Does insect mother know under what conditions it will make their offspring live?

According to the optimal oviposition theory, the larval success of insects depends on the oviposition site selection by females. Females are expected to choose a site with many resources and few competitors or predators to allow the best performance for their progeny, assuming that “mother knows best.” However, this is not systematically observed. The Aphidoletes aphidimyza larvae are generalist aphid predators and females consequently lay their eggs near or inside aphid colonies. The goal of this study was to investigate the impact of intraspecific competition on oviposition behavior of A. aphidimyza females. First, we counted the number of eggs laid by a female on a leaf with 20 aphids, in the presence of 0, 2, 4, or 6 conspecific eggs or in the absence of eggs but in presence of 3 virgin females. The same experiment was also performed under choice condition with 2 oviposition sites. Our results show that the presence of low densities of conspecific eggs, or the presence of conspecific females, have no significant impact on the number of eggs laid by A. aphidimyza females. One of the hypotheses advanced to explain these results is the advantages of conspecifics presence. At low densities, the presence of eggs on an oviposition site can indicate the suitability of the site for the females. The conspecific presence can also insure a dilution effect against predator and increase the presence of potential mating partners for this monogenic species.     

Prey Abundance, Intraguild Predators, Ants and the Optimal Egg-laying Strategy of a Furtive Predator

Larval performance can have a great influence on female oviposition choice, especially in insects where the newly hatched offspring are unable to move any great distance to find an appropriate food source. For furtive predators, like the predatory midge Aphidoletes aphidimyza which preys on aphids while simultaneously residing and remaining undetected within their colonies, oviposition behaviour is crucial because these slow moving offspring are restrained to their natal colony. Here we develop a new model for predicting the optimum number of eggs that a furtive predator should lay in an aphid colony, based on: (1) the number of available prey (aphids); (2) the protection from predation conferred by “hiding” in the colony and (3) the effects of interspecific and intraspecific competition. We also explore the effect of aphid attendance by ants on oviposition behavior. We compare model predictions with empirical field observations of the clutch sizes of A. aphidimyza in apple orchards. The simplest of the four models best fits the observed data and provides the first field evidence that a furtive predator adjusts its clutch size as a function of prey density. The slope of the relationship between clutch size and aphid number is quite close to that predicted by our models suggesting that intra-clutch competition is the main factor governing furtive aphid midge oviposition choice.     

Divergent preferences of Rhagoletis pomonella host races for olfactory and visual fruit cues

The quality of different species of aphids as food for aphidiphagous ladybird beetles varies greatly. The optimal oviposition theory predicts that a female should lay eggs preferentially in patches of suitable prey and should be reluctant to oviposit in patches of less suitable prey. A no‐choice experiment was used to test whether aphids (Homoptera: Aphididae) of different suitability influence the oviposition behaviour of the two‐spot ladybird beetle, Adalia bipunctata (L.) (Coleoptera: Coccinellidae). The results indicate that A. bipunctata females are not more reluctant to lay eggs in the presence of moderately suitable compared to highly suitable aphids. However, females laid fewer eggs in the presence of toxic aphids.     

Egg cannibalism by ladybird larvae is less frequent than expected from the nutritional benefit accrued to cannibals

