Survival, growth, and reproduction of two aphid species on sucrose solutions containing host or non-host honeydews

Aphids, like most phloem-feeding insects, commonly exhibit a high degree of host specificity. Plant-specific chemical compounds are likely to serve as important host selection cues for monophagous aphids and such substances could be present in aphid honeydew. Apterous virginoparae ofMyzus persicae (Sulzer) andPhorodon humuli (Schrank) were reared on a buffered sucrose solution containing various aphid honeydews or a mixture of amino acids. In two separate experiments, the host-specificP. humuli (hop aphid) could grow and reproduce only on diets containing honeydew collected from hop (Humulus lupulus L.).M. persicae (the green peach aphid, GPA) did not perform well on diets containing hop honeydew, perhaps because hop is a poor GPA host. Honeydew collected from preferred GPA host plants rape,Brassica napus L., and jimsonweed,Datura stramonium L., allowed GPA growth and reproduction. Hop aphids, however, performed poorly on rape and jimsonweed honeydew diets. Bell pepper,Capsicum annuum L., honeydew supported neither the hop aphid nor GPA. The study of aphid honeydew components may contribute towards a more complete understanding of host preference and selection phenomena in aphids.     

Starving Aphelinus asychis negatively affects host feeding and parasitism on Myzus persicae

Aphelinus asychis (Walker) is an effective biological control agent for many species of aphids found on various crops. To provide strategies for releasing these parasitoids into a crop ecosystem, the effects of a short-duration starvation experiment on A. asychis were measured under laboratory conditions using Myzus persicae (Sulzer) as the host on cabbage and chili pepper plants. The survival rate of starved A. asychis female adults decreased sharply as the starving time increased, and the longevity of the starved parasitoids also decreased significantly. The number of aphids killed by the parasitoids decreased gradually with the extended duration of starvation. In addition, the number of aphids on chili peppers and cabbages killed by starved A. asychis females over their lifespan was significantly lower than that in the control group. Our results indicated that a short period of starvation might not cause significantly negative effects on the parasitoids and may be beneficial for the control of M. persicae at low densities after 1?day; however, starvation for >1?day seriously affected the performance of A. asychis females over their entire lifespan. The parasitoids performed similarly when aphids were fed chili pepper or cabbage plants.     

Functional responses of aphid parasitoids,Aphidius colemani (Hymenoptera: Braconidae) and Aphelinus asychis (Hymenoptera: Aphelinidae)

We evaluated the functional responses of two aphid parasitoids: Aphidius colemani on the green peach aphid Myzus persicae (Hemiptera: Aphididae), and Aphelinus asychis on M. persicae and the potato aphid, Macrosiphum euphorbiae (Hemiptera: Aphididae). Parasitoid oviposition occurred at host densities of 5, 10, 20, 30, 50, 80 or 100 aphids for A. colemani and 5, 10, 20, 30 or 50 aphids for A. asychis. More M. persicae were parasitized by A. colemani than by A. asychis at an aphid density of 50. Among the three types of functional response, type III best described the parasitoid response to the host densities both in A. colemani and A. asychis. The estimated handling time was shorter for A. colemani than for A. asychis (0.017 and 0.043 d, respectively). The proportion of aphids that were parasitized exhibited the same characteristic curve among the three host-parasitoid combinations: a wave form that appeared to be a composite of a decelerating (as in type II) response at low host density and an accelerating-and-decelerating (as in type III) response at medium to high host density. We hypothesize that the novel host species (and its host plant), density-dependent superparasitism, and/or density-dependent host-killing may have induced the modified type III response.     

The susceptibility of Myzus persicae and Brevicoryne brassicae to 14C-phorate in artificial diets

Colonies of Myzus persicae and Brevicoryne brassicae were established on artificial diets and the honeydew produced by them collected on aluminium foils. The diets were later exchanged for others containing a range of ¹⁴C-phorate concentrations. The honey-dew produced while feeding on the treated diets was collected separately and mortalities were recorded. The diets, aphids and their honeydew were subsequently analysed. About 1.6% of the doses applied initially were found in the diets at the end of the bio-assay period. Thin-layer chromatography of diets containing LC₅₀ concentrations of insecticides showed that phorate and its metabolites were present in similar proportions. The LC₅₀ values were 15.5 nM and 277 nM phorate equivalents for B. brassicae and M. persicae respectively.     

