Aphid-mediated coexistence of ladybirds (Coleoptera: Coccinellidae) and the wood ant Formica rufa: seasonal effects, interspecific variability and the evolution of a coccinellid myrmecophile.

It is generally believed that most homopteran-eating insects avoid ant-tended colonies of Homoptera, due to the ant aggression they encounter there. However, because homopteran colonies which are ant-tended often persist for longer than untended colonies, some homopteran-eaters may utilise ant-tended Homoptera when untended colonies are scarce. Furthermore, a few homopteran-eaters are myrmecophilous, habitually coexisting with ants. To investigate these phenomena, a study was made of aphids and aphidophagous coccinellids (ladybirds) on Scots pine, Pinus sylvestris , growing in areas foraged and unforaged by the wood ant Formica rufa . The non-tended aphid Schizolachnus pineti exhibited a marked population decline in late summer but persisted in both areas at very low density. Facultatively tended Cinara aphids exhibited higher population densities when associated with F. rufa , and remaining colonies of these aphids were only found associated with ants in late summer. Coccinellids exhibited considerable interspecific variability in their level of association with F. rufa , and there was some evidence of an increase in certain species' frequencies of occurrence with the ant when Cinara aphids were all ant-tended, in late summer. Coexistence with ants appears to be associated with either an intolerance of low aphid densities, in Coccinella septempunctata and Harmonia quadripunctata , or with extreme dietary specialisation, in Myzia oblongoguttata . Similar factors to those which bring C. septempunctata into contact with ants were probably of importance in the initial stages of the evolution of myrmecophily of its congener, Coccinella magnifica .     

Low parasitoid success on a myrmecophilous host is maintained in the absence of ants

Abstract.  1. Studies of Dinocampus coccinellae , a parasitoid of ladybird beetles, have generally shown congruence between field parasitism rates of different host species and parasitoid preference and/or host suitability in the laboratory, suggesting that host intrinsic factors rather than habitat-related extrinsic factors are of greatest importance in determining D. coccinellae occurrence.
2. The myrmecophilous Coccinella magnifica exhibits much lower D. coccinellae prevalence in the field than most other Coccinella species: it has been suggested that this is a manifestation of enemy-free space provided by the predatory Formica rufa group ants with which the C. magnifica occurs.
3. Coccinella magnifica collected at the same time and locality as parasitised Coccinella septempunctata were unparasitised by D. coccinellae . In the laboratory, in the absence of ants, although the parasitoid attacked C. magnifica as readily as C. septempunctata , C. magnifica was not parasitised successfully.
4. Such results are consistent with those from other ladybirds and C. magnifica does not now benefit directly from any putative D. coccinellae -free space provided by aggressive ants. Because its close relatives exhibit high levels of D. coccinellae parasitism, C. magnifica may be useful in determining some elements important in the evolution of host protection against parasitoid attack.     

Cornicle secretions of Uroleucon nigrotuberculatum (Homoptera: Aphididae) as the last bullet against lady beetle larvae

Aphids have evolved various defense strategies against natural enemies, including secretions from their cornicles. We assessed the defensive function of cornicle secretions by the goldenrod aphid, Uroleucon nigrotuberculatum (Olive), against larvae of the lady beetles Coccinella septempunctata bruckii Mulsant and Propylea japonica (Thunberg) (Coleoptera: Coccinellidae). The aphid secreted red droplets from its cornicles when attacked by the larvae. Two‐thirds of the C. septempunctata bruckii larvae and 46.7% of the P. japonica larvae that preyed on the aphids died before reaching the pre‐pupal stage. The secretions caused molting failure when smeared on the larvae's heads or glued to the larvae's mouthparts, killing 56.7% of C. septempunctata bruckii larvae and 36.7% of P. japonica larvae. Second instar larvae were affected most. About 40% of third and fourth instar larvae of C. septempunctata bruckii vomited soon after ingesting the aphids. In the field, up to 40% of first and second instar larvae were smeared with red secretions. Our results show that these cornicle secretions are an effective and active defense against earlier instars of coccinellid larvae.     

Predator and parasitoid attacking ant-attended aphids: effects of predator presence and attending ant species on emerging parasitoid numbers

