Impact of the entomopathogenic fungus Verticillium lecanii on development of an aphid parasitoid, Aphidius colemani

The parasitoid Aphidius colemani developed normally (approximately 90% adult emergence) when its cotton aphid (Aphis gossypii) host was treated with Verticillum lecanii conidia 5 or 7 days after parasitization. Fungus exposure 1 day before or up to 3 days after parasitization, however, reduced A. colemani emergence from 0 to 10%. Also, numbers of spores and mycelial fragments in aphid homogenates were much higher in aphids exposed to the fungus up to 3 days after parasitization than in aphids treated after 5 or 7 days. Our results suggest that the parasitoid and fungus may be used together for aphid biocontrol as long as fungus applications are timed to allow late-instar development of the parasitoid.     

Preference and performance of the hyperparasitoid Syrphophagus aphidivorus (Hymenoptera: Encyrtidae): fitness consequences of selecting hosts in live aphids or aphid mummies

Abstract.  1. Theoretical models predict that ovipositional decisions of parasitoid females should lead to the selection of the most profitable host for parasitoid development. Most parasitoid species have evolved specific adaptations to exploit a single host stage. However, females of the aphid hyperparasitoid Syrphophagous aphidivorus (Mayr) (Hymenoptera: Encyrtidae) display a unique and atypical oviposition behaviour by attacking either primary parasitoid larvae in live aphids, or parasitoid pupae in dead, mummified aphids.
2. In the laboratory, the correlation between host suitability and host preference of S. aphidivorus on the host Aphidius nigripes Ashmead parasitising the aphid Macrosiphum euphorbiae (Thomas) was investigated.
3. The relative suitability of the two host stages was determined by measuring hyperparasitoid fitness parameters (survival, development time, fecundity, sex ratio, and adult size of progeny), and calculating the intrinsic rate of population increase ( r _m). Host preference by S. aphidivorus females and the influence of aphid defence behaviour on host selection was also examined.
4. Hyperparasitoid offspring performance was highest when developing from hosts in aphid mummies and females consistently preferred this host to hosts in parasitised aphids. Although aphid defensive behaviour may influence host selection, it was not a determining factor. Ecological and evolutionary processes that might have led to dual oviposition behaviour in S. aphidivorus are discussed.     

Contact Kairomones Mediating the Foraging Behavior of the Aphid Hyperparasitoid Alloxysta victrix (Westwood) (Hymenoptera: Charipidae)

A variety of host-related substances was assessed in relation to their ability to induce arrestment and antennal examination behavior in adult females of the aphid hyperparasitoid Alloxysta victrix (Westwood). In laboratory bioassays, whole-body homogenates of both unparasitized host aphids [Myzus persicae (Sulzer)] and those parasitized by the primary parasitoid Aphidius colemani Viereck failed to elicit a response. However, significant kairomonal activity was associated with aphid cornicle secretions, aphid honeydew, and solvent extracts of parasitized aphids. Solvent extracts of unparasitized aphids (in either hexane or butan-1-ol) failed to elicit arrestment or antennal examination behavior in hyperparsitoid females. The response to aphid honeydew was significantly lower in experienced females than in naive individuals, suggesting that even relatively strong innate responses can be modified by learning.     

Comparing and contrasting life history variation in four aphid hyperparasitoids

1. In primary parasitoids, significant differences in life history and reproductive traits are observed among parasitoids attacking different stages of the same host species. Much less is known about hyperparasitoids, which attack different stages of primary parasitoids. 2. Parasitoids exploit hosts in two different ways. Koinobionts attack hosts that continue feeding and growing during parasitism, whereas idiobionts paralyse hosts before oviposition or attack non‐growing host stages, e.g. eggs or pupae. 3. Koino‐/idiobiosis in primary parasitoids are often associated with different expression of life history trade‐offs, e.g. endo‐ versus ectoparasitism, high versus low fecundity and short versus long life span. 4. In the present study, life history parameters of two koinobiont endoparasitic species (Alloxysta victrix; Syrphophagus aphidivorus), and two idiobiont ectoparasitic species (Asaphes suspensus; Dendrocerus carpenteri) of aphid hyperparasitoids were compared. These hyperparasitoids attack either the parasitoid larva in the aphid before it is killed and mummified by the primary parasitoid or the parasitoid prepupa or pupa in the dead aphid mummy. 5. There was considerable variation in reproductive success and longevity in the four species. The idiobiont A. suspensus produced the most progeny by far and had the longest lifespan. In contrast, the koinobiont A. victrix had the lowest fecundity. Other developments and life history parameters in the different species were variable. 6. The present results reveal that there was significant overlap in life history and reproductive traits among hyperparasitoid koinobionts and idiobionts, even when attacking the same host species, suggesting that selection for expression of these traits is largely association specific.     