Dynamic host-feeding and oviposition behavior of an aphid parasitoid <Emphasis Type="Italic">Aphelinus asychis</Emphasis>

In order to maximize the lifetime reproductive success of parasitoids, they should be induced to dynamically accept individual hosts that have different suitability for oviposition. Parasitoids tend to exhibit higher host-selective behavior when their egg load is limited, and are less selective if they are facing time constraints. Here, we evaluated the effects of parasitoid age on egg load, fecundity and host instar preference of a honey-fed aphid parasitoid, Aphelinus asychis Walker (Hymenoptera: Aphelinidae). Host selective experiment was conducted to measure host-preference of honey-fed A. asychis females at different ages, using the second and fourth instars of the green peach aphid Myzus persicae as their hosts. The results showed that the choice of host-instar for oviposition was significantly influenced by the parasitoid age. Honey-fed parasitoids in the age groups of 1, 5, 10 and 20 days tended to parasitize predominantly second-instar aphids, whereas 15-days old parasitoids showed no significant preference of host instars. On the other hand, host-feeding preference was not affected by parasitoid age. Parasitoid females of all ages preferred younger aphids to older aphids. This result could help evaluate the effectiveness of A. asychis for biological control of M. persicae when they encountered mixed-instar aphids in the field. In addition, the results might be helpful in assessing the host killing effects of other host-feeding parasitoids.     

Osmoregulation by the aphid Myzus persicae: A physiological role for honeydew oligosaccharides

The dry matter content of honeydew produced by Myzus persicae feeding on artificial diets increased with increasing sucrose concentrations of the diet. Whereas the diet osmolalities ranged from 828 to 1800 milliosmolal, the honeydew osmolality was relatively constant (about 500 milliosmolal). This osmoregulatory capacity is achieved largely by variations in the mean molecular weight of glucose-containing honeydew oligosaccharides.     

Interactions betweenAcyrthosiphon kondoi [Homoptera: Aphidoidea] andAphelinus asychis [Hymenoptera: Chalcidoidea] and other parasites and hosts

In laboratory trials to investigate the parasite/host spectra of certain aphid pests and hymenopterous parasites, the aphidAcyrthosiphon kondoi Shinji encapsulated the egg of the aphelinid parasiteAphelinus asychis Walker. The resultant brown, sclerotic capsule was formed within 24 h of exposure of the aphid to parasitization and as far as is known prevented the development of the parasite to the larval stage. The capsule remained throughout the life of the aphid, whose longevity and fecundity were apparently not seriously impaired. A small number ofAphelinus escaped encapsulation, especially in aphids already containing capsule(s), and developed into normal, reproductive adults.A. kondoi did not encapsulate, andA. asychis was not encapsulated by any other species. However, thoughA. asychis readily parasitizedAphis citricola van der Goot,A. nerii Boyer de Fonscolombe andToxoptera citricidus (Kirkaldy), most of its progeny ceased development in these aphids before reaching the mummification stage, and died within the dead or dying, non-mummified aphid host.     

Effects of aphid honeydew sugars on the longevity and fecundity of the aphidophagous gall midge Aphidoletes aphidimyza

The predatory gall midge Aphidoletes aphidimyza, which is used for augmentative biological control of aphids in greenhouses, uses aphid honeydew as an energy source. Currently, Rhopalosiphum padi on barley plants and Melanaphis sacchari on sorghum plants are used as the banker plant systems for A. aphidimyza to control Aphis gossypii on eggplant in Japan. We analyzed the sugar components of the honeydew of these three species by HPLC. The major components of honeydew were sucrose, fructose, and melezitose for A. gossypii; glucose and fructose for R. padi; and glucose, fructose, and melezitose for M. sacchari. Maltose and trehalose were minor components of the honeydew of these species. We investigated the influence of sugars, including three artificial aphid honeydews, six sugar components, and distilled water, on the longevity of unmated A. aphidimyza. Both females and males attained the greatest longevity on sucrose and artificial honeydew of A. gossypii. Mean longevities of both females and males were shortest when they were provided only with water. We conducted another experiment in which a mated female was released in a cage with an eggplant seedling infested with A. gossypii and fed with sucrose or only water. Females fed with sucrose lived significantly longer and had higher lifetime fecundity than those fed only water.     

