Feeding and egg distribution studies of Heringia calcarata (Diptera: Syrphidae), a specialized predator of woolly apple aphid (Homoptera: Eriosomatidae) in Virginia apple orchards

Predation by the aphidophagous syrphid fly Heringia calcarata (Loew) on woolly apple aphid, Eriosoma lanigerum (Hausmann), was studied in the laboratory and in Virginia apple orchards. Feeding studies compared the prey suitability of three temporally sympatric aphid pests of apple: spirea aphid, Aphis spiraecola Patch; rosy apple aphid, Dysaphis plantaginea (Passerini); and woolly apple aphid. Significantly more H. calcarata larvae survived and completed development on a pure diet of woolly apple aphid than on rosy apple aphid, and none survived on spirea aphid. Final larval weights were significantly greater, and the larval developmental period was significantly shorter on woolly apple aphid than on rosy apple aphid, but neither the duration of pupal development nor adult weight differed between diets. H. calcarata larvae consumed an average of 105 woolly apple aphids during their development. Na?ve, neonate larvae given access to all possible pair combinations of woolly apple aphid, rosy apple aphid, and spirea aphid consumed significantly more woolly apple aphids in all pairings that included woolly apple aphid. When given a choice of rosy apple aphid and spirea aphid, significantly more rosy apple aphids were consumed. Weekly counts of syrphid eggs found in woolly apple aphid, rosy apple aphid, and spirea aphid colonies collected from apple trees showed that two generalist hover fly predators, Eupeodes americanus (Wiedemann) and Syrphus rectus Osten Sacken, were present in colonies of all three aphid species and that E. americanus was the most abundant syrphid predator in A. spiraecola and D. plantaginea colonies. H. calcarata eggs were found only in woolly apple aphid colonies and were more abundant there than E. americanus and S. rectus. These data suggest that H. calcarata is a specialized predator of woolly apple aphid in the apple ecosystem in Virginia.     

Intraguild predation of the aphid parasitoid Aphelinus certus by Coccinella septempunctata and Harmonia axyridis

Coincidental intraguild predation is expected to be less disruptive to biological control than omnivorous intraguild predation, and strong intraguild predation is not expected to occur in natural systems. Coincidental intraguild predation in a foodweb involving introduced pest and natural enemy species was examined to determine whether intraguild predation would be disruptive of biological control services in soybean agroecosystems. Introduced natural enemies are important regulators of soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), populations in North America. Seven-spotted lady beetles, Coccinella septempunctata L., and multicolored Asian lady beetles, Harmonia axyridis Pallas (Coleoptera: Coccinellidae), are key predators of soybean aphid in North America while the chalcidoid wasp, Aphelinus certus Yasnosh (Hymenoptera: Aphelinidae), is the most common parasitoid of soybean aphid in Ontario, Canada. Predation of parasitized soybean aphids at two stages (newly parasitized aphids and mummified aphids) by adults and third instar larvae of both C. septempunctata and H. axyridis was examined in laboratory experiments. In choice experiments, all stages of lady beetles preferred non-parasitized aphids over mummified aphids. In cage experiments, third instar larvae and male and female adults of both lady beetles did not discriminate between newly parasitized and non-parasitized aphids. The influence of coincidental intraguild predation on the efficacy of parasitoids as biological control agents, and implications for soybean aphid management decisions based on natural enemies, are discussed.     