Influence of host size variation on the development of a koinobiont aphid parasitoid, Lysiphlebus ambiguus Haliday (Braconidae, Hymenoptera)

To determine whether host body size is the currency used by the aphidiine parasitoid, Lysiphlebus ambiguus Haliday (Hymenoptera: Braconidae), in assessing host quality, the aphid, Aphis fabae Scopoli (Homoptera: Aphididae), was reared at either high or low temperature to yield hosts of the same instar with different body sizes. Cohorts of A. fabae raised at 15 degrees C and 30 degrees C and exposed to individual female L. ambiguus in no-choice tests were successfully parasitized in all host stages from 1st instar nymphs to adults. However, younger and smaller aphids were more susceptible to parasitism than older and larger nymphs or adults, as measured by the number of mummies produced. For aphid cohorts reared at 15 degrees C, the proportion of female progeny, progeny adult size, and development time all increased linearly with aphid size at the time of attack. In contrast, for aphid cohorts raised at 30 degrees C, the proportion of female progeny and progeny adult size declined with aphid size, while development time remained unaffected. Through manipulation of host rearing temperature, we have shown that at cooler temperatures the koinobiont parasitoid, L. ambiguus, responds to host size in the same way as an idiobiont parasitoid, but that this response is compromised at higher temperatures. Our results suggest that differential mortality during development is likely to influence the observed secondary sex ratio in relation to aphid size for aphid cohorts raised at higher temperatures due to disruption of the activity of the host's primary endosymbiont and that such reduced nutritional quality of aphids cannot be compensated by increased development time.     

Foraging behaviour at the fourth trophic level: a comparative study of host location in aphid hyperparasitoids

In studies of foraging behaviour in a multitrophic context, the fourth trophic level has generally been ignored. We used four aphid hyperparasitoid species: Dendrocerus carpenteri (Curtis) (Hymenoptera: Megaspilidae), Asaphes suspensus Walker (Hymenoptera: Pteromalidae), Alloxysta victrix (Westwood) (Hymenoptera: Alloxystidae) and Syrphophagus aphidivorus (Mayr) (Hymenoptera: Encyrtidae), to correlate their response to different cues with their ecological attributes such as host range and host stage. In addition, we compared our results with studies of primary parasitoids on the same plant–herbivore system. First, the olfactory response of females was tested in a Y‐tube olfactometer (single choice: plant, aphid, honeydew, parasitised aphid, aphid mummy, or virgin female parasitoid; dual choice: clean plant, plant with aphids, or plant–host complex). Second, their foraging behaviour was described on plants with different stimuli (honeydew, aphids, parasitised aphids, and aphid mummies). The results indicated that olfactory cues are probably not essential cues for hyperparasitoid females. In foraging behaviour on the plant, all species prolonged their total visit time and search time as compared to the control treatment (clean plant). Only A. victrix did not react to the honeydew. Oviposition in mummies prolonged the total visit time because of the long handling time, but the effect of this behaviour on search time could not be determined. No clear correlation between foraging behaviour and host stage or host range was found. In contrast to specialised primary aphid parasitoids that have strong fixed responses to specific kairomones and herbivore‐induced synomones, more generalist aphid hyperparasitoids seem to depend less on volatile olfactory stimuli, but show similarities with primary parasitoids in their use of contact cues while searching on a plant.     