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.     

Females of Cotesia vestalis,a parasitoid of diamondback moth larvae,learn to recognise cues from aphid‐infested plants to exploit honeydew

1. To maximise their reproductive success, the females of most parasitoids must not only forage for hosts but must also find suitable food sources. These may be nectar and pollen from plants, heamolymph from hosts and/or honeydew from homopterous insects such as aphids. 2. Under laboratory conditions, females of Cotesia vestalis, a larval parasitoid of the diamondback moth (Plutella xylostella) which does not feed on host blood, survived significantly longer when held with cruciferous plants infested with non‐host green peach aphids (Myzus persicae) than when held with only uninfested plants. 3. Naïve parasitoids exhibited no preference between aphid‐infested and uninfested plants in a dual‐choice test, but those that had been previously fed aphid honeydew significantly preferred aphid‐infested plants to uninfested ones. 4. These results suggest that parasitoids that do not use aphids as hosts have the potential ability to learn cues from aphid‐infested plants when foraging for food. This flexible foraging behaviour could allow them to increase their lifetime reproductive success.     

Living on a high sugar diet: the fate of sucrose ingested by a phloem-feeding insect,the pea aphid Acyrthosiphon pisum

The natural diet of aphids, plant phloem sap, generally contains high concentrations of sucrose. When pea aphids (Acyrthosiphon pisum) were fed on chemically defined diets containing sucrose radiolabelled in the glucose or fructose moiety, 2 to 12-fold and 87 to 110-fold more radioactivity was recovered from the tissues and honeydew, respectively, of aphids that ingested [U-(14)C-glucose]-sucrose than from those ingesting [U-(14)C-fructose]-sucrose. The total radioactivity recovered was 70% of the ingested [U-(14)C-glucose]-sucrose and <5% of ingested [U-(14)C-fructose]-sucrose. The dominant honeydew sugars produced by aphids feeding on 0.75 M sucrose diets were oligosaccharides comprising glucose. In vitro the guts of pea aphids had high sucrase activity, 1-5 U mg(-1) protein, generating equimolar glucose and fructose except at high sucrose concentrations where glucose production was inhibited (K(si)=0.1 M). These data suggest that the fructose moiety of ingested sucrose is assimilated very efficiently and may be preferentially respired by the aphid, and that the glucose moiety of sucrose is incorporated into oligosaccharides by the transglucosidase activity of the gut sucrase at high sucrose concentrations. These differences in the fate of sucrose-derived glucose and fructose are important elements in both the carbon nutrition and osmoregulation of aphids.     

Ecology of the aphid pests of protected pepper crops and their parasitoids

Myzus persicae, Macrosiphum euphorbiae, Aphis gossypii and Aulacorthum solani (Homoptera: Aphididae) are principal pests of protected pepper crops in southeastern Spain. Our goal was to determine the incidence of aphids on pepper crops and the role of vegetation surrounding greenhouses as a source of aphids and their parasitoids. The population dynamics were followed in six commercial greenhouses during 3 years. Another 82 greenhouses and their surrounding vegetation were surveyed occasionally. Myzus persicae had the highest incidence in pepper greenhouses followed by M. euphorbiae and A. solani. Parasitism of all aphid species in greenhouses was low, Aphidius matricariae and Aphidius colemani being the most abundant parasitoids. Myzus persicae and Macrosiphum euphorbiae were the most abundant and polyphagous aphids, being present on 77 and 55% of the plants sampled outside greenhouses, respectively; species of Brassicaceae were the main hosts for both aphids. Aulacorthum solani was only present on Malva parviflora and at low numbers. Outside greenhouses, A. matricariae was the most common parasitoid of M. persicae, followed by Diaeretiella rapae and A. colemani. Aphidius matricariae was the most polyphagous, being present in 10 out of 22 aphid species. Macrosiphum euphorbiae and A. solani were both parasitised by A. ervi and Praon volucre. Aphelinus asychis was found on A. solani. Parasitoids were found in other aphids not attacking pepper. The role of natural vegetation as a reservoir of aphid pests of pepper and of parasitoids is discussed.     

