalism and IGP. In petri dish experiments, we show that both H. axyridis and C. septempunctata avoid foraging in areas with conspecific larval tracks. Using a method of preventing larvae from depositing tracks, we then demonstrate that the frequency of cannibalism is greater for both species when larvae are prevented from depositing tracks compared with when the tracks are deposited. For multi-species interactions we show in petri dish experiments that C. septempunctata avoids H. axyridis larval tracks but H. axyridis does not avoid C. septempunctata larval tracks, demonstrating an asymmetry in response to larval tracks that parallels the asymmetry in aggressiveness between these species as intraguild predators. On single plants, we show that the presence of H. axyridis larval tracks reduces the risk of IGP by H. axyridis on C. septempunctata. Our study suggests that larval tracks can be used in more ways than previously described, in this case by changing coccinellid larval behavior in a way that reduces cannibalism and IGP.     

The use of honeydew in foraging for aphids by larvae of the ladybird beetle, Coccinella septempunctata L. (Coleoptera: Coccinellidae)

Abstract.  1. To clarify the use of honeydew in foraging for aphids by larvae of the ladybird beetle, Coccinella septempunctata L., searching behaviour of ladybird larvae for Aphis craccivora Koch and Acyrthosiphon pisum Harris and the abundance of honeydew under aphid colonies were examined in laboratory experiments.
2. More larvae responded by climbing the plants with aphids than responded to plants without aphids. When the plants were replaced with sticks, in order to exclude visual and olfactory cues from plants and aphids, more larvae of C. septempunctata climbed sticks above the area that contained honeydew than climbed sticks above the area that did not contain honeydew. Then, ladybird larvae use honeydew as a contact kairomone when foraging for aphids.
3.  Aphis craccivora deposited a larger number of honeydew droplets beneath the plants than did similar numbers of A. pisum. Thus, C. septempunctata larvae licked more frequently the honeydew of A. craccivora than that of A. pisum and spent longer searching on the area containing honeydew of A. craccivora than that of A. pisum . Consequently, a larger number of larvae climbed a stick above honeydew of A. craccivora than that of A. pisum.
4. It may be also considered that C. septempunctata larvae can distinguish honeydew of the two aphid species and respond more strongly to A. craccivora than A. pisum.