Endoparasitism in cereal aphids: molecular analysis of a whole parasitoid community

Insect parasitoids play a major role in terrestrial food webs as they are highly diverse, exploit a wide range of niches and are capable of affecting host population dynamics. Formidable difficulties are encountered when attempting to quantify host–parasitoid and parasitoid–parasitoid trophic links in diverse parasitoid communities. Here we present a DNA-based approach to effectively track trophic interactions within an aphid–parasitoid food web, targeting, for the first time, the whole community of parasitoids and hyperparasitods associated with a single host. Using highly specific and sensitive multiplex and singleplex polymerase chain reaction, endoparasitism in the grain aphid Sitobion avenae (F) by 11 parasitoid species was quantified. Out of 1061 aphids collected during 12 weeks in a wheat field, 18.9% were found to be parasitized. Parasitoids responded to the supply of aphids, with the proportion of aphids parasitized increasing monotonically with date, until the aphid population crashed. In addition to eight species of primary parasitoids, DNA from two hyperparasitoid species was detected within 4.1% of the screened aphids, with significant hyperparasitoid pressure on some parasitoid species. In 68.2% of the hyperparasitized aphids, identification of the primary parasitoid host was also possible, allowing us to track species-specific parasitoid-hyperparasitoid links. Nine combinations of primary parasitoids within a single host were found, but only 1.6% of all screened aphids were multiparasitized. The potential of this approach to parasitoid food web research is discussed.     

Host handling and specificity of the hyperparasitoid wasp, Dendrocerus carpenteri (Curtis) (Hym., Megaspilidae): importance of host age and species

The oviposition behaviour of Dendrocerus carpenteri (Curtis), an ectophagous hyperparasitoid of aphidiine wasps inside mummified aphids was examined. Hyperparasitoids were provided in the laboratory with pea aphids ( Acyrthosiphon pisum ) which had been parasitized by three different species of aphidiine wasps ( Aphidius ervi, Ephedrus californicus and Praon pequodorum ) ranging in physiological age from the late larval stage to the late pupal stage. Females accepted only the hosts inside mummified aphids; they ignored live aphids, and did not accept dead, but not yet mummified aphids, although the latter were sometimes probed with the ovipositor. Female behaviour in handling A. ervi or E. californicus mummies did not change with experience; handling and oviposition times were stereotypic. However, naive females needed experience to locate the cocoon of P. pequodorum and distinguish it from the empty aphid mummy. Host acceptance and specificity were influenced more by the developmental stage than the species of the primary parasitoid. In dichotomous choice tests, hyperparasitoids 'preferred' prepupae over younger pupae of A. ervi , but they did not distinguish between these stages of E. californicus; older pupae were accepted at a low rate. Host preference was not influenced by conditioning on the rearing host. We consider several constraints on the host range of D. carpenteri , and discuss alternative explanations of differential hyperparasitism in the field.     

Superparasitism limitation in an aphid parasitoid: cornicle secretion avoidance and host discrimination ability

Superparasitism avoidance by the endoparasitoid Aphidius rhopalosiphi De Stefani Perez on the grain aphid, Sitobion avenae was studied. Experiments were carried out in which aphids were exposed to two consecutive attacks by parasitoids. Results showed that superparasitism avoidance in A. rhopalosiphi was mediated by two successive stimuli whose effectiveness depended on the time interval between attacks. For short time intervals (<16 h), host rejections were mainly associated with the presence of dried cornicle secretion on the host's body which was exuded during the first attack. The repellency of this secretion declined with the time interval between attacks, becoming ineffective 2 days after the first parasitization, and allowed females to reject up to 30% of parasitized hosts. For longer time intervals (>/=16 h), host rejection behavior was a response of parasitoid females to internal changes in host quality associated with parasite development. This response gradually increased with an increase in time interval, reaching no more than 60%, 96 h after initial parasitization. This host discrimination ability did not allow females to distinguish between hosts parasitized by themselves or by conspecifics. Consequently, these findings suggest that superparasitism is a common event in A. rhopalosiphi and especially on recently parasitized hosts.     

Impact of a parasitoid on the bacterial symbiosis of its aphid host

Embryo production in aphids is absolutely dependent on the function of symbiotic bacteria, mainly Buchnera, and the growth and development of koinobiont parasitoids in aphids requires the diversion of nutrients from aphid embryo production to the parasitoid. The implication that the bacterial symbiosis may be promoted in parasitized aphids to support the growing parasitoid was explored by analysis of the number and biomass of mycetocytes, and the aphid cells bearing Buchnera, in the pea aphid Acyrthosiphon pisum Harris (Hemiptera: Aphididae) parasitized by the wasp Aphidius ervi Haliday (Hymenoptera: Braconidae). Aphids hosting a young larval parasitoid bore more mycetocytes of greater total biomass, and embryos of lower biomass than unparasitized aphids. Furthermore, one of the three aphid clones tested, which limited teratocyte growth (giant cells of parasitoid origin having a trophic role), bore smaller mycetocytes and larger embryos, than one or both of the two aphid clones with greater susceptibility to the parasitoid. These data suggest that susceptibility of the aphid‐Buchnera symbiosis to parasitoid‐mediated manipulation may, directly or indirectly, contribute to aphid susceptibility to parasitoid exploitation.     