Sugar, organic acid, phenolic acid and plant growth regulator content of extracts of honeydew of the aphid Myzus persicae and of its host plant, Raphanus sativus

The honeydew of Myzus persicae feeding on radish seedlings contains glucose, fructose, trehalose, melezitose and sucrose, of which glucose and fructose are present in radish seedlings. In addition, the honeydew contains eight organic acids, of which seven are present in uninfested seedlings and six are present in infested radish seedlings: of the eighteen phenolic acids in the honeydew, five are present in uninfested radish seedlings. Auxins, gibberellins, growth inhibitors and cytokinins are present in the honeydew. The presence of carbonate and bicarbonate previously recorded in honeydew of M. persicae could not be confirmed, but ammonia is present in fresh honeydew and accounts for its high pH.     

Influence of Experience on the Response of Bathyplectes curculionis (Hymenoptera: Ichneumonidae), a Nonaphidophagous Parasitoid, to Aphid Odor

Bathyplectes curculionis (Thomson) is an introduced natural enemy of the alfalfa weevil in North America. The wasp requires carbohydrate foods as an adult. Adult wasps have increased longevity and fecundity when provided access to pea aphid, Acyrthosiphon pisum (Harris), honeydew in the laboratory, and adults respond positively to the presence of pea aphids in alfalfa fields. However, it is unknown how these wasps find aphid honeydew in the field. In a series of Y-tube olfactometer experiments, we evaluated the response of naïve and experienced adult female B. curculionis to odors from pea aphids, alfalfa, and pea aphids on alfalfa. Naïve adult females did not respond positively to pea aphid odor even when hungry. But adult females were able to learn aphid odor, and the mechanism of learning appears to be associative rather than by sensitization. Naïve females also showed no preference for alfalfa odor but learned alfalfa odor through sensitization. The wasps did not distinguish between alfalfa with aphids and alfalfa without aphids, even after exposure to aphids or alfalfa with aphids. However, they preferred pea aphid odor to alfalfa odor after a feeding experience in the presence of pea aphid odors. But after exposure to mixed odors of aphids and alfalfa while feeding, B. curculionis females preferred the odor of alfalfa to the odor of pea aphids. These results suggest that alfalfa odors mask or override aphid odors when aphids are associated with alfalfa (as happens naturally), thus interfering with the wasp's ability to respond to learned aphid odors. Therefore, although the wasps are capable of learning to find pea aphids and their honeydew in a simplified laboratory setting, it appears unlikely that they do so in the field.     

Host plant recognition in monophagous weevils: Specialization ofCeutorhynchus inaffectatus to glucosinolates from its host plantHesperis matronalis

Several aphid honeydews were incorporated into sucrose solutions and presented to hop aphids, Phorodon humuli (Schrank), as artificial diets in free-choice bioassays. Small additions of honeydew collected from two species of aphid feeding on hop, Humulus lupulus L., arrested the searching behavior of the hop aphid and appeared to stimulate prolonged periods of ingestion. This effect was more dependent on the host plant honeydew source than the species of aphid that produced the honeydew. Aphid honeydews collected from plants other than hop (non-hosts to P. humuli) contained hop aphid phagostimulants that were less effective. Our results indicate that analysis of aphid honeydew could help describe chemical cues involved in the recognition of appropriate host plants by aphid species.     

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.     

