Use of odours by Cycloneda sanguinea to assess patch quality

Adult ladybirds are likely to encounter various species of prey when foraging for oviposition sites. Optimal oviposition theory predicts that females should lay eggs in those sites that are the most suitable for offspring development. Therefore, factors that directly affect offspring mortality, such as the presence of predators and food, are expected to play an important role in the assessment of patch profitability by ladybird predators. Using a Y‐tube olfactometer, we tested whether the predatory ladybird Cycloneda sanguinea L. (Coleoptera: Coccinellidae) can use volatile cues to assess patch profitability and avoid predator‐rich patches. We assessed the foraging behaviour of C. sanguinea in response to odours associated with tomato plants infested with a superior prey, Macrosiphum euphorbiae Thomas (Homoptera: Aphididae), and with an inferior prey, Tetranychus evansi Baker and Pritchard (Acari: Tetranychidae), in the presence or absence of the heterospecific predator Eriopis connexa Mulsant (Coleoptera: Coccinellidae). Females of C. sanguinea significantly preferred plants infested by M. euphorbiae to plants infested by T. evansi and avoided odours emanating from plants on which E. connexa females were present. Our results show that C. sanguinea use volatile cues to assess patch profitability and to avoid patches with heterospecific competitors or intraguild predators.     

Age and experience influence patch assessment for oviposition by an insect predator

Abstract.  1. Dynamic models of optimal foraging predict that an animal's decision to accept or reject a patch depends not only on the environment and patch quality, but also on its internal state. Previous experiments have shown that the two-spot ladybird beetle, Adalia bipunctata (L.), is reluctant to lay eggs in a patch of prey contaminated by the oviposition-deterring pheromone produced by conspecific larvae.
2. An experiment was conducted to test whether the internal state of an A. bipunctata female affects its oviposition response to oviposition-deterring pheromone. Firstly, the oviposition response to oviposition-deterring pheromone of young and old females was compared. Secondly, the oviposition response to oviposition-deterring pheromone of females previously exposed continuously to oviposition-deterring pheromone was compared with that of females of the same age but with no previous experience of oviposition-deterring pheromone.
3. Old females and females with previous experience of oviposition-deterring pheromone were less reluctant to lay eggs in the presence of oviposition-deterring pheromone than young and naive females. These results are consistent with the predictions of optimal foraging theory.     

Within‐patch oviposition site shifts by spider mites in response to prior predation risks decrease predator patch exploitation

In egg‐laying animals with no post‐oviposition parental care, between‐ or within‐patch oviposition site selection can determine offspring survival. However, despite the accumulation of evidence supporting the substantial impact predators have on oviposition site selection, few studies have examined whether oviposition site shift within patches (“micro‐oviposition shift”) reduces predation risk to offspring. The benefits of prey micro‐oviposition shift are underestimated in environments where predators cannot disperse from prey patches. In this study, we examined micro‐oviposition shift by the herbivorous mite Tetranychus kanzawai in response to the predatory mite, Neoseiulus womersleyi, by testing its effects on predator patch exploitation in situations where predatory mites were free to disperse from prey patches. Adult T. kanzawai females construct three‐dimensional webs on leaf surfaces and usually lay eggs under the webs; however, females that have experienced predation risks, shift oviposition sites onto the webs even in the absence of current predation risks. We compared the predation of eggs on webs deposited by predator‐experienced females with those on leaf surfaces. Predatory mites left prey patches with more eggs unpredated when higher proportions of prey eggs were located on webs, and egg survival on webs was much higher than that on leaf surfaces. These results indicate that a micro‐oviposition shift by predator‐experienced T. kanzawai protects offspring from predation, suggesting adaptive learning and subsociality in this species. Conversely, fecundity and longevity of predator‐experienced T. kanzawai females were not reduced compared to those of predator‐naïve females; we could not detect any costs associated with the learned micro‐oviposition shift. Moreover, the previously experienced predation risks did not promote between‐patch dispersal of T. kanzawai females against subsequently encountered predators. Based on these results, the relationships of between‐patch oviposition site selection and micro‐oviposition shift are discussed.     