Egg cannibalism is a widespread phenomenon in predatory arthropods. However, conflicting results have been reported regarding the nutritional value of conspecific eggs. Therefore, evaluation of the value of a mixed diet of conspecific eggs and aphids for survival and growth of Adalia bipunctata (Coccinellidae) larvae was tested. Subsequently, the propensity for cannibalism of naive and experienced larvae was assessed in two experiments in which the relative density and quality of conspecific eggs were manipulated in an experimental arena. It was found that larvae that were fed a mixed diet of conspecific eggs and aphids moulted into larger adults than those fed either aphids or eggs, and those that fed on conspecific eggs lost less mass than those fed only aphids during pupal stage. Additionally, in an experimental arena, attacks on aphids were more frequent than expected when conspecific eggs occupied 50% and 75% of the patches. When 50% of patches were occupied by conspecific eggs, the preference for aphids was less marked when larvae had previously experienced cannibalism (76% vs. 52% respectively) or when offered in the arena conspecific egg the cuticular hydrocarbons of which had been removed (76% vs. 48%, respectively). However, cannibalism was not enhanced if larvae experienced heterospecific prey shortages, but were supplemented with an artificial diet. Given that prey choice in A. bipunctata larvae is driven by chemical cues and that hydrocarbons on the egg surfaces and in larval tracks are very similar, we hypothesize that the naive larvae avoid eggs because of the uncertainty that those hydrocarbons indicate either eggs or conspecific larvae.     

Oviposition site selection of Episyrphus balteatus

The oviposition behaviour of Episyrphus balteatus DeGeer (Diptera: Syrphidae) was investigated in four-choice experiments in screen cages and in experiments with direct behavioural observations. Females laid hardly any eggs in the absence of aphids and preferred larger aphid colonies to small ones. Honeydew attracted the females via olfaction and elicited oviposition. Females were able to perceive the presence of conspecific eggs and oviposited less often in aphid colonies in which eggs were present. The oviposition deterring stimulus was also active when the eggs were removed, hence, the deterrent did not act visually, but probably olfactorily.     

Responses of Episyrphus balteatus DeGeer (Diptera: Syrphidae) in relation to prey density and predator size

Laboratory experiments were conducted to determine the functional and numerical responses of the aphidophagous hover fly Episyrphus balteatus DeGeer (Diptera: Syrphidae) to different densities of 4th instar black bean aphids, Aphis fabae Scopoli (Homoptera: Aphididae), on broad bean, Vicia faba L. (Fabaceae). Two different-sized larvae of predators were tested in different densities of similar-sized prey to determine whether functional response parameters depended on the body sizes of predator and prey. In numerical response experiments, gravid E. balteatus females were exposed individually to different densities of 4th instars of A. fabae on cut sections of the broad bean plant, V. faba L. Logistic regression suggested a type II functional response for both larval sizes of E. balteatus. The searching efficiency (a) of the larger larvae was higher than that of the smaller ones. Prey consumption was higher, and handling time (T_h) was lower for larger larvae than smaller ones. The theoretical maximum number of A. fabae nymphs eaten by the different-sized larvae was 125 and 269 nymphs per day. Larger E. balteatus larvae are more efficient predators for aphid management strategies. The reproductive numerical response, in terms of the number of eggs laid, increased curvilinearly with increasing prey density, but the proportion of eggs laid (egg number/prey density) decreased as the initial density of prey increased.     

Oviposition responses to patch quality in the larch ladybird Aphidecta obliterata (Coleoptera: Coccinellidae): effects of aphid density, and con- and heterospecific tracks

The effects and persistence of oviposition-deterring semiochemical cues from conspecific and heterospecific larval tracks on the oviposition rate of Aphidecta obliterata (Linnaeus) females were investigated. In addition, the effects of varying aphid prey density were considered and also whether any resulting response originated from differential nutritional status of females and/or due to aphid odour stimuli. The existence of oviposition responses to conspecific egg chemicals was also considered. Gravid A. obliterata females were deterred from oviposition by conspecific larval tracks and the effect was density dependent. Females actively avoided searching in these contaminated areas. Tracks induced a significant effect on oviposition for up to three days. Heterospecific tracks of the coccinellid Adalia bipunctata (Fabricius) or the chrysopid Chrysoperla carnea (Stephens) did not induce any oviposition response in A. obliterata females. Increasing aphid density induced increased oviposition rate in A. obliterata females. Nutritional status of females was an important factor in the relationship between aphid density and oviposition rate, but aphid associated cues (odours) were not. There was an inhibitory effect of extracts of conspecific egg-surface chemicals on oviposition by A. obliterata females. In the field, cannibalism, competition and limited food availability represent the major threats to egg and larval survival. Patch quality assessment mechanisms enable females to lay eggs at sites where offspring survival is maximized. Oviposition-deterring semiochemicals tend to promote more even distribution of predators over prey patches.     