Effects of the parasitization of a braconid, Apanteles, on the blood of its host, Pieris

Parasitization of a braconid wasp, Apanteles glomeratus, of larvae of a common cabbage butterfly, Pieris rapae crucivora, caused changes in differential haemocyte count (DHC), total haemocyte count (THC), and encapsulative capacity against dead eggs of Apanteles in the fourth and fifth instar host larvae.However, no correlation could be found between the number of Apanteles eggs deposited and THC of the middle fourth instar host larvae or between the number of parasitoid larvae and specific gravity of the haemolymph from the late fifth instar host larvae.From the changes in DHC and in THC of both non-parasitized and parasitized Pieris larvae, an increase in the number of plasmatocytes of non-parasitized Pieris larvae in the early fourth instar period was supposed to be due to transformation of prohaemocytes into plasmatocytes, and a low population of plasmatocytes of parasitized larvae in the comparable period was assumed to be due to a suppression of transformation of prohaemocytes by some factor released from the parasitoid eggs.Failure of the parasitized fourth instar Pieris larvae to encapsulate injected dead eggs of Apanteles indicated that the parasitoid embryos were, in some way, actively inhibiting the encapsulation reactions of the host.The increase in THC of the parasitized fifth instar larvae could not be ascribed to a decrease in the volume of host haemolymph. Rather it could be interpreted by a suppression of adhesive capacity of haemocytes in the host haemocoel to tissue surfaces.Reduced encapsulative capacity of the parasitized fifth instar larvae might be attributed either to a depression of the adhesive activity of plasmatocytes resulting from a depletion of energy source for haemocytes in the host haemolymph by parasitization, or from an active suppression of adhesiveness of the plasmatocytes by secretions from ‘giant cells’ (teratocytes) originated from the parasitoid.     

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.     

Queen-worker conflict and social parasitism in bumble bees (Hymenoptera: Apidae)

Psithyrus ashtoni (Hymenoptera: Apidae) is an obligate, workerless bumble, bee social parasite which invades nests of Bombus affinis. Although parasites are limited by host worker defence to invading very small colonies, there is considerable flexibility in the way parasites control host brood bionomics once they are accepted inside the nest. A study of 46 parasitized and 22 non-parasitized laboratory colonies of B. affinis showed that P. ashtoni females cohabited with host queens and workers while the worker force increased, but not to the maximum normally achieved in non-parasitized nests. While colony reproductive success was correlated with the number of workers reared, parasites risked being killed or ejected from the comb by workers, after the queen had lost dominance. Host bees usually succeeded in rearing offspring, and Psithyrus reproductive success was related to the ability of parasites to control proportional investment in the two species. In addition to displacing P. ashtoni females, host bees ate the eggs of parasites and ejected their larvae. These behaviours were also exhibited by workers in the later stages of development of non-parasitized colonies. These results indicate that social parasites are at least partially subject to the conflict of genetic self-interest between the queen and her workers which is believed to influence the control of reproductive investment in haplodiploid Bombus societies.     

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

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

Morphological observations on the preimaginal stages ofAphelinus varipes (Hym., Aphelinidae) and the effects of this parasitoid on the aphidRhopalosiphum padi (Hom., Aphididae)

Three instar larvae could be observed forAphelinus varipes. In the second and third instars, the colon which forms the largest part of the hindgut was composed of secretory cells. There was a reduction in the size and number of embryos produced by parasitized aphids. Fat cells of parasitized aphids also degenerated sooner than those of unparasitized aphids. The number of mycetocytes remained higher in parasitizedRhopalosiphum padi than in non-parasitized aphids. During the last instar ofA. varipes the host aphid developed into a mummy in which black pigments were incorporated into the exocuticle and the integument of the aphid became sclerotized.     

Effects of mummy consumption on fitness and oviposition site selection on Harmonia axyridis