Assessment of patch quality by ladybirds: role of larval tracks

Gravid females of the two-spot ladybird, Adalia bipunctata (L.), were deterred from ovipositing when kept in petri dishes that had previously contained conspecific larvae but not conspecific adults, or the larvae of another two species of ladybird, Adalia decempunctata (L.) and Coccinella septempunctata L. The deterrent effect was density dependent and mediated via a chloroform-soluble contact pheromone present in the larval tracks. Similarly, gravid females of C. septempunctata were deterred from ovipositing by conspecific larval tracks and chloroform extracts of these tracks, but not by the tracks or extracts of tracks of A. bipunctata larvae. That is, in ladybirds the larvae produce a species-specific oviposition-deterring pheromone. In the field, the incidence of egg cannibalism in ladybirds increases very rapidly with the density of conspecific eggs or larvae per unit area. Thus, in responding to the species specific oviposition deterring pheromone female ladybirds reduce the risk of their eggs being eaten and spread their offspring more equally between patches. Received: 14 March 1997 / Accepted: 26 August 1997     

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.     

Effects of food and temperature on development,fecundity and life‐table parameters of Adalia bipunctata (Coleoptera: Coccinellidae)

Development, reproduction and life tables of Adalia bipunctata (L.) were studied at three temperatures (19, 23 and 27°C) on a mixture of frozen pollen and Ephestia kuehniella Zeller eggs as a factitious food and on the aphids Myzus persicae (Sulzer) and Acyrthosiphon pisum (Harris) as natural foods. Development time of A. bipunctata on all tested diets decreased with increasing temperature. Mortality was lowest at 23°C, averaging 44.5%, 42.6% and 24.3% on factitious food, A. pisum and M. persicae respectively. The shortest developmental time from egg to adult at this temperature was observed on factitious food (18.55 days). However, the factitious food was inferior to the aphid diets in terms of reproduction, yielding the longest pre‐oviposition period, shortest oviposition period and lowest fecundity. The mean oviposition rate at 23°C varied from 19.94 to 25.03 eggs day^?1 on factitious food and M. persicae respectively. The intrinsic rate of increase (r_m) on different foods increased with increasing temperature and ranged from a minimum of 0.08 females/female/day on factitious food (19°C) to a maximum of 0.18 females/female/day on A. pisum (27°C). The results suggest that a mixture of E. kuehniella eggs and pollen fully support development of A. bipunctata larvae and can be used as an alternative to live aphids in the mass rearing of the pre‐imaginal stages of the predator. However, reproductive performance of a laboratory population may be better on aphids than on the factitious food.     

Laboratory study of cannibalism and interspecific predation in ladybirds

Abstract.

• 1 In the absence of aphids, adult females of Adalia bipunctata (L.) showed a greater reluctance to eat eggs than males.
• 2 Eggs and young larvae were more vulnerable to cannibalism than older larvae and starved larvae were more vulnerable than well-fed larvae.
• 3 Both egg and larval cannibalism is inversely related to the abundance of aphids.
• 4 Eggs are a better food, in terms of larval growth and survival, than aphids.
• 5 In the absence of aphids interspecific predation occurred, but not equally, between the coccinellids A.bipunctata, A.decempunctata (L.), Coccinella septempunctata L. and C.undecempunctata L.
• 6 Larvae and adults of A. bipunctata and C.septempunctata were reluctant to eat conspecific eggs painted with a water extract of the other species' eggs and larvae of C. septempunctata were more likely to die after eating a few eggs of A.bipunctata than vice versa.
• 7 These results indicate that cannibalism occurs mainly when aphid prey is scarce and is adaptive in that it improves the chances of survival, and coccinellids, to varying degrees, are defended against interspecific predation.

     

Habitat or prey specialization in predatory ladybird beetles: a case study of two closely related species

This study examines the niche and diet breadth of two closely related sympatric aphidophagous ladybirds: Adalia decempunctata and A. bipunctata. The degree of habitat specialization of these species is investigated, and its effect on life history traits of females is explored. The importance of prey quality in determining the diet breadth is also examined. The niches occupied by these species in three countries, the UK, Belgium and southern France, are similar: A. decempunctata is an arboreal habitat specialist with a narrower set of prey than A. bipunctata, which is commonly found on several types of vegetation. The niches of the two species overlap on trees. Experiments indicate that habitat specialization has resulted in A. decempunctata investing more in each of its offspring than A. bipunctata. A. decempunctata females lay, relative to their body size, heavier eggs than those of the more generalist A. bipunctata, which results in A. decempunctata having bigger larvae. In addition, A. decempunctata larvae are better at surviving starvation than A. bipunctata larvae. In contrast to the expected pattern in food specialization, our study failed to demonstrate a better efficiency of the specialist when fed its usual prey and a detrimental effect when fed on prey that it is unlikely to encounter in the field. The reproductive performance of the specialist ladybird was better when fed an aphid that it was unlikely to regularly feed on in the field. Therefore, the narrow diet of the specialist ladybird is most likely a consequence of it occupying a narrow habitat rather than the quality of the prey. Although further studies on specialization in predatory insects are needed, the results indicate that unlike the role of plant quality in host specialization in herbivorous insects, prey quality has not been the main determinant of ecological specialization in these predatory insects.     