The oviposition behavior ofAphidius ervi andMonoctonus paulensis (Hymenoptera: Aphididae) encountering different host species (Homoptera: Aphididae) in sequential patches

Two-day-old mated females ofAphidius ervi Haliday andMonoctonus paulensis (Ashmead) were each provided with two sequential host patches. Patches were comprised of plastic petri dishes containing either 15 pea aphids,Acyrthosiphum pisum (Harris), or 15 alfalfa aphids,Macrosiphum creelii Davis. Both wasp species parasitized more hosts in patches containing pea aphids than in those containing alfalfa aphids, regardless of sequence. Females ofA. ervi also laid more eggs per aphid in patches containing pea aphids than in patches containing alfalfa aphids. When both patches contained alfalfa aphids,M. paulensis females parsitized more aphids in the second patch than in the first. Fewer alfalfa aphids were parasitized in the second patch when the first patch contained pea aphids, and fewer eggs were laid per alfalfa aphid. Parasitoid females of both species exhibited consistently higher rates of oviposition into their preferred host species and adjusted their reproductive allocation to hosts and host patches as a function of their experience in previous patches.     

Avoidance responses of an aphidophagous ladybird, Adalia bipunctata, to aphid-tending ants

Abstract.  1. Insect predators often aggregrate to patches of high prey density and use prey chemicals as cues for oviposition. If prey have mutualistic guardians such as ants, however, then these patches may be less suitable for predators.
2. Ants often tend aphids and defend them against predators such as ladybirds. Here, we show that ants can reduce ladybird performance by destroying eggs and physically attacking larvae and adults.
3. Unless ladybirds are able to defend against ant attacks they are likely to have adaptations to avoid ants. We show that Adalia bipunctata ladybirds not only move away from patches with Lasius niger ants, but also avoid laying eggs in these patches. Furthermore, ladybirds not only respond to ant presence, but also detect ant semiochemicals and alter oviposition strategy accordingly.
4. Ant semiochemicals may signal the extent of ant territories allowing aphid predators to effectively navigate a mosaic landscape of sub-optimal patches in search of less well-defended prey. Such avoidance probably benefits both ants and ladybirds, and the semiochemicals could be regarded as a means of cooperative communication between enemies.
5. Overall, ladybirds respond to a wide range of positive and negative oviposition cues that may trade-off with each other and internal motivation to determine the overall oviposition strategy.     

Discrimination of parasitized aphids by a hoverfly predator: effects on larval performance, foraging, and oviposition behavior

The choice of oviposition site by female aphidophagous predators is crucial for offspring performance, especially in hoverflies whose newly hatched larvae are unable to move over large distance. Predator and parasitoid interactions within the aphidophagous guild are likely to be very important in influencing the choices made by predatory hoverfly females. In the present study, the foraging and oviposition behavior of the aphidophagous hoverfly Episyrphus balteatus DeGeer (Diptera: Syrphidae) was investigated with respect to the parasitized state of its aphid prey, Acyrthosiphon pisum Harris (Homoptera: Aphididae), that were parasitized by Aphidius ervi Haliday (Hymenoptera: Aphidiidae). We also recorded the number of eggs laid by hoverfly females when subjected to parasitized aphids. Furthermore, we studied the influence of being fed with parasitized aphids on hoverfly larval performance. Hoverfly females did not exhibit any preference for plants infested with unparasitized or aphids parasitized for 7 days. On the other hand, plants infested with mummies or exuvia were less attractive for E. balteatus . These results were correlated with (i) the number of eggs laid by E. balteatus females and (ii) larval performance. Thus, our results demonstrate that E. balteatus behavior is affected by parasitoid presence through their exploitation of aphid colonies. Indeed, hoverfly predators select their prey according to the developmental state of the parasitoid larvae.     