Interaction between a predator and a parasitoid attacking ant-attended aphids was examined in a system on photinia plants, consisting of the aphid Aphis spiraecola, the two ants Lasius japonicus and Pristomyrmex pungens, the predatory ladybird beetle Scymnus posticalis, and the parasitoid wasp Lysiphlebus japonicus. The ladybird larvae are densely covered with waxy secretion and are never attacked by attending ants. The parasitoid females are often attacked by ants, but successfully oviposit by avoiding ants. The two ants differ in aggressiveness towards aphid enemies. Impacts of the predator larvae and attending ant species on the number of parasitoid adults emerging from mummies per aphid colony were assessed by manipulating the presence of the predator in introduced aphid colonies attended by either ant. The experiment showed a significant negative impact of the predator on emerging parasitoid numbers. This is due to consumption of healthy aphids by the predator and its predation on parasitized aphids containing the parasitoid larvae (intraguild predation). Additionally, attending ant species significantly affected emerging parasitoid numbers, with more parasitoids in P. pungens-attended colonies. This results from the lower extent of interference with parasitoid oviposition by the less aggressive P. pungens. Furthermore, the predator reduced emerging parasitoid numbers more when P. pungens attended aphids. This may be ascribed to larger numbers of the predator and the resulting higher levels of predation on unparasitized and parasitized aphids in P. pungens-attended colonies. In conclusion, a negative effect of the predator on the parasitoid occurs in ant-attended aphid colonies, and the intensity of the interaction is affected by ant species.     

Differential Interactions Between an Aphid Endohyperparasitoid and Three Honeydew-Collecting Ant Species: A Field Study of Alloxysta brevis (Thomson) (Hymenoptera: Alloxystidae)

The behavioral interactions between the chemically protected aphid hyperparasitoid Alloxysta brevis and three trophobiotic ant species were examined in the field on thistles. The patterns were not essentially influenced by hyperparasitoid sex. Ants differed in their guarding behavior of aphids and their response toward A. brevis. Lasius niger attacked the hyperparasitoid more readily than Myrmica laevinodis, while aggression by Formica rufa was intermediate. Apart from applying chemical defense, A. brevis responded to ants by flying away (mainly at L. niger) or with avoidance behavior (mainly at M. laevinodis). Additionally, females might switch their tactics from flight to defense with increasing age. Females left the plant more often after encounters with L. niger or F. rufa than with M. laevinodis. Disturbance by any ant species affected the foraging activities, reducing oviposition success to nearly zero.     

Interactions between ants attendingAphis fabae ssp.cirsiiacanthoidis on thistles and foraging parasitoid wasps

We describe the behavioral interactions between honeydew-collecting workers of the ants Lasius nigerand Myrmica ruginodisand females of three species of aphidiid wasps (Lysiphlebus cardui, Lysiphlebus testaceipes, Trioxys angelicae)foraging for their aphid host, Aphis fabaessp. cirsiiacanthoidis,on thistles. Using field and laboratory experiments, we show that the ant-parasitoid interactions are species specific. Workers of both ant species generally attacked and killed females of T. angelicae,but they ignored those of L. cardui.This pattern was not altered when we anesthetized the wasps slightly with carbon dioxide to reduce their mobility. Prior contacts between L. carduiand either conspecific L. nigerfrom a different nest or workers of a different ant species (M. ruginodis)did not influence L. niger'snonaggressive behavior. The number of aphids parasitized by L. testaceipeswas significantly reduced in aphid colonies attended by L. niger,although this parasitoid was rarely attacked by ants. In encounters between these species of ants and wasps, ant aggression is consistent with differences in wasp behavior. We suggest that, in addition, chemical cues located in the cuticula may enable L. carduito avoid detection by honeydew-collecting ants.     

Survival, development and life tables of two congeneric ladybirds in aphidophagous guilds

Two congeneric aphidophagous ladybirds, Coccinella septempunctata and Coccinella transversalis, were reared on three aphid species, Lipaphis erysimi, Myzus persicae and Aphis nerii, to estimate the effect of prey quality and intra- and interspecific interactions on their survival and development of life stages. Mortality of first instar ladybirds of both species was highest feeding on A. nerii. Preimaginal mortafity was lowest when feeding on L. erysimi （C. septempunctata, 1.6% and C. transversalis, 3.2%）, and highest when feeding on A. nerii （ C. septempunctata, 6.2% and C. transversalis, 8.2%）. Comparatively higher weight and larger size of C. septempunctata along with the lower levels of mortality recorded suggested that it is more likely to have acted as an intraguild predator than C. transversalis. High recorded mortality of C. transversalis is attributed to probable intraguild predation on account of its smaller size. The major sources of mortality were probably cannibalism, intraguild predation and other unknown factors. Lower prey quality increased the incidence of cannibalism and intraguild predation, especially in C. transversalis. The investigation suggests an intrinsic competitive advantage for C. septempunctata over C. transversalis in guilds of three aphid species.     