Effect of temperature and host stage on performance of Aphelinus varipes Förster (Hym., Aphelinidae) parasitizing the cotton aphid, Aphis gossypii Glover (Hom., Aphididae)

Development time, mummification, pupal mortality, host feeding and sex ratio of a Norwegian strain of Aphelinus varipes Förster parasitizing the cotton aphid, Aphis gossypii Glover were studied at 20, 25 and 30°C in controlled climate cabinets. Petri dishes with cucumber ( Cucumis sativus L) leaves on agar were used as experimental units. Cotton aphids in different larval instars and as adults, reared at the three different temperatures, were presented to A. varipes in a `no-choice' situation for 6 h. These presentations were done at 25°C in each experiment to avoid an influence of temperature on parasitization rate. More first instar aphids were parasitized than third and fourth instars among the aphids reared at 20°C. Pupal mortality of the parasitoid was not influenced by temperature. It was lower in aphids parasitized as adults than in aphids parasitized in second instar. The sex ratio of A. varipes was female-biased, and varied between 92% females developed from aphids reared at 25°C and 70% from aphids reared at 20°C. The sex ratio was not significantly influenced by host stage. The development time of A. varipes ranged from 17.5 days at 20°C to 9.8 days at 30°C.     

Host instar and host plant effects on Aphidius colemani

Abstract:  The effect of Myzus persicae age (I–IV instar nymphs) on parasitism by Aphidus colemani was investigated in choice experiments with either aubergine ( Solanum melongena L.) or pepper ( Capsicum annuum L.) as the aphid host plant species. Aphidius colemani could develop successfully to the mummy stage in all ages of aphid tested, on both pepper and aubergine plants. The greatest proportion of parasitoid mummies was found with II and III aphid instars on pepper and on I, II and III aphid instars on aubergine. On aubergine, I instar nymphs were also parasitized to an appreciable degree. Successful parasitism of IV instar nymphs was consistently low on both crops. The potential implications of host plant effects on the effectiveness of A. colemani as a biological control agent are discussed.     

The developmental strategy of an idiobiont ectoparasitoid, Dendrocerus carpenteri : influence of variations in host quality on offspring growth and fitness

Dendrocerus carpenteri (Curtis) (Hymenoptera: Megaspilidae) is a solitary hyperparasitoid, which attacks prepupal and pupal stages of hymenopteran parasitoids inside mummified aphids. The larva feeds externally on the host, which is envenomed by the female at oviposition. To evaluate the influence of variations in host quality on the growth, development and fitness of D. carpenteri, we varied the size and developmental stage of the primary parasitoid host (Aphidius ervi Haliday), which was reared on different instars of pea aphid [Acyrthosiphon pisum (Harris)] and English grain aphid [Sitobion avenae (F.)]. Within each kind of host, females eclosed from the relatively larger mummies, while males eclosed from the smaller mummies. Host size and hyperparasitoid size were correlated, and females were larger than males. In hyperparasitoids developing on prepupal and pupal hosts, development time from oviposition to adult eclosion was proportional to size; females required more time for development than males. The mean relative growth rate was the same in males and females and increased with host quality, as predicted by the growth model of Mackauer and Sequeira (1993) for idiobiont parasitoids. Larvae developing on late-pupal stages and pharate adults of A. ervi were unable to consume sclerotized host tissues; they were smaller and needed more time for development. The average number of mature eggs at eclosion was six, except in females developing on suboptimal hosts, which contained only one egg or none. Egg volume was correlated with female size, possibly reflecting differences in larval ontogeny. We provide equations describing the relationship between host quality as indexed by hind-tibia length of the mummified aphid and adult body size in terms of dry mass, development time and mean relative growth rate of D. carpenteri. We discuss the usefulness of host size as a proxy of host quality for idiobiont parasitoids, and provide examples of exceptions. Received: 14 December 1997 / Accepted: 23 July 1998     

The influence of parasitism on wing development in male and female pea aphids

Wing formation in presumptive alate morphs (virginoparae and males) was observed for the pea aphid, Acyrthosiphon pisum, exposed to attack by the parasitoid, Aphidius ervi, at different stages of host development. Morphological abnormalities in parasitized aphids such as complete apterization (development of a wingless form), formation of rudimentary wing buds, and deformed wings indicate a possible disruption of the endocrine system. Changes in the body shape and the number of olfactory secondary rhinaria on the antennae could indicate an influence of juvenile hormone in parasitized A. pisum but the development of fifth-stadium supernumerary larvae (indicated by an extra moult and which can be induced by exogenous juvenile hormone treatments) was not found in parasitized aphids. In addition, while apterization of virginoparae can also be induced by the pro-allatocidal compound Precocene III, this was not possible in the male. Males which survived parasitoid attack without forming aphid mummies (indicating that oviposition had not occurred) developed as wingless individuals suggesting that the reproductive-tract-fluids from the female parasitoid were important in the wing inhibition process. Teratocytes from the parasitoid appeared to promote developmental arrest in parasitized aphids.     

Effect of parasitism on flight behavior of the soybean aphid, Aphis glycines

Many aphid species possess wingless (apterous) and winged (alate) stages, both of which can harbor parasitoids at various developmental stages. Alates can either be parasitized directly or can bear parasitoids eggs or larvae resulting from prior parasitism of alatoid nymphs. Winged aphids bearing parasitoid eggs or young larvae eventually still engage in long-distance flights, thereby facilitating parasitoid dispersal. This may have a number of important implications for biological control of aphids by parasitoids. In this study, we determined the effect of parasitism by Aphelinus varipes (Hymenoptera: Aphelinidae) on wing development and flight of the soybean aphid, Aphis glycines (Hemiptera: Aphididae). We also quantified the influence of aphid flight distance on subsequent A. varipes development. Parasitism by A. varipes was allowed at different A. glycines developmental stages (i.e., alatoid 3rd and 4th-instar nymphs, alates) and subsequent aphid flight was measured using a computer-monitored flight mill. Only 35% of aphids parasitized as L3 alatoid nymphs produced normal winged adults compared to 100% of L4 alatoids. Flight performance of aphids parasitized as 4th-instar alatoid nymphs 24 or 48 h prior to testing was similar to that of un-parasitized alates of identical age, but declined sharply for alates that had been parasitized as 4th-instar alatoid nymphs 72 and 96 h prior to testing. Flight performance of aphids parasitized as alate adults for 24 h was not significantly different from un-parasitized alates of comparable ages. Flight distance did not affect parasitoid larval or pupal development times, or the percent mummification of parasitized aphids. Our results have implications for natural biological control of A. glycines in Asia and classical biological control of the soybean aphid in North America.     

The reactions of two cereal aphid parasitoids, Aphidius uzbekistanicus and A. ervi to host aphids and their food-plants

ABSTRACT. A Y-tube olfactometer was used to test the reactions of the hymenopteran cereal aphid parasitoids Aphidius uzbekistanicus Luzhetski and A. ervi Haliday to odours from aphids and their host plants. Only females responded to aphids but both sexes responded to plant odours. A. uzbekistanicus responded to the cereal aphids Sitobion avenae (F.) and Metopolophium dirhodum (Walker) whilst A. ervi , which has a broad host range, responded to M. dirhodum and the pea aphid, Acyrthosiphon pisum. Female A. uzbekistanicus responded to wheat leaves only but males responded to a range of plant material. Both male and female A. ervi responded to wheat and bean leaves. The failure of A. ervi to respond to either nettle aphids, Microlophium carnosum (Bukt.), or nettle leaves, despite its frequent parasitization of this aphid in the field, suggests the existence of more than one race of the parasitoid and casts doubts on the usefulness of alternative hosts as reservoirs for A. ervi in integrated control programmes. Males of both species responded to their respective females suggesting the presence of a sex specific attractant.     

Within-patch foraging behaviour of the aphid parasitoidAphidius funebris: plant architecture, host behaviour, and individual variation

The influence of plant architecture, host colony size, and host colony structure on the foraging behaviour of the aphid parasitoidAphidius funebris Mackauer (Hymenoptera: Aphidiidae) was investigated using a factorial experimental design. The factorial design involved releasing individual parasitoid females in aphid colonies consisting of either 10 or 20 individuals ofUroleucon jaceae L. (Homoptera: Aphididae) of either only larval instar L3 or a mixture of host instars, both on unmanipulated plants and on plants that had all leaves adjacent to the colony removed. Interactions between the parasitoid and its host were recorded until the parasitoid had left the plant. The time females spent on the host plant and the number of eggs laid varied greatly among females. Host colony size significantly affected patch residence time and the number of contacts between parasitoids and aphids. Plant architecture influenced the time-budget of the parasitoids which used leaves adjacent to the aphid colony for attacking aphids. Female oviposition rate was higher on unmanipulated plants than on manipulated plants. No further significant treatment effects on patch residence time, the number of contacts, attacks or ovipositions were found. Oviposition success ofA. funebris was influenced by instar-specific host behaviour. Several rules-of-thumb proposed by foraging theory did not account for parasitoid patch-leaving behaviour.     

Superparasitism and host discrimination byEphedrus cerasicola [Hym.: Aphidiidae], an aphidiid parasitoid ofMyzus persicae [Hom.: Aphididae]

Myzus persicae (Sulzer) at different densities (1 to 120 aphids) on a paprika plant in a 1.8 dm³ cage were exposed at 21°C to single females of the parasitoidEphedrus cerasicola Stary. Three different exposure periods were used: 1 hr, 6 hrs, 24 hrs. The aphids were dissected 6 days after parasitization. Superparasitism was measured as number of hosts superparasitized and number of parasitoid larvae per aphid. It attained a maximum around host density=5 and decreased with increasing host density and decreasing exposure time. Almost no superparasitism occurred during the 1st hour. A non-random larval distribution indicated thatE. cerasicola discriminates between unparasitized and parasitized aphids, but probably not between aphids with different numbers of parasitoid eggs. Larvae in superparasitized aphids developed slower than single larvae. The supernumerary larvae died during the 1st instar, probably killed by chemical means since no physical attacks between larvae have been observed.     

Behaviour of Aphidius colemani Searching for Aphis gossypii: Functional Response and Reaction to Previously Searched Aphid Colonies

Understanding the searching strategy of Aphidius colemani Viereck (Hymenoptera: Braconidae), might gain insight into the mechanisms by which control of Aphis gossypii Glover (Homoptera: Aphididae) is obtained in glasshouses, and provide information on how to improve the biological control of aphids. The functional response of A. colemani in Petri dishes is described, as well as its behaviour on returning to a previously visited leaf disk with aphids. The number of aphids attacked during the first visit followed a sigmoid functional response. The increase of the parasitization rates was clearest at densities of up to 10 aphids/leaf disk. The duration of the first visit to a leaf disk increased with increasing aphid density. After re-entering a recently visited leaf disk, the parasitoid stayed for a much shorter time than on the first visit, and no effect of host density on the duration of the visit was observed. No evidence of patch marking was found, so the reduction of visiting times was probably caused by encounters with parasitized hosts.     

Plant virus and parasitoid interactions in a shared insect vector/host

Interactions between barley yellow dwarf luteovirus (BYDV) and the aphid parasitoid, Aphidius ervi Haliday (Hymenoptera: Aphidiidae), were investigated while sharing the vector/host, Sitobion avenae (F.) (Homoptera: Aphididae). Aphids, which were parasitized during their second larval stadium, had access to virus-infected plants before, immediately after, or several days after parasitoid attack. The larval development of A. ervi in S. avenae was significantly delayed when virus acquisition took place before or shortly after the parasitoid had hatched, but not when the parasitoid was at the second larval stage during virus acquisition. Similarly, the presence of BYDV led to a significantly higher aphid mortality when they acquired virus up to and including the time that A. ervi was at the first larval stage. Adult female parasitoids deposited fewer eggs in viruliferous aphids. Virus transmission was not reduced by parasitization, and in some experiments aphids which were subjected to parasitoid attack transmitted BYDV more efficiently than unattacked insects.