Hymenopteran parasitoids and dipteran predators of the invasive aphid Diuraphis noxia after enemy introductions: Temporal variation and implication for future aphid invasions

Shifts in prevalence and abundance of hymenopteran parasitoids and dipteran predators, Diuraphis noxia, and other aphids were measured in the west-central Great Plains of North America, April–September, in 2001 and 2002, corresponding to over a decade after first detection of D. noxia and first release of D. noxia enemies. Significant temporal shifts in enemy species prevalence and diversity were detected in this study and more broadly during an 11 year time span. At any given time, some species were relatively common. One parasitoid had been predominant throughout (Aphelinus albipodus), two had shifted in dominance (Lysiphlebus testaceipes and Diaeretiella rapae), three parasitoids had been detected infrequently (Aphidius avenaphis, Aphidius matricariae, and Aphelinus asychis), one parasitoid was detected in the 1990s but not during 2001 and 2002 (Aphelinus varipes), two predatory flies occurred at occasional significant levels (Leucopis gaimarii and Eupeodes volucris), and two parasitoids may have been minor members of the fauna (Aphidius ervi and Praon yakimanum). Aphid populations detected were usually very low or not detected, precluding estimation of percent parasitism. The best evidence of suppression was observations of parasitoids in the rare case of D. noxia exceeding economic thresholds, which complemented past studies using high aphid densities. The D. noxia enemies detected were primarily endemic or long-time residents derived from previous introductions. This enemy community may provide flexibility in responding to a future aphid invasion, allowing more strategic use of biological control and other pest management approaches.     

Survey of the parasitoids of the tuliptree aphid,Illinoia liriodendri (Hom: Aphididae), in northern California

A survey of the parasitoids ofIllinoia liriodendri (Monell) in northern California conducted from 1988–1990 revealed the presence of 12 primary and 14 hyper-parasitoid species. The most common primary parasitoid wasAphidius polygonaphis (Fitch), which was imported from the eastern United States in the 1970's and is now established throughout the area. New host records were noted forA. ervi Haliday,A. avenaphis (Fitch), Praon occidentale Baker,P. unicum Smith,Diaeretiella rapae M'Intosh,Lysiphlebus testaceipes (Cresson), andMonoctonus nervosus (Haliday) (all Hymenoptera: Braconidae: Aphidiinae), andAphelinus sp. nr.asychis Walker (Hymenoptera: Aphelinidae). The most common hyperparasitoid species werePachyneuron aphidis (Bouché) andAsaphes californicus Girault (both Hymenoptera: Pteromalidae). New hyperparasitoid host records were noted forPachyneuron californicum Girault on Aphidiine and Aphelinidae spp. andCoruna clavata Walker (Hymenoptera: Pteromalidae) onAphelinus sp.     

Interspecific host discrimination and intrinsic competition between Aphelinus asychis and Aphidius gifuensis in Myzus persicae

Aphelinus asychis Walker (Hymenoptera: Aphelinidae) and Aphidius gifuensis Ashmead (Hymenoptera: Braconidae: Aphidiinae) are solitary kionobiont endoparasitoids, which can parasitize the green peach aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae). We determined the influence of oviposition sequence and various time intervals (0, 24, 48, and 72 h) between two ovipositions on self‐ and conspecific discrimination and interspecific intrinsic competition between A. asychis and A. gifuensis. When offered unparasitized M. persicae and those parasitized by the other parasitoid species, the two parasitoid species oviposited more often in unparasitized hosts. Aphelinus asychis and A. gifuensis could, however, not avoid to multiparasitize hosts parasitized by the other species. Both parasitoid species had a limited interspecific discrimination ability through ovipositor insertion to detect internal cues. Aphidius gifuensis most often out‐competed A. asychis. The outcome of this interspecific competition was not influenced by oviposition sequence or time intervals between two ovipositions. Aphidius gifuensis eliminated competitors by physical combat at the first instar and probably by physiological suppression in later stages; A. asychis possibly used physiological suppression in all larval stages.     