Ovarian dynamics and oosorption in two species of predatory lady beetles (Coleoptera: Coccinellidae)

Abstract Ovarian development and oviposition dynamics of two species of lady beetle, Coccinella septempunctata L. and C. transversoguttata richardsoni Brown, are examined in laboratory experiments in which pea aphids (Acyrthosiphon pisum Harris) are provided ad libitum and then removed. Both species respond to prey removal by stabilizing at lower body weights, and by laying progressively fewer and smaller eggs of reduced viability, until oviposition ceases altogether after several days of starvation. Dissections of females after prey removal reveal similar patterns of oosorption in both species. However, C. septempunctata reduces oviposition more rapidly after prey removal than does C. transversoguttata. When prey are again provided, C. septempunctata soon lay as many eggs as previously but C. transversoguttata lay fewer. Females, especially of C. septempunctata, that stop producing and resorb eggs in the absence of prey lay more eggs subsequently than do females that feed continually on prey provided ad libitum and lay eggs throughout the experiment. Thus, although both species are responsive to a rapid change in prey availability, C. septempunctata appears to be especially responsive. Rapid responses to changes in prey availability may contribute to the greater abundance and reproductive success of this introduced species relative to the native C. transversoguttata in western North American alfalfa fields that exhibit widely varying pea aphid densities. However, both species engage in oosorption as a means of reserving resources under poor prey conditions and enhancing future reproductive effort when prey conditions improve.     

Small-scale disturbances spread along trophic chains: leaf-cutting ant nests, plants, aphids, and tending ants

Small-scale disturbances caused by animals often modify soil resource availability and may also affect plant attributes. Changes in the phenotype of plants growing on disturbed, nutrient-enriched microsites may influence the distribution and abundance of associated insects. We evaluated how the high nutrient availability generated by leaf-cutting ant nests in a Patagonian desert steppe may spread along the trophic chain, affecting the phenotype of two thistle species, the abundance of a specialist aphid and the composition of the associated assemblage of tending ants. Plants of the thistle species Carduus nutans and Onopordum acanthium growing in piles of waste material generated by leaf-cutting ant nests (i.e., refuse dumps) had more leaves, inflorescences and higher foliar nitrogen content than those in non-nest soils. Overall, plants in refuse dumps showed higher abundance of aphids than plants in non-nest soils, and aphid colonies were of greater size on O. acanthium plants than on C. nutans plants. However, only C. nutans plants showed an increase in aphid abundance when growing on refuse dumps. This resulted in a similar aphid load in both thistle species when growing on refuse dumps. Accordingly, only C. nutans showed an increase in the number of ant species attending aphids when growing on refuse dumps. The increase of soil fertility generated by leaf-cutting ant nests can affect aphid abundance and their tending ant assemblage through its effect on plant size and quality. However, the propagation of small-scale soil disturbances through the trophic chain may depend on the identity of the species involved.     

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.     

七星瓢虫成虫觅食行为的观察

本文研究了七星瓢虫成虫捕食麦长管蚜、洋槐蚜和绣线菊蚜的行为 ,发现其觅食行为包括 7个明显动作 ,即搜寻、捕捉、嚼食、梳理、静止、展翅和排泄。     

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     

Reaction of Ants to, and Feeding Biology of, a Congeneric Myrmecophilous and Non-myrmecophilous Ladybird

Coccinella magnifica Redtenbacher lives only in close contact with species of the Formica rufa group. Laboratory experiments were set up to determine how this species may be adapted to living with ants by comparing its behaviour with that of the closely related Coccinella septempunctata L. Eggs and larvae of C. magnifica placed on the foraging trails of ants were bitten significantly less often by the ants than those of C. septempunctata. However, the ants responded similarly to the adults of both species. For these two species, the presence of ants resulted in a significant decrease in predation efficiency. However, C. magnifica was more efficient at catching aphids in the presence of ants than C. septempunctata. The behaviour of this myrmecophilous species is discussed by taking into account that it is a generalist in terms of prey specificity.     

Reproductive performance of four aphidophagous ladybirds on cowpea aphid, Aphis craccivora Koch

Abstract:  This study investigated prey consumption, egg production, percent progeny loss, reproductive, pre- and post-reproductive periods, reproductive time ratio, reproductive rate and bioconversion efficiency of four aphidophagous ladybirds, viz. Cheilomenes sexmaculata (Fabricius), Coccinella septempunctata Linnaeus, Coccinella transversalis Fabricius and Propylea dissecta (Mulsant) on Dolichos lablab Linnaeus infested with cowpea aphid, Aphis craccivora Koch. C. sexmaculata had the highest bioconversion efficiency, reproductive rate and reproductive time ratio followed in rank order by P. dissecta , C. transversalis and C. septempunctata . This study indicates that C. sexmaculata has a narrow ecological relationship with A. craccivora . The increased allocation of resources to reproduction as indicated through a high reproductive time ratio and high bioconversion efficiency of C. sexmaculata and P. dissecta suggest that they may be better adapted to compete for this prey with larger species like C. transversalis and C. septempunctata .     

Interference and competitive behaviour of the aphid predators,Chrysoperla carnea andCoccinella septempunctata in the laboratory

Interference and competition betweenChrysoperla carnea (Stephens) andCoccinella septempunctata L. was investigated in the absence and presence of aphid prey. When larvae of similar vigour encountered each other,C. carnea larvae were superior toC. septempunctata. Otherwise the larger of 2 individuals always killed the smaller. In the absence of preyC. carnea adults were attacked by their own 2nd and 3rd instar larvae as well as by 3rd instar larvae ofC. septempunctata. In all encounters the adults ofC. septempunctata were superior. Since the eggs ofC. carnea are protected to some extent by being on egg stalks, they were less susceptible to cannibalism and predation thanC. septempunctata eggs which are deposited in batches directly on plant leaves. In the presence of prey cannibalism and predation were reduced, especially between larvae. Only eggs and 1st instar larvae were endangered. In the present experimentsC. carnea showed a slight superiority overc. septempunctata. Paper presented at the 17th International Congress of Entomology held in August 20–26 1984 in Hamburg, F.R. Germany.     

<Emphasis Type="Italic">Aphidius ervi</Emphasis> Preferentially Attacks the Green Morph of the Pea Aphid, <Emphasis Type="Italic">Acyrthosiphon pisum</Emphasis>

The pea aphid, Acyrthosiphon pisum Harris (Hemiptera: Aphididae) is found in red and green color morphs. Previous work has suggested that the aphidiine parasitoid Aphidius ervi Haliday preferentially attacks green pea aphids in the field. It is not clear whether these results reflect a real preference, or some unknown clonal difference, such as in immunity, between the aphids used in the previous studies. We used three susceptibility-matched pairs of red and green morph pea aphid clones to test for preferences. In a no-choice situation, the parasitoids attacked equal proportions of each color morph. When provided with a choice, A. ervi was significantly more likely to oviposit into colonies formed from green morphs when the neighboring colony was formed from red morph aphids. In contrast, red morphs were less likely to be attacked when their neighboring colony was of the green morph. By preferentially attacking green colonies, A. ervi may reduce the likelihood of intraguild predation, as it is suggested that visually foraging predators preferentially attack red aphid colonies. Furthermore, if this host choice behavior is replicated in the field, we speculate that color morphs of the pea aphid may interact indirectly through their shared natural enemies, leading to intraspecific apparent competition.     

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.     

Are ant-aphid associations a tritrophic interaction? Oleander aphids and Argentine ants

Summary Oleander aphids, (Aphis nerii), which are sporadically tended by ants, were used as a moded system to examine whether host plant factors associated with feeding site influenced the formation of ant-aphid associations. Seasonal patterns of host plant utilization and association with attendant ants were examined through bi-weekly censuses of the aphid population feeding on thirty ornamental oleander plands (Nerium oleander) in northern California in 1985 and 1986. Colonies occurred on both developing and senescing plant terminals, including leaf tips, floral structures, and pods. Aphids preferentially colonized leaf terminals early in the season, but showed no preference for feeding site during later periods. Argentine ants (Iridomyrmex humilis) occasionally tended aphid colonies. Colonies on floral tips were three to four times more likely to attract ants than colonies on leaf tips, even though the latter frequently contained more aphids. Ants showed a positive recruitment response to colonies on floral tips, with a significant correlation between colony size and number of ants. There was no recruitment response to colonies on leaf tips. These patterns were reproducible over two years despite large fluctuations in both aphid population density and ant activity. In a laboratory bioassay of aphid palatability, the generalist predator,Hippodamia convergens, took significantly more aphids reared on floral tips compared to those reared on leaf tips. The patterns reported here support the hypothesis that tritrophic factors may be important in modifying higher level arthropod mutualisms.     

Chill out: cooling promotes aggressive behavior in the ant Formica xerophila

Studies of insect behavior often involve cooling individuals prior to performing experiments or making observations. For such studies, it is important to know how cooling might affect subsequent behavior. Here I investigate how anesthetization by cooling (relative to anesthetization by carbon dioxide or control individuals) affects the aggressive behaviors of two closely related ant species, Formica xerophila and F. integroides. These species regularly compete for resources, and individuals of both species regularly experience nighttime temperatures similar to those of cold-induced anesthetization. I show that cooling increases aggression (toward both interspecific competitors as well as nestmates) for F. xerophila, but has no effect on F. integroides behavior. Although previously cooled F. xerophila are more aggressive during both intraspecific and interspecific interactions, intraspecific fights are much shorter in length than interspecific fights. Furthermore, aggression by F. xerophila decreases as time since being cooled increases. These data suggest that cooling produces a short-term reduction in the ants’ discriminatory abilities, which leads to mistaken identities during encounters. The difference in species’ behaviors after cooling can be attributed to their differences in strategies when encountering potential competitors. Results here confirm that cold anesthesia can affect subsequent behavior, and needs to be tested in behavioral studies with insects. Received 6 September 2008; revised 29 October 2008; accepted 4 November 2008.