Attack strategy of ladybird beetles (Coccinellidae): factors shaping their numerical response

Summary Temporal changes in aphid abundance pose a considerable challenge to ovipositing aphidophagous ladybirds, as in order to maximize their fitness they need to synchronize their reproduction with the early development of aphid populations. Field census data and laboratory experiments were used to determine how ovipositing females of the two-spot ladybird, Adalia bipunctata (L.), assess whether an aphid population is suitable for exploitation. In the field, two-spot ladybirds usually laid eggs well before aphid populations peaked in abundance. In the laboratory they showed a marked reduction in their reproductive numerical response in the presence of larvae of their own species but not of other aphidophagous ladybirds. At the highest aphid density this was not a consequence of competition for food between larvae and ovipositing females. In the presence of conspecific larvae gravid females were very active and as a consequence more likely to leave an area, and when confined with other conspecific females or larvae laid fewer eggs and later than females kept on their own. The extent of the inhibition of egg laying is negatively correlated with the rate of encounter with larvae. Thus it is proposed that gravid females appear mainly to use the presence of conspecific larvae to assess the potential of an aphid colony for supporting the development of their offspring.     

The effect of rearing the ladybirdHarmonia axyridis onEphestia kuehniella eggs on the response of its larvae to aphid tracks

Larvae ofHarmonia axyridis Pallas (Col., Coccinellidae) exhibited two walking patterns during prey search. Extensive search occurred when searching for prey patches and was characterized by long linear paths and a fast speed. Intesive search, which appeared after the ingestion of a prey in a patch, resulted from a lowering of the linear speed and an increase in the number of stops and angular speed. When larvae reared on the aphidAcyrthosiphum pisum Harris (Hom., Aphidae) crossed an artificial substratum previously contaminated by this prey, they changed their path direction and adopted intensive search. They probably perceived aphid odor tracks and consequently modified their walking pattern. This gustatory capacity probably allowed very mobile larvae to locate prey patches more rapidly and improve encounter with preys in every patch.H. axyridis larvae reared on a substitute prey, the eggs ofEphestia kuehniella Zeller (Lep., Pyralidae), for more than a hundred generations, also changed their path orientation but retained extensive search. The weak response of these larvae to aphid tracks may have resulted from either a decrease in their sensitivity to gustatory aphid stimuli or their difficulty in associating aphid odor with aphid presence. These larvae needed more time and more preliminary encounters than larvae reared on aphids before catching prey.     

Olfactory response by the aphidophagous gall midge, Aphidoletes aphidimyza to honeydew from green peach aphid, Myzus persicae

Female adults of the aphidopagous gall midge, Aphidoletes aphidimyza (Rondani) (Diptera: Cecidomyiidae), showed an olfactory response to honeydew excreted by the green peach aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae) under laboratory conditions. The response was only elicited by treatments with honeydew, whereas aphids, aphids with pepper plants or leaves, and pepper plants or leaves were not attractive to the midges. Dose‐dependent responses were observed from whole honeydew, honeydew volatiles extracted in pentane, and honeydew volatiles captured on Porapak Q®. When honeydew was eluted with three sequential pentane washes, a positive response was only observed from the midges for the first wash. Female midges laid more eggs on pepper plants infested with higher densities of M. persicae. The olfactory response of midges to honeydew is discussed with respect to prey location.     

Prey finding by larvae and adult females of shape Episyrphus balteatus

The prey-location behaviour of larvae of Episyrphus balteatus DeG. (Dipt.: Syrphidae) was investigated in two different experimental set-ups. First instar larvae exhibited directed search over short distances, guided by olfactory cues from aphids, but not from honeydew. However, second and third instars did not respond to aphid-plant-complex odours in a 4-arm-olfactometer. Aphid extracts, honeydew and sucrose were found to be feeding stimulants for the larvae. The oviposition behaviour of female syrphids was investigated in a series of two-choice experiments: females were able to evaluate aphid numbers and adjust oviposition rates accordingly, with higher prey numbers eliciting increased oviposition, even when the aphids were removed at the start of the experiment. The presence of conspecific syrphid larvae did not inhibit oviposition when the females were deprived of suitable oviposition sides before the experiments were conducted.     

Cannibalism and interspecific predation in two predatory ladybirds in relation to prey abundance in the field

Life tables for two predatory ladybirds,Coccinella septempunctata andHarmonia axyridis, were constructed in two years in which prey abundance differed. The prey aphid,Aphis gossypii, was abundant on its primary host from late May to late June. Females ofH. axyridis andC. septempumctata laid their eggs during the increase and peak in aphid abundance. The oviposition period ofC. septempunctata started before and was shorter than that ofH. axyridis. In both species, intraguild predation and/or cannibalism of the egg and fourth instar stages, but rarely of other developmental stages, were observed. Fourth instar larvae ofH. axyridis had to complete their development when aphids were scarce more frequently than those ofC. septempunctata. The highest frequency of intra- and interspecific predation was of fourth instarH. axyridis larvae. In terms of intraguild predation, the larvae ofH. axyridis preyed on larvae ofC. septempunctata, but the reverse was not observed. Percentage survival from egg to adult inH. axyridis was higher than inC. septempunctata in both years, and least in both species in the year of low aphid abundance. These results suggest that prey abundance influenced the frequency of cannibalism and intraguild predation, which were important in structuring this guild of ladybirds.     

Intraguild Predation among the Hoverfly Episyrphus balteatus de Geer (Diptera: Syrphidae) and Other Aphidophagous Predators

Aphidophagous predators compete for the same prey species. During their foraging activity they frequently encounter heterospecific aphid predators. These situations can lead to intraguild predation and may disrupt biological control efforts against aphids where more than one predator species is present. We investigated the behavior of larvae of the hoverfly Episyrphus balteatus de Geer and its interaction with three other aphid predators: the ladybird Coccinella septempunctata L., the lacewing Chrysoperla carnea Stephens, and the gall midge Aphidoletes aphidimyza (Rondani). Interspecific interactions between predators were examined in arenas of different sizes and in the presence of extraguild prey. The outcome of interactions between E. balteatus larvae and the other predators depended predominantly on the relative body size of the competitors. Relatively large individuals acted as intraguild predators, while relatively smaller individuals became intraguild prey. Eggs and first- as well as second-instar larvae of E. balteatus were highly susceptible to predation by all other predators, whereas pupae of E. balteatus were preyed upon only by the larvae of C. carnea. Interactions between A. aphidimyza and E. balteatus were asymmetric and always favored the latter. Eggs and first- as well as second-instar larvae of E. balteatus sustained intraguild predation irrespective of the size of the arena or the presence of extraguild prey. However, the frequency of predation on third-instar larvae of E. balteatus was significantly reduced. This study indicated that the same species can be both intraguild predator and intraguild prey. It is suggested that combinations of predators must be carefully chosen for success in biological control of aphids.     

Functional response and reproductive attributes of the aphidophagous ladybird beetle,Harmonia dimidiata (Fabricius) in oak trees of sericultural importance

Harmonia dimidiata (Fabricius) (Coleoptera: Coccinellidae) is the dominant predator of the aphid species Cervaphis quercus Takahashi. This aphid is a serious pest of oak trees in several parts of north-east India. Young leaves of oak trees are used in sericulture by rural people and by industry in several parts of north-east India. The effect of different aphid densities on food consumption and fecundity of H. dimidiata was studied in the laboratory. Female beetles were maintained from the time of eclosion till death at a fixed density of 25, 50, 75,100 or 125 aphids. Both the functional response and the reproductive numerical response showed the upper asymptote at 100 adult aphids/female. At this density, females matured earlier and produced more eggs over a longer reproductive period. At lower prey densities, females matured late and they either did not produce eggs or produced fewer eggs. At the higher prey densities, females did not produce more eggs than the asymptote. Results suggested that H. dimidiata are an effective predator of C. quercus aphids on oak trees and could be exploited as a biological control agent in the rising phase of aphid population growth.     