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.     

Decline in native ladybirds in response to the arrival of Harmonia axyridis: early evidence from England

1. Harmonia axyridis (Coleoptera: Coccinellidae) is an invasive non‐native ladybird in Europe, where it was introduced as a biological control agent of aphids and coccids. 2. This study assesses changes to ladybird species assemblages, in arboreal habitats, over a 3‐year period encompassing the invasion phase of H. axyridis in eastern England. The effects of H. axyridis and other factors (weather and prey availability) on native ladybirds are assessed. 3. Harmonia axyridis increased from 0.1% to 40% of total ladybirds sampled, whilst native aphidophagous species declined from 84% to 41% of total ladybirds. The actual number of native aphidophagous ladybirds per survey decreased from a mean of 19.7 in year 1, to 10.2 in year 3. 4. Three ladybird species in particular experienced declines: Adalia bipunctata, Coccinella septempunctata, and Propylea quattuordecimpunctata. Harmonia axyridis was the most abundant species by the end of the study. 5. The decline in native aphidophagous ladybirds could be attributed to competition for prey and intraguild predation of eggs, larvae, and pupae by H. axyridis. Physiological and behavioural traits of H. axyridis are likely to confer an advantage over native ladybird species.     

Sex differences in foraging behaviour and oviposition site preference in an insect predator, Orius sauteri

The effects of patch quality on the foraging behaviour of an anthocorid predator Orius sauteri (Poppius) were compared between sexes. Prior experience in patches was also studied to determine whether this was a factor affecting oviposition decisions. Patch quality affected patch residence time differently for the two sexes; females stayed much longer in a patch with prey (60 Thrips palmi larvae) than a patch without prey, while males did not remain in any patch for extended periods. Most of the females remained in or moved to patches with prey, whereas males dispersed, irrespective of patch quality. Both females released in patches with prey and females released in patches without prey deposited more eggs per hour in patches with prey than in patches without prey. Females released in patches without prey laid eggs in patches with prey at higher rates than did females released in patches with prey. Causes for the sex difference in patch residence time and allocation are discussed in relation to optimal foraging theory. The significance of selective oviposition and the role of experience in oviposition decisions within heterogeneous environments are also discussed.     

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.     

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.     

Oviposition site preference and developmental performance of a gall‐inducing leafhopper on galled and non‐galled host plants

Oviposition preferences of herbivorous insects affect offspring performance. Both positive and negative links between oviposition preference and offspring performance have been reported for many species. A gall‐inducing leafhopper, Cicadulina bipunctata Melichar (Hemiptera: Cicadellidae), feeds on various Poaceae plants and induces galls of enhanced nutritional value for their offspring. Although gall induction by C. bipunctata improves nymphal performance, the oviposition preference of females between galled and non‐galled host plants is still unclear. In this paper, the nymphal performance and oviposition and feeding‐site preference of C. bipunctata were investigated using galled wheat, Triticum aestivum L., and non‐galled barley, Hordeum vulgare L., as host plants. The survival rate of C. bipunctata on wheat was significantly higher than on barley. In the choice test, significantly more eggs were laid into barley, whereas the number of eggs deposited on both hosts was not significantly different in the no‐choice test. The number of settling individuals per leaf area was not significantly different between wheat and barley, suggesting no clear preference for oviposition between these plants. Experience as a nymph with a growing host did not affect oviposition preference as adult female. The inconsistent correspondence between offspring performance and oviposition preference of C. bipunctata may reflect the high mobility of nymphs and/or differences in leaf area between host plants. The results indicate that the previous finding that oviposition preference and offspring performance are not always positively correlated in herbivorous insects is applicable to gall‐inducing insects.     