Intraguild predation (IGP) has been commonly reported between predators and parasitoids used as biological control agents as predators consuming parasitoids within their hosts. However, the effect of parasitoid–mummy consumption on the fitness of the predator and subsequent oviposition site selection have not been well studied. In our study, we conducted two laboratory experiments to examine the influence of Aphidius gifuensis Ashmead (Hymenoptera: Braconidae) mummies as prey on fitness and subsequently oviposition site selection of Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). Results indicate that when H. axyridis was reared on A. gifuensis mummies only, its larval development was prolonged, and body weight of the 4th instar larvae and newly emerged adults, and fecundity decreased. Moreover, H. axyridis did not exhibit oviposition preference on plants infested with unparasitized aphids or aphids parasitized for shorter than 9 days. However, compared with plants with mummies (parasitized ≥9 days), H. axyridis laid more eggs on plants with unparasitized aphids. In contrast, H. axyridis previously fed with A. gifuensis mummies did not show a significant oviposition preference between plants with unparasitized aphids and those with mummies (parasitized ≥9 days). Overall, our results suggest that mummy consumption reduced the fitness of H. axyridis. Although H. axyridis avoided laying eggs on plants with A. gifuensis mummies, prior feeding experience on A. gifuensis mummies could alter the oviposition site preference. Thus, in biological control practice, prior feeding experience of H. axyridis should be carefully considered for reduction of IGP and increase of fitness of H. axyridis on A. gifuensis.     

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.     

Effect of parasitism by Cardiochiles nigriceps on food consumption and utilization by Heliothis virescens

Parasitism of Heliothis virescens larvae by the endoparasitoid Cardiochiles nigriceps resulted in a reduction in the amount of food consumed by parasitized larvae. This effect was attributed in part to inoculation of material from the accessory reproductive glands of the female at the time of oviposition. Injection of solutions of either the calyx fluid or the poison gland (0·04 gl/larva) into non-parasitized larvae resulted in a reduction in the amount of food consumed by these larvae. A 1 : 1 mixture of these glands (total of 0·04 gl/larva) appeared to be more active than either of the two glands alone. Both of these glands were essential for total activity since larvae parasitized by females lacking the poison gland (poi gl^? female) continued to eat and consumed more food than did those parasitized by a normal female.Parasitism resulted in a slower rate of crop-emptying. This effect was, however, shown to be a result of the quantity of food consumed. Inhibition of gut movement was therefore not considered the cause for the reduction in the amount of food consumed by parasitized larvae.The effect of parasitism on the ability of H. virescens larvae to utilize ingested food was partially reduced by parasitism. Larvae parasitized by a normal female were less efficient than non-parasitized larvae in digesting food. Those larvae parasitized by a poi gl^? female did not convert as much of their food to body substance as did non-parasitized larvae. Injection of solutions of accessory glands into non-parasitized larvae did not cause these effects.     

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.     

Social wasp parasites affect the nestmate recognition abilities of their hosts (<Emphasis Type="Italic">Polistes atrimandibularis</Emphasis> and <Emphasis Type="Italic">P. biglumis</Emphasis>, Hymenoptera,Vespidae)

Summary. Queens of the parasitic social wasp, Polistes atrimandibularis, temporarily mimic the odor of their host species, Polistes biglumis, but their offspring have parasite-specific odors. As a consequence, in parasitized colonies individuals with different odors co-inhabit the colony and host workers, who are responsible for colony defense, accept wasps with different odors. In order to verify whether this particular condition causes a change in recognition abilities of hosts, we tested nestmate/non-nestmate discrimination in field colonies invaded by social parasites (and in non-parasitized colonies as controls). Results show that parasitized colonies distinguish between nestmates and non-nestmates, distinguish their parasite queen from those that usurped alien colonies, and accept their parasite's non-mimetic offspring but make more recognition errors than non-parasitized colonies. The optimal acceptance threshold model predicts that when the frequency of encountering non-kin increases, residents become less permissive towards intruders. However, my data show that parasitized colonies are more permissive towards non-nestmates with respect to non-parasitized colonies but they are also more aggressive towards nestmates, suggesting that host workers' learning abilities are impaired.     

Effects of a parasitic nematode on male mate choice in a livebearing fish with a coercive mating system (western mosquitofish, Gambusia affinis)

I examined the effects of the parasitic larval nematode, Eustrongylides ignotus, on male mate choice in the western mosquitofish, Gambusia affinis. I hypothesized that parasite presence influences male mate choice either directly (via reduction in male mating behavior due to presence of parasite in females) or indirectly (via reduction in male mating behavior due to reduced condition of infected females). Specifically, I tested the predictions that (1) males would mate preferentially with uninfected over infected females (scoring both mating attempts and association time with females); (2) parasitized females would be in poorer condition than non-parasitized females (measured as soluble fat stores); and (3) parasitized females would have reduced fecundity (measured as number of developing embryos). Males preferred to mate with non-parasitized over parasitized females, but showed no differences in association time between females. The nematode did not decrease female body condition, but did decrease female mass, and appeared to decrease female fecundity via reduction in broods (# embryos). Results support that parasites affect male mate choice in mosquitofish; however, the mechanisms used by males to differentiate between parasitized and non-parasitized females remain untested. This study provides the first empirical evidence of parasite affects on male mate choice in livebearing fishes, and suggest a potentially important role for parasite-mediated sexual selection in organisms that use coercive mating as the primary mechanism of obtaining mates.     

Predation on Mindarus abietinus infestingbalsam fir grown as Christmas trees: the impact ofcoccinellid larval predation with emphasis on Anatis mali

The impact of natural coccinellid larvalpredation on the balsam twig aphid was evaluated bysystematically removing coccinellid egg masses in a6–8 year-old balsam fir (Abies balsamea)Christmas tree plantation in southwesternQuebec. Among coccinellid species hunting on firfoliage during development of Mindarus abietinusfundatrices in May, the indigenous Anatis mali was by far the most abundant and themain one to oviposit on trees. Comparison of trees onwhich coccinellid larval predation was excluded withcontrol trees showed that A. mali had a markedimpact both during and after the phase of rapid M. abietinus population growth that followedfundatrix maturation. On trees where coccinellidlarvae were allowed, aphid colonies became inactive(i.e. no live aphids in the colony) about two weeksearlier than on controls. A strong dampening effect onaphid density was also observed in those colonies thatremained active until the end of the aphid life cycle.Predation on aphid colonies reduced sexualsproduction, as the density of M. abietinusoverwintering eggs per shoot subsequently was reducedby 32%. Predation by coccinellid larvae occurred toolate to prevent needle damage to current year shoots,which affects the aesthetic value of Christmas trees.However, current year shoots measured in the mid-crownof trees late in the season were 19% longer on treeswhere aphid predation by coccinellid larvae wasallowed, compared with trees where they were excluded.Rearing all larval stages of A. mali on 4thinstar and adult sexuparae of M. abietinusindicated an average consumption of 269 aphids tocomplete larval development and pupate, which wasequivalent to at least seven colonies of M.abietinus at maximum aphid density at theexperimental site. Anatis mali is an importantnatural control factor of balsam twig aphid inChristmas tree plantations, hence its activity shouldbe protected and possibly stimulated by favourablepest management practices.     

Antipredator response of pea aphids <Emphasis Type="Italic">Acyrthosiphon pisum</Emphasis> (Hemiptera: Aphididae): effects of predation risks from an alternative patch on a current patch

To escape from predators, herbivorous prey could leave their current patch and relocate to an alternative patch. However, when other predators are present on the new patch, prey are again exposed to predation risk. Thus, patch leaving might be affected by the other predators. We studied patch leaving of pea aphids Acyrthosiphon pisum Harris (Hemiptera: Aphididae) in response to ladybird larvae Harmonia axyridis Pallas (Coleoptera: Coccinellidae) on broad bean Vicia faba L. shoots that were offered as patches for aphids. We tested whether shoot leaving was affected by the presence of predators on alternative shoots under laboratory conditions. Odors from alternative shoots were evaluated as possible cues used by aphids to assess predation risk on the shoots. We exposed aphids to odors from alternative shoots with conspecifics plus either adult or larval ladybirds or larval green lacewings Mallada desjardinsi Navas (Neuroptera: Chrysopidae). Shoot leaving was reduced only when adult ladybirds were present on the alternative shoots compared with controls (i.e., no predators on the alternative shoots). Odors of both adult ladybirds and of conspecifics being attacked by ladybird larvae were required for reduced leaving. Hence, predation risks on current and alternative patches might affect the antipredator responses of aphids.     

Inhibition of Host Queen Reproductive Capacity by the Obligate Social Parasite Polistes atrimandibularis (Hymenoptera,Vespidae)

Polistes atrimandibularis is the obligate and permanent parasite of the social paper wasp Polistes biglumis bimaculatus. This parasite lives together with the host foundress for a considerable period on the invaded nest. Ovarian development was measured in females of the host species (foundresses and, when present, workers) from 18 parasitized and 14 non-parasitized colonies. The reproductive capacity of foundresses from parasitized nests decreased faster than that of foundresses from non-parasitized nests. These results indicate that the presence of the parasite lowers reproductive capacity of the host queen. Simultaneously, the fertility of the host worker is inhibited.     

The performance of an aphid parasitoid is negatively affected by the presence of a circulative plant virus

Plant viruses and aphids can interact via contest competition for plant resources and induce changes in plant physiology, which can have effects on a third trophic level. The aim of this study was to determine how the interactions between a circulative plant virus and its aphid vector may affect the performance of an endoparasitoid and how parasitism may affect the efficiency of virus transmission by its aphid vector. The timing when parasitized aphids were transferred to virus-infected lettuce leaves was critical for the performance of A. ervi. Higher parasitoid larvae mortality, longer developmental times and lower percentages of mummification were detected on viruliferous/parasitized aphid nymphs when the time lag between parasitism and exposure to the virus was less than 24 h. No significant differences were detected in virus transmission rate between parasitized and non-parasitized M. euphorbiae aphids.     

Developmental rates of two congeneric parasitoids,Encarsia formosa and E. pergandiella (Hymenoptera: Aphelinidae), utilizing different egg provisioning strategies

Endoparasitic Hymenoptera vary in the extent to which they provision their eggs and thus in the degree to which they appear to rely on their hosts for resources during embryonic development. In this study, developmental rates were examined in two congeneric parasitoid species, Encarsia formosa and E. pergandiella, that provision their eggs to different degrees. E. formosa eggs are much larger than E. pergandiella eggs. E. formosa eggs hatch significantly earlier than the eggs of E. pergandiella when deposited in 1st or 4th instar nymphs of a common whitefly host, Bemisia tabaci. Both species hatch earlier in 4th instar nymphs, but the delay in hatching in hosts parasitized as 1st instars is much greater in E. pergandiella. While E. formosa develops more rapidly to the 1st larval instar, E. pergandiella emerge as adults significantly earlier, though smaller, than E. formosa adults regardless of the host instar parasitized. These findings show that the extent of provisioning in the eggs of these wasps does not strictly determine their order of progression through different stages of development.     

Role of aphid predator guild in controlling spirea aphid populations on apple in West Virginia,USA

Spirea aphid populations and their predators were studied on apple to identify predators of importance in controlling aphid populations. Methods included random and non-random sampling from apple orchards in West Virginia, USA, sentinel aphid colonies, laboratory feeding studies, and predator exclusion studies. Aphidoletes aphidimyza (Diptera: Cecidomyiidae), chrysopids (Neuroptera: Chrysopidae), Harmonia axyridis (Coleoptera: Coccinellidae), and Orius insidiosus (Hemiptera: Anthocoridae) were the most abundant predators associated with spirea aphid colonies on apple. Parasitoids were all but absent in the study. Abundance of all predators was density dependent with greater responses to aphid populations at the orchard scale than to tree or individual colony scales. A. aphidimyza, O. insidiosus, chrysopids, and syrphids (Diptera) had the greatest degree of density dependence on aphid populations, and spiders showed inverse density dependence. Exclusion of predators with both cages and insecticides produced significantly higher aphid populations. Because of high abundance, good synchrony with aphid populations, and high impact per individual, H. axyridis adults were the most important spirea aphid predator on apple.