Supercooling capacity of Eurasian and North American populations of parasitoids of the Russian wheat aphid, >Diuraphis noxia

Supercooling points were estimated for seven populations of >Aphelinus albipodus, five populations of >Aphelinus asychis, and four populations of >Diaeretiella rapae to assess whether their supercooling points were sufficiently low to provide the potential for overwintering survival in colder temperate climatic areas. Test individuals from all 16 of the parasitoid populations were collected originally from mummies of the Russian wheat aphid, >Diuraphis noxia. Mummies containing parasitoid pupae were maintained for 1 wk under three different temperature conditions (treatments): at room temperature (24.8 ± 0.2 °C), 1 wk at 0 °C, and 1 wk –5 °C, and the supercooling points across treatments, and within and among species were compared. Statistical differences in supercooling points were found among populations of >A. albipodus for each treatment, and for >A. asychis when maintained for 1 wk at room temperature. No differences in supercooling points were found among populations of >D. rapae mummies maintained under the three temperature treatments. The lowest supercooling points obtained for the three parasitoid species maintained at room temperature were the >A. albipodus population from Montana (–31.68 °C), the >A. asychis population from Greece (–32.04 °C), and the >D. rapaepopulation from the Caucasus (–33.12 °C). Preconditioning the parasitoid mummies to cold had no effect on the supercooling points for >A. albipodus, and in some cases unexpectedly increased the supercooling points for >A. asychisand >D. rapae. In comparing the overall mean supercooling points of the three parasitoid species, no differences were found within species (among temperature treatments), nor among species (within temperature treatments). It was concluded that observed differences in supercooling points of only a few degrees Centigrade among parasitoid populations and species would not be expected to cause differences in their overwintering success, especially given the expected variability in temperatures within and among overwintering sites.     

Species diversity, abundance, and phenology of aphid natural enemies on spring wheats resistant and susceptible to Russian wheat aphid

The species composition, relativeabundance, and seasonal dynamics of selectednatural enemies of cereal aphids were monitoredin spring wheat fields in Moscow, Idaho in 1997and 1998. Trials also examined the potentialimpact of resistance to Russian wheat aphid(RWA), Diuraphis noxia (Mordvilko)(Homoptera: Aphididae) in wheat, on aphidbiological control agents. Natural enemypopulations were monitored on two springwheats: D. noxia susceptible variety`Centennial' and resistant genotype `IDO488'. Field plots were artificially infested withadult D. noxia, and sampled for cerealaphids and parasitoids weekly. Coccinellidpredators were monitored once in 1997 and twicein 1998. The coccinellids Hippodamiaconvergens Guerin, Coccinellaseptempunctata L., C. transversoguttataBrown and C. trifasciata Mulsant weredetected. No significant differences in adultor immature coccinellid densities were observedbetween the D. noxia resistant andsusceptible genotypes. During both years, themost abundant primary hymenopteran parasitoidswere Diaeretiella rapae (M'Intosh), Aphidius ervi Haliday, A. avenaphis(Fitch), and Lysiphlebus testaceipes(Cresson), Aphelinus varipes (Foerster),Aphidius colemani Viereck, Aphidiuspicipes (Nees), Aphidius sp., Monoctonus washingtonensis Pike & Stary, Praon gallicum Stary, Praon occidentaleBaker, and Praon sp. were also detected. Numbers of both D. noxia and D.rapae were significantly greater on Centennialthan on IDO488 in both years. When all speciesof cereal aphids and parasitoids areconsidered, the total percentage parasitism wasnot significantly different between thegenotypes. There was no interaction betweenD. noxia resistance and the populationdensity of the predators or parasitoidsmonitored. These results suggest that the D. noxia resistant line had no adverse impacton natural enemies under the conditions ofthese field experiments.     

Recognition of heterospecific parasitism: Competition between Aphidiid (Aphidius ervi) and Aphelinid (Aphelinus asychis) parasitoids of Aphids (Hymenoptera: Aphidiidae; Aphelinidae)

The solitary parasitoids Aphidius erviHaliday (Hymenoptera: Aphidiidae) and Aphelinus asychisWalker (Hymenoptera: Aphelinidae) attacked but generally did not oviposit in pea aphids parasitized by the other species. Wasps selectively oviposited in unparasitized hosts when given a choice. Host discrimination depended on the recognition of internal cues. Females of A. asychiseither could not recognize or ignored A. ervi'sexternal host marking pheromone. Under most conditions, A. ervisurvived in superparasitized hosts, killing competing A. asychislarvae by physical attack and possibly physiological suppression. The outcome of larval competition was not affected by oviposition sequence or age difference between larvae; A. asychissurvived only when it had substantially completed larval development before the host was superparasitized by A. ervi.It is suggested that competition for host resources incurs a cost, for the winner in terms of reduced size or increased development time and for the loser in terms of lost progeny and searching time. Consequently, heterospecific host discrimination can be functional. Internal, and probably general, cues enable wasps to recognize and avoid oviposition in hosts already parasitized by an unrelated species.     

Oviposition behaviour and patch-time allocation in two aphid parasitoids exposed to deltamethrin residues

Neurotoxic insecticides are widely used for crop protection. One consequence is that changes in behaviour can be expected in surviving beneficial insects because of an impairment of host perception and motor abilities. Under laboratory conditions, we studied the impact of deltamethrin, a pyrethroid, on the oviposition behaviour of two hymenopterous parasitoids of aphids, Aphidius matricariae (Haliday) and Diaeretiella rapae (McIntosh) (Hymenoptera: Braconidae). They both parasitize Myzus persicae (Sulzer) (Homoptera: Aphididae), which is the preferred host of A. matricariae, regardless of the host plant, whereas D. rapae is a major parasitoid of aphids on Cruciferae crops, including M. persicae. After exposure to deltamethrin, the different items of oviposition behaviour and the total time spent on the patch were recorded. The results showed that the patch time allocation by both parasitoid species was not significantly affected by deltamethrin treatment, when compared with the controls. Nor were the frequencies and sequences of behavioural items modified (e.g., frequency of sting). It therefore appeared that the patch use of A. matricariae and D. rapae on new colonies of M. persicae was not disturbed by deltamethrin at the three doses tested. The possibility that parasitoid strains are partially tolerant to deltamethrin is discussed.     

Parasitoid spectrum (Hymenoptera: Braconidae; Aphelinidae) of the soybean aphid Aphis glycines (Homoptera: Aphididae) in Japan and Indonesia (Java and Bali)

Aphidiine and aphelinid parasitoids collected from the soybean aphid, Aphis glycines, on Glycine max in Japan and Indonesia (Java and Bali) were identified to clarify the parasitoid spectrum of the aphid there. Nine parasitoid species from Japan (Aphidiinae: Aphidius gifuensis, Aphidius sp., Binodoxys communis, Diaeretiella rapae, Lipolexis gracilis, Lysiphlebia japonica; Aphelinidae: Aphelinus asychis, A. gossypii, A. varipes) and two parasitoid species from Indonesia (B. communis, A. gossypii) were found to be associated with A. glycines.     

Native primary parasitoids and hyperparasitoids attacking an invasive aphid Uroleucon nigrotuberculatum in Japan

Since the invasion of Uroleucon nigrotuberculatum from North America we searched for parasitoids of this aphid on Solidago altissima in Japan to determine what species of native parasitoids attack the newly invasive aphid. We found three primary parasitoid species: Ephedrus plagiator and Praon yomenae (Braconidae, Aphidiinae) and Aphelinus albipodus (Aphelinidae). We also found eight hyperparasitoid species: Syrphophagus sp. (Encyrtidae), Dendrocerus carpenteri (Megaspilidae), Asaphes suspensus (Pteromalidae) and Pachyneuron aphidis (Pteromalidae) through both E. plagiator and A. albipodus; Phaenoglyphis villosa (Figitidae, Charipinae), Aprostocetus sp. (Eulophidae, Tetrastichinae) and D. laticeps through E. plagiator, and Alloxysta sp. nr brevis (Figitidae, Charipinae) through A. albipodus. Uroleucon nigrotuberculatum is usually attacked by rather polyphagous primary parasitoids, E. plagiator and A. albipodus, in Japan, where an oligophagous parasitoid specialized to allied aphid species is probably absent. The hyperparasitoid community of U. nigrotuberculatum is common to those of the aphids occurring in open field‐type habitats in Japan.     

Release and recovery in South Africa of the exotic aphid parasitoid <Emphasis Type="Italic">Aphelinus hordei</Emphasis> verified by the polymerase chain reaction

The exotic aphid parasitoid Aphelinushordei Kurdjumov (Hymenoptera: Aphelinidae) was released at five Russian wheat aphid [Diuraphis noxia (Mordvilko)] infested wheat fields in the eastern parts of the Free State Province of South Africa during the 1998 and 1999 growing seasons. Except for differences in the setae on the ventralside of the forewings, this species is verysimilar in colour and structure to A.varipes (Foerster) and A. albipodusHayat & Fatima, which also parasitise D.noxia. It is therefore difficult todistinguish between them, and to determinetheir establishment. Therefore a polymerasechain reaction, using specific primers for bothITS2 and mitochondrial 16s DNA sequencesof the three parasitoids, followed by HinfIrestriction endonuclease digestion and agarosegel electrophoresis, was tested to distinguishbetween them. Parasitoid recoveries were madeat the release sites within weeks after theywere released. Putative individuals of A.hordei were also collected during 1999 and2000 on D. noxia in Lesotho, whichis situated on the eastern border of the FreeState Province. The procedure separated the three Aphelinus spp.reliably. Between 94 and 100% of theindividuals recovered during the two fieldseasons were identified as being A.hordei, thus verifying recovery of this exoticaphid parasitoid in South Africa.     

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.     

麦双尾蚜及其天敌在春小麦和野生寄主上的种群动态

在塔城麦田调查发现,麦双尾蚜Diuraphis noxia (Mordvilko) 在春小麦和野生寄主上的百株蚜量从大到小依次为春小麦、黑麦和野燕麦,在春小麦上最早出现高峰期。在春小麦上,瓢虫类数量最多达到516头/百株,菜蚜茧蜂Diaeretiella rapae和白足蚜小蜂Aphelinus albipodus的最高寄生率分别达到31.6%和12.9%。在黑麦上,麦双尾蚜主要被白足蚜小蜂寄生,最高寄生率达到42.9%,斑腹蝇幼虫Leucopis annulipes最高达到16头/百株。在野燕麦上,白足蚜小蜂和菜蚜茧蜂最高寄生率分别达到62.3%和31.8%。瓢虫和菜蚜茧蜂发生较早,白足蚜小蜂和斑腹蝇发生时间相对较晚。     

Host stage preference, functional response and mutual interference of Aphidius matricariae (Hym.: Braconidae: Aphidiinae) on Aphis fabae (Hom.: Aphididae)

Host stage preference, functional response and mutual interference of Aphidius matricariae (Haliday) (Hym.: Braconidae: Aphidiinae), parasitoid of the black bean aphid, Aphis fabae Scopoli (Hom.: Aphididae) were investigated in a growth chamber at a temperature of 25°C, 65% relative humidity and a photoperiod of 16 h light : 8 h dark on the PP8 variety of sugar beet. Nicholson's model and linear regression were used to determine per capita searching efficiency and interference coefficient, respectively. The highest parasitism percentage was observed on the third instar nymphs of A. fabae in both choice and no‐choice preference tests. There was significant difference between rates of parasitism on different stages of A. fabae (P < 0.01). Using logistic regression, a type II functional response was determined for A. matricariae. The Holling and Rogers models were used for estimating searching efficiency (a) and handling time (T_h). The data was fitted by the Rogers equation better than by the Holling disc equation based on the R² values. The estimated values of searching efficiency and handling time were 0.040 ± 0.013/h and 3.439 ± 0.383 h, respectively. The per capita searching efficiency decreased significantly from 0.272 to 0.139 as parasitoid densities increased from one to five. Therefore, different host‐parasitoid ratios could affect the efficacy of A. matricariae.     

Aphelinus albipodus(Hymenoptera: Aphelinidae) andDiaeretiella rapae(Hymenoptera: Braconidae) Parasitism onDiuraphis noxia(Homoptera: Aphididae) Infesting Barley Plants Differing in Plant Resistance to Aphids

Russian wheat aphid,Diuraphis noxia(Mordvilko), as a pest of small grains, has prompted research into biological control and host plant resistance. In the presence of Russian wheat aphid, leaves of a susceptible barley (Morex) are curled and chlorotic and sustain large densities of this aphid, while leaves of a resistant barley (STARS-9301B) remain flat and green and sