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.     

Decision to superparasitize based on larval survival: competition between aphid parasitoids Aphidius ervi and Aphidius smithi

Oviposition by a parasitoid wasp in an already parasitized host (= superparasitism) may result in larval competition and the loss of offspring. Consequently, in solitary species, the decision to superparasitize should be based on the probability of offspring survival. Females of Aphidius ervi Haliday and A. smithi Sharma & Subba Rao (Hymenoptera: Aphidiidae), two parasitoids of the pea aphid, discriminated between conspecific-and heterospecific-parasitized hosts. Both species showed partial preference for aphids previously attacked by A. smithi, a result predicted from the fact that A. ervi is superior to A. smithi in larval competition under most conditions. Females of A. smithi selectively attacked conspecific-parasitized pea aphids when given a choice between these and self-parasitized hosts. Results indicated that females of both species responded to an external pheromone-like marker to discriminate between selfconspecific-and heterospecific-parasitized aphids. In addition, A. smithi may use internal cues to recognize, and avoid oviposition in, aphids previously parasitized by A. ervi.

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Résumé L'oviposition par une guêpe parasite dans un hôte qui a déjà été parasité (= superparasitisme) pourrait conduire à une compétition entre larves et à une perte de progéniture. Par conséquent, dans les espèces solitaires, la décision de superparasiter devrait être basée sur la probabilité de survie de la progéniture. Les femelles de Aphidius ervi Haliday et de A. smithi Sharma & Subba Rao (Hymenoptera: Aphidiidae), deux parasites du puceron du pois, ont discriminé entre les hôtes parasités par des individus de la même espèce et ceux parasités par des individus d'une espèce différente. Les deux espèces de parasite ont montré une préférence partielle pour les pucerons préalablement parasités par A. smithi, résultat qui était prévisible du fait que, dans la majorité des cas, A. ervi est supérieur à A. smithi dans la compétition entre larves. Les femelles de A. smithi ont sélectivement attaqué les pucerons parasités par un individu de la même espèce lorsqu'il leur était donné de choisir parmi ceux-ci et ceux parasités par les même individu. Les résultats indiquaient que les femelles des deux espèces répondaient à une sorte de phéromone externe pour distinguer les pucerons parasités par le même individu de ceux parasités par un individu de la même espèce et ceux parasités d'une autre espèce. En plus, A. smithi pourrait utiliser des signaux internes pour reconnaître et éviter l'oviposition dans les pucerons préalablement parasités par A. ervi.

     

Instar-specific defense of the pea aphid,Acyrthosiphon pisum: Influence on oviposition success of the parasiteAphelinus asychis (Hymenoptera: Aphelmidae)

The parasite Aphelinus asychisWalker (Hymenoptera: Aphelinidae) oviposits in all four instars of the pea aphid, Acyrthosiphon pisum(Harris) (Homoptera: Aphididae). Searching females display a highly stereotyped sequence of behaviors when encountering a host. Once recognized, an aphid is examined and probed by the wasp with the everted ovipositor prior to oviposition. Oviposition success is influenced by aphid behavior that is related to aphid size and expressed through instarspecific escape and defense reactions. Being smaller and less able to defend themselves, first and early-second instars of pea aphid are more susceptible to successful parasitism than third and fourth instars, in that order. Observed patterns of preference by Aphelinus females for particular aphid species and instars reflect the outcome of behavioral interactions between the hosts and the parasites, rather than preference in the strict sense.     

Learning by the parasitoid wasp, Aphidius ervi (Hymenoptera: Braconidae), alters individual fixed preferences for pea aphid color morphs