Effects of conspecific and heterospecific competitors on feeding and oviposition of a predatory ladybird: a laboratory study

Abstract There are several examples of intraguild interactions among insect predators of aphids, but little is known regarding the effects of interactions on feeding and oviposition of individual competitors in a guild. In the laboratory, we determined the feeding and oviposition responses of a ladybird predator to its conspecific and heterospecific competitors in an aphidophagous guild. Gravid females of Menochilus sexmaculatus (Fabricius) (Coleoptera, Coccinellidae) reduced oviposition, but not feeding, when exposed to immobilised conspecific or Coccinella transversalis (Fabricius) (Coleoptera, Coccinellidae) individuals in the short‐term (3 h) and long‐term (24 h). Feeding and oviposition responses were not affected when M. sexmaculatus females were exposed to larvae or adults of Scymnus pyrocheilus Mulsant (Coleoptera, Coccinellidae) beetles or larvae of the syrphid fly Ischiodon scutellaris (Fabricius) (Diptera: Syrphidae). The ratio of eggs laid to numbers of aphids consumed by M. sexmaculatus females was also affected by the presence of conspecific or C. transversalis larvae. The results suggest that fecundity of this predator may be affected by both conspecific and heterospecific competitors in a patchy resource.     

Hyperpredation by generalist predatory mites disrupts biological control of aphids by the aphidophagous gall midge Aphidoletes aphidimyza

Biological control of different species of pest with various species of generalist predators can potentially disrupt the control of pests through predator-predator interactions. We evaluate the impact of three species of generalist predatory mites on the biological control of green peach aphids, Myzus persicae (Sulzer) with the aphidophagous gall midge Aphidoletes aphidimyza (Rondani). The predatory mites tested were Neoseiulus cucumeris (Oudemans), Iphiseius degenerans (Berlese) and Amblyseius swirskii Athias–Henriot, which are all commonly used for pest control in greenhouse sweet pepper. All three species of predatory mites were found to feed on eggs of A. aphidimyza, even in the presence of abundant sweet pepper pollen, an alternative food source for the predatory mites. In a greenhouse experiment on sweet pepper, all three predators significantly reduced population densities of A. aphidimyza, but aphid densities only increased significantly in the presence of A. swirskii when compared to the treatment with A. aphidimyza only. This stronger effect of A. swirskii can be explained by the higher population densities that this predator reached on sweet pepper plants compared to the other two predator species. An additional experiment showed that female predatory midges do not avoid oviposition sites with the predator A. swirskii. On the contrary, they even deposited more eggs on plants with predatory mites than on plants without. Hence, this study shows that disruption of aphid control by predatory mites is a realistic scenario in sweet pepper, and needs to be considered when optimizing biological control strategies.     

Imperfect oviposition decisions by the pitcher plant mosquito (Wyeomyia smithii)

Summary Wyeomyia smithii mosquitoes distribute their eggs across available oviposition sites (water-holding pitcher plant leaves) of varying quality. I experimentally examined responses to three components of site quality: conspecific larval density, larval density of the pitcher plant midge,Metriocnemus knabi, and pitcher size. Responses to larval treatments were complex and apparently suboptimal. Although mosquito larval performance is better in leaves with fewer conspecific and more midge larvae, females did not lay more eggs in such pitchers. Instead, more eggs were laid in experimental pitchers containing either midge or mosquito larvae, but fewer eggs in pitchers with neither or both. More eggs were laid in larger pitchers, which tend to accumulate more resources and dry out less often. Therefore, although the oviposition decisions made were suboptimal, they were better than random.