Oviposition Behavior of the Predatory Midge Aphidoletes aphidimyza in Response to Aphid Patch Quality

Female Aphidoletes aphidimyza confronts serious challenges from both aphid prey and conspecifics. These challenges constitute strong selective pressures on the predatory midge to have an adaptive oviposition strategy. We did laboratory experiments to investigate clutch size of A. aphidimyza in response to the aphid Rhopalosiphum padi (density and age) and the presence of conspecific eggs (density) and larvae (age) in aphid colonies. The results of our study show that A. aphidimyza female adjusts its foraging effort by assessing the quality of prey patches. The number of eggs laid increased in response to aphid density. However, patches consisting of older aphids received fewer eggs. The number of eggs laid decreased in response to the presence of conspecific eggs, and in response to the presence of 2-day old conspecific larvae. Our study reveals deterrent effects on A. aphidimyza oviposition decisions on clutch size in response to older aphids and the presence of more conspecific eggs and older larvae.     

Oviposition avoidance of parasitized aphid colonies by the syrphid predator Episyrphus balteatus mediated by different cues

Oviposition decisions made by members of a guild of natural enemies can have evolved to avoid intraguild predation, potentially avoiding the disruption of the extraguild prey control. We have studied the oviposition preference of the aphidophagous predator Episyrphus balteatus De Geer (Diptera: Syrphidae) within colonies of Myzus persicae Sulzer (Hemiptera: Aphididae) in the presence of two developmental stages of the aphid parasitoid Aphidius colemani Viereck (Hymenoptera: Aphidiidae). Results from a greenhouse choice experiment showed that E. balteatus females lay significantly fewer eggs in colonies with mummified aphids than in unparasitized colonies. Colonies of parasitized, but not yet mummified did not contain significantly fewer eggs than colonies with unparasitized aphids. In three no-choice experiments, we assessed stimuli coming from aphid honeydew, from the aphids themselves and also from extracts of the aphid bodies, and all of these stimuli mediate the discrimination of mummified aphids from healthy aphids. To a lesser extent these stimuli also contribute to the discrimination against aphids that are parasitized but not yet mummified. These results suggest that the effects of these two species could be complementary for the control of M. persicae, since the species that acts as an intraguild predator, E. balteatus, avoids ovipositing on aphid colonies parasitized by the intraguild prey, A. colemani.     

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.     

Predators induce egg retention in prey

To prevent predation on their eggs, prey often avoid patches occupied by predators. As a result, they need to delay oviposition until they reach predator-free patches. Because many species allocate energy to egg production in a continuous fashion, it is not clear what kind of mechanism prey use to delay oviposition. We used females of the phytoseiid mite Neoseiulus cucumeris to study these mechanisms. Females were placed in patches with pollen, a food source they use for egg production, and they were exposed to another phytoseiid mite, Iphiseius degenerans, which is an intraguild predator of N. cucumeris juveniles. We found that the oviposition of N. cucumeris females on patches with the predator was lower than on patches without the predator. Cues left by the intraguild predator were not sufficient to elicit such behaviour. Females of N. cucumeris reduced oviposition when exposed to the predator by retaining the egg inside their body, resulting in a lower developmental rate once these eggs were laid. Hence, females are capable of retaining eggs, but the development of these eggs continues inside the mother’s body. In this way, females gain some time to search for less risky oviposition sites.     

Oviposition in Cryptolaemus montrouzieri stimulated by wax filaments of its prey

The oviposition responses of Cryptolaemus montrouzieri Mulsant (Coleoptera: Coccinellidae) to the soft scale Eupulvinaria hydrangeae (Steinweden) (Homoptera: Coccidae) and to the mealybug Planococcus citri (Risso) (Homoptera: Pseudococcidae) have been compared in the laboratory. The females delay oviposition and withhold mature eggs in their lateral oviducts in the absence of wax filaments produced by the prey (only present in the ovisac of E. hydrangeae, present in all stages of P. citri). Contact chemical cues perceived by females when probing the wax filaments with their mouthparts are the signals inducing the search for oviposition sites. The second step is under the control of the ovipositor by which females locate confined sites to lay eggs. This oviposition behaviour could have a considerable impact on the prey exploitation strategy of this important biocontrol agent and might help to understand its apparent ineffectiveness in situations of low prey density.     

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.