Learning, defined as changes in behavior that occur due to past experience, has been well documented for nearly 20 species of hymenopterous parasitoids. Few studies, however, have explored the influence of learning on population-level patterns of host use by parasitoids in field populations. Our study explores learning in the parasitoid Aphidius ervi Haliday that attacks pea aphids, Acyrthosiphon pisum (Harris). We used a sequence of laboratory experiments to investigate whether there is a learned component in the selection of red or green aphid color morphs. We then used the results of these experiments to parameterize a model that examines whether learned behaviors can explain the changes in the rates of parasitism observed in field populations in South-central Wisconsin, USA. In the first of two experiments, we measured the sequence of host choice by A. ervi on pea aphid color morphs and analyzed this sequence for patterns in biased host selection. Parasitoids exhibited an inherent preference for green aphid morphs, but this preference was malleable; initial encounters with red aphids led to a greater chance of subsequent orientation towards red aphids than predicted by chance. In a second experiment, we found no evidence that parasitoids specialize on red or green morphs; for the same parasitoids tested in trials separated by 2 h, color preference in the first trial did not predict color preference in the second, as would be expected if they differed in fixed preferences or exhibited long-term (> 2 h) learning. Using data from the two experiments, we parameterized a population dynamics model and found that learning of the magnitude observed in our experiments leads to biased parasitism towards the most common color morph. This bias is sufficient to explain changes in the ratio of aphid color morphs observed in field sites over multiple years. Our study suggests that for even relatively simple organisms, learned behaviors may be important for explaining the population dynamics of their hosts.     

Oviposition and host-feeding patterns in Aphelinus asychis (Hymenoptera: Aphelinidae) at different aphid densities

Abstract. 1. The patterns of host-feeding and oviposition were examined in Aphelinus asychis Walker, which had been provided with second-instar pea aphids as hosts.
2. Female wasps responded to increasing host density (between one and forty aphids for 24 h) with an increasing tendency to oviposit rather than to feed. Superparasitism occurred at all aphid densities, even when unparasitized aphids were available.
3. Aphids intended for feeding were paralysed and died. Wasps did not feed on and oviposit in the same aphid.
4. Feeding to satiation lasted between 4 min and 42 min. Females that had starved for ≰18 h generally deposited one or more eggs before feeding again, while the reverse was true in wasps that had starved for 21 h.
5. The host-feeding behaviour of A. asychis is determined by a female's nutritional status. At low rates of host encounter, the anhydropic eggs may be resorbed. This reproductive strategy conforms to the destructive non-concurrent type among the Hymenoptera.     

The Effect of Abiotic Factors on the Male Mate Searching Behavior and the Mating Success of Aphidius ervi (Hymenoptera: Aphidiidae)

The effect of wind speed and distance from the source on the male response of the aphid parasitoid, Aphidius ervi (Hymenoptera: Aphidiidae), to a pheromone source was studied in a wind tunnel. The number of males taking flight, entering the plume and successfully reaching the source, decreased at wind speeds >50 cm/s. Furthermore, the proportion of those attempting upwind flight that fell to the ground increased with increasing wind speed. In contrast, distance from the source had no significant effect on any of the parameters examined. While male flight behavior was significantly reduced at 70 cm/s, some males walked to the source when there was a bridge connecting the pheromone source and the release platform. This suggests that ambulatory behavior could be a significant component of male mate searching in A. ervi when wind conditions are too strong for upwind flight. The possible effects of variation in atmospheric pressure on male flight behavior to the long distance pheromone, as well as to the short distance one, were also investigated. No significant effects of atmospheric pressure were observed. These findings differ significantly from those previously reported for another aphid parasitoid, A. nigripes, and the reasons for such differences are discussed.     

Effect of Adult Experience on in-Flight Orientation to Plant and Plant–Host Complex Volatiles inAphidius erviHaliday (Hymenoptera, Braconidae)

The effect of adult experience on in-flight orientation to plant–host complex volatiles byAphidius erviHaliday was studied in a wind tunnel bioassay, usingAcyrthosiphon pisum(Harris), maintained on broad bean plants (Vicia faba) as host. A short oviposition experience (15 s) on the plant–host complex (PHC) was sufficient to induce a drastic decrease of flight propensity and stimulated a foraging behavior characterized by intense walking activity. However, flight activity resumed to normal levels 1 h after the oviposition experience on the PHC occurred. For parasitoids conditioned on the PHC for at least 1 min the recorded proportion making oriented flights to the PHC was significantly higher than that for naive females. In contrast, oviposition experience in the absence of plant material did not influence theA. erviflight response. Oviposition attempts on aphid dummies without egg release did not reduce flight activity. WhenA. ervifemales were exposed to glass beads coated withAc. pisumcornicle secretion, a priming effect was observed, resulting, compared with naive females, in a significantly higher rate of oriented flights to the PHC. In contrast, oviposition attempts visually induced by colored aphid dummies did not influence flight behavior. A strong reaction to volatile cues from uninfested plants was induced by oviposition experience on newly infested broad bean plants. This appears to be a case of associative learning. In fact, uninfested broad bean plants are basically unattractive to naiveA. ervifemales. The results demonstrate that adult experience has a considerable influence onA. ervibehavior and may have important implications for biological control of natural pest aphid populations.     

Chemically mediated associative learning in the host foraging behavior of the aphid parasitoidAphidius ervi (Hymenoptera: Braconidae)

The effect of experience on the responsiveness of the braconid parasitoidAphidius ervi to host(Acyrthosiphon pisum)-associated cues was investigated on bean plants(Vicia faba) using a wind tunnel bioassay. Oviposition experience on the plant-host complex significantly increased the oriented flight and landing responses ofA. ervi females to an undamaged plant and to a plant-host(A. pisum) complex. However, oviposition experience onA. pisum aphids when isolated from the plant did not change their responses to the intact plant and the complex. Searching on an unwashed plant which had been previously damaged byA. pisum also increased their response to an undamaged plant and a host-damaged plant, whereas the experience of searching on an undamaged plant did not significantly change their responses to undamaged plants. However, when parasitoids were allowed to search on an undamaged plant which had been sprayed withA. pisum honeydew, this significantly increased their response to an undamaged plant. Oviposition experience on the plant-host complex and foraging experience on a host-damaged plant or an undamaged plant sprayed with honeydew also significantly reduced the mean time taken by the parasitoids to respond in the wind tunnel. The behavioral changes associated with such experience were acquired within 30 min and persisted for at least 3 days. The results demonstrate the capacity ofA. ervi to learn associatively olfactory cues from plants, host-damaged plants, and plant-host complexes and confirm the role of aphid honeydew as a host recognition kairomone forA. ervi.     

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.     

Behavioural differences between Aphidius ervi populations from two tritrophic systems are due to phenotypic plasticity

The Palaeoarctic parasitoid Aphidius ervi Haliday (Hymenoptera, Aphidiidae) parasitises legume aphids in its region of origin. In Chile, it parasitises both legume and cereal aphids. This special situation was studied at two levels: (i) the host searching behaviour of A. ervi from two different tritrophic systems (Acyrthosiphon pisum on alfalfa and Sitobion avenae on wheat) was investigated in dual choice tests in a wind tunnel between odours from both A. pisum-alfalfa host plant complex (HPC) and S. avenae-wheat HPC, and (ii) the genetic structure of A. ervi populations from both sources using molecular markers. Responses of A. ervi females to volatile olfactory cues emanating from A. pisum-alfalfa HPC and S. avenae-wheat HPC were significantly higher towards the HPC on which they were reared during the last generation before experimentation, regardless of the origin of the parasitoid. As previously described for this parasitoid species, oviposition experience was also of major relevance in the preferences of female parasitoids. On the other hand, variation in mitochondrial DNA segments and RAPD-PCR polymorphism using total DNA showed the absence of host-based population structure and a high genetic homogeneity between these A. ervi populations. These results reject the possible existence of different host-strains of this parasitoid in Chile.     

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

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

The temperature-dependent duration of development and parasitism of three cereal aphid parasitoids, Aphidius ervi, A. rhopalosiphi, and Praon volucre

Temperature dependencies were established for the egg-to-mummy and mummy-to-adult phases, for mummy mortality, and for parasitism of Aphidius ervi Haliday, Aphidius rhopalosiphi De Stefani-Perez, and Praon volucre (Haliday) (Hymenoptera, Aphidiidae), three parasitoids of Sitobion avenae (Fabricius) (Homoptera, Aphididae), at 8°C, 12°C, 16°C, 20°C, and 25°C on winter wheat (cv. Haven). A physiological model described temperature-dependent development over the full temperature range, whereas a linear model was fitted for data above 8°C and used to estimate the lower temperature thresholds and day-degrees (° D) required for development. The thresholds for A. ervi were 2.2°C for egg-mummy development and 6.6°C for mummy-adult development, those for A. rhopalosiphi were 4.5°C and 7.2°C, and those for P. volucre were 3.8°C and 5.5°C. The time to develop into mummies and adults differed significantly between the three species: A. ervi development into mummies required an average of 159 ° D, while development into adults took an average of 73 ° D. The corresponding average times required for A. rhopalosiphi and P. volucre to develop mummies were 124° D and 126° D, while their development into adults required an average of 70° D and 150° D, respectively. Mummy mortality was 25–35% at 8°C and less at the higher temperatures tested, but began to increase again at 25°C, showing a quadratic relationship between mortality and temperature. Parasitization was very low or, in the case of P. volucre, absent up to 12°C and thereafter increased with increasing temperature. The relationship between parasitization, recorded as percent aphids mummified, and temperature was linear at the temperatures tested and depended on species. A. ervisuperparasitized 11.1% aphids at 20°C and 16.6% aphids at 25°C, whereas superparasitism was low in A. rhopalosiphi and absent in P. volucre. From 16°C to 25°C the P. volucre sex ratio increased. For A. ervi and A. rhopalosiphi there was no trend with temperature, but at 20°C and 25°C it was close to even. Field data for 1996 and 1997 allowed for a comparison of actual and expected emergence of overwintering mummies. In both years, parasitoids were predicted to have emerged from overwintering mummies well in advance of the onset of aphid infestation, and more than a month earlier than the first parasitized aphids were found in winter wheat. Observations from trap plants in other crops supported the predictions of the models. Other factors that can affect biological control by cereal aphid parasitoids are discussed.     

A comparison between two strains from Japan and Europe of Aphidius ervi

A European strain of Aphidius ervishall be introduced into Japan for the control of Macrosiphum euphorbiaeon greenhouse tomatoes. We compared this strain, which is originating from The Netherlands (EVP), with a native strain from Hokkaido, Northern Japan (SPR) in several characteristics. The percentage of parasitism of SPR and EVP was significantly different, when attacking three aphid species: 13% and 30% on M. euphorbiaeon tomato, 68% and 93% on Acyrthosiphon pisumon broad bean and 10% and 42% on Aulacorthum solanion sweet pepper, respectively. SPR and EVP differed morphologically (in the colouration of the petiole) and in the esterase banding patterns. Furthermore, cross mating experiments showed that SPR and EVP are partially reproductively isolated from each other. Complete reproductive isolation is evident in the one direction cross (EVP females and SPR males).     

Plant structure and the foraging success of Aphidius rhopalosiphi (Hymenoptera: Aphidiidae)

Abstract. 1. A study of searching behaviour on wheat and host preference of Aphidius rhopalosiphi (DeStefani-Perez) is described.
2. Parasitoids divided their time equally between the leaves but spent very little time on the ear.
3. After contact with honeydew or an aphid host, parasitoids were arrested in a particular area and increased the time spent searching.
4. Aphids feeding on the ear were parasitized less successfully, since their position between the grains protected them from parasitoid attacks.
5. A.rhopalosiphi exhibited no preference for Metopolophium dirhodum (Walker) or Sitobion avenae (Fabricius), although the handling time for the latter was significantly longer; this resulted in fewer S.avenae being parasitized when it was abundant. Parasitoids did not switch between hosts in these experiments.
6. As a result of its searching behaviour, A.rhopalosiphi will encounter and parasitize M.dirhodum feeding on the leaves more frequently than S.avenae, which feeds on the ear. This will limit the parasitoid's ability to regulate populations of the cereal aphid S. avenae.     

Survival time and resistance to desiccation of diapause and non-diapause eggs of temperate Aedes (Stegomyia) mosquitoes

Time-related changes in the patterns of host discrimination may have a complex form depending on whether or not hosts are marked following first parasitisation, the persistence of chemicals in these marks, and changes in the host as a result of being parasitised. Here we present an experimental design capable of detecting temporal patterns in host discrimination of solitary parasitoids. This method is tested against experimental data from Aphidius ervi attacking the aphid, Acyrthosiphon kondoi. The results demonstrate that there are statistically significant changes in the patterns of egg distribution in aphid hosts held for intervals between 1 and 48 h between parasitisation. These changes appear to be attributable to increasing oviposition restraint by the superparasitising female as the time interval between attacks is increased. The form of this relationship is not significantly different to a sigmoid function and the rate of change of restraint was greatest between 6–8 h after the first oviposition.     

Evaluation of the establishment of Aphidius ervi Haliday (Hymenoptera: Braconidae) in lucerne aphid populations in New South Wales

The aphid parasitoid Aphidius ervi was released in the major lucerne-growing areas of New South Wales (NSW), Australia, between 1978 and 1981. With the collaboration of district agronomists of the New South Wales Department of Agriculture, five State-wide surveys were conducted in 1982–1983 to determine the success of the release program. In each survey, the distribution of the parasitoid was checked in relation to populations of the aphids Acyrthosiphon kondoi Shinji and Acyrthosiphon pisum (Harris) (Hemiptera: Aphididae). The surveys confirmed the successful dispersal and establishment of A. ervi in the major lucerne-growing areas of NSW. They demonstrated its ability to survive and recover rapidly after a severe and widespread drought.     

The phylogenetic relationships of introduced Aphelinus (Hymenoptera: Aphelinidae), biological control agents of the Russian wheat aphid (Homoptera: Aphididae)

Abstract  Several species of Aphelinus have been introduced to the US from the Old World for biological control of the Russian wheat aphid, Diuraphis noxia (Modvilko). Reproductive incompatibility has been observed among populations collected from different geographic areas. We examined whether or not the reproductive incompatibility between strains of A. asychis was caused by distant phylogenetic relationships. Ribosomal DNA sequences of internal transcribed spacers 2 (ITS2) were analyzed in several species of Aphelinus collected from multiple sites of Europe and Asia. The phylogenetic analysis showed that strains within the species A. albipodus and A. asychis are not monophyletic, and two clearly divergent clades were revealed among sequenced samples. Our results suggest that the reproductive incompatibility between three exotic strains of A. asychis was more likely caused by divergence of phylogeny than by symbiotic bacteria.     

Asymmetric size effect of sexes on reproductive fitness in an aphid parasitoid Aphidius ervi (Hymenoptera: Aphidiidae)

Most studies on size–fitness relationships focus on females and neglect males. Here, we investigated how body size of both sexes of an aphid parasitoid, Aphidius ervi Haliday, affected the reproductive fitness. Reproductive fitness was generally positively correlated with body size for both sexes in this species. Large individuals of both sexes had greater longevity, large males fathered more progeny, and large females had higher fecundity, parasitism, and greater ability in host searching and handling. We demonstrated in this study that size effects of males and females were asymmetric on different reproductive fitness parameters. With increasing body size females gained more than males in longevity and fecundity while males gained more than females in the number of female progeny. Regardless of female size, large males sustained a female-biased population longer than small males. These results suggest that male body size should also be considered in the quality control of mass-rearing programs and the evaluation of parasitoid population growth.     

Parasitism of aphid embryos by Aphidius smithi: some effects of extremely small host size

Embryos of the pea aphid, Acyrthosiphon pisum (Harris), were successfully parasitized by Aphidius smithi Sharma & Subba Rao while still inside their mother. Parasites from embryos were much smaller, laid fewer eggs, but survived as long as their counterparts that had developed in adult viviparous aphids. Lifetime fecundity was positively correlated with wasp size, as measured by dry weight at the time of death. A. smithi females produced the same offspring sex ratio at eclosion on both host classes, although emergence was significantly lower from mummified adult aphids than from embryos. The data are discussed with regard to progeny and sex allocation decisions by solitary hymenopterous parasites. It is suggested that, in A. smithi, the decision to lay a fertilized or unfertilized egg is influenced by the host's overall size, rather than by the size and quality of a smaller target area inside the host, such as embryos.