Intraguild predation on the aphid parasitoid <Emphasis Type="Italic">Aphelinus asychis</Emphasis> by the ladybird <Emphasis Type="Italic">Harmonia axyridis</Emphasis>

We investigated intraguild predation (IGP) on an aphid parasitoid, Aphelinus asychis Walker (Hymenoptera: Aphelinidae), by the multicolored Asian ladybird, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), and used the green peach aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae) as the prey/host in the laboratory. The ladybirds reared on artificial diet and on aphids consumed more aphids than mummies, while those reared on parasitized aphids consumed similar numbers of aphids and mummies. The ladybirds chose more mummies in treatments when mummies were more abundant, and more aphids when numbers of aphids and mummies were equal, or when aphids were more abundant. However, at all density treatments, rejection rates of mummies (36%) were much greater than of aphids (2%). H. axyridis prey on more aphids than A. asychis mummies, which enhances biological control by the two species. However, prior feeding experience affected subsequent choice, increasing the competition between natural enemies which would reduce their combined effectiveness for biological control.     

Effects of honeydew sugar composition on the longevity of Aphidius ervi

Feeding on sugar‐rich foods such as nectar and honeydew is important for survival of many adult parasitoids. Especially in agricultural systems, honeydew is often the most prevalent carbohydrate source. However, relative to plant nectar, honeydew may be relatively unsuitable, as a result of an unfavourable sugar composition or the presence of secondary plant compounds. We studied survival of the aphid parasitoid Aphidius ervi Haliday (Hymenoptera: Braconidae) on honeydew collected from various aphid species feeding on potato (Solanum tuberosum L., cv. Desiree) (Solanaceae), wheat (Triticum aestivum L., cv. Bobwhite) (Poaceae), or artificial diet, as well as the sugar composition of the different honeydews. Honeydews from the tested aphid species on potato, wheat, or artificial diet were found to be relatively suitable food sources for adult A. ervi, although not always as suitable as a 2 M sucrose solution. There were differences in honeydew sugar composition among the different aphid species on the various host plants. Multivariate statistics showed that the factor ‘aphid species’ had a significant influence on the sugar composition of the honeydew, explaining 27% of the variation in the potato system and 89% in the wheat system. When exploring the relationship between carbohydrate composition of the honeydews from aphids on potato and wheat plants, and their nutritional value for A. ervi, data revealed that differences in parasitoid longevity can to some extent be explained by carbohydrate composition. Furthermore, our results confirm that sucrose and its hexose components glucose and fructose are very suitable carbohydrate sources for hymenopteran parasitoids and show that parasitoid survival on an equimolar solution of the two monosaccharides glucose and fructose does not exceed performance on the disaccharide sucrose.     

Effect of six carbohydrate sources on the longevity of a whitefly parasitoid Eretmocerus hayati (Hymenoptera: Aphelinidae)

Parasitoid adults often acquire carbohydrates by feeding on floral nectar and honeydew which provides them with energy and prolongs their life span. The concentration and type of saccharide in nectar and honeydew are variable by species of plant and insect. To explore the effects of various sugar type and concentrations on parasitoid fitness, we compared 5%, 10% and 20% (w/v) solutions of six different sugar resources (glucose, fructose, sucrose, trehalose, melezitose and honey) on the longevity of Eretmocerus hayati, a larval parasitoid of the whitefly Bemisia tabaci in China. Male and female longevity was increased by all of the sugar diets, but female wasps survived longer than the males when the same sugar diet was supplied. Female parasitoids feeding on 10% glucose and 10% honey increased longevity, respectively up to 6.2- and 5.9-fold longer than distil water; 5% honey and 10% fructose had the greatest effects on male longevity, up to 3.5- and 3.3-fold. All six sugar diets, no matter which concentration, significantly changed the survival curves. Glucose, sucrose and honey were optimal sugar diets for this wasp, and 10% was the optimal concentration. Our results could provide an insight into the nutritional requirements of E. hayati under laboratory conditions. Such information can be a basis to improve the longevity of this biological control agent by sugar feeding during the indoor mass-rearing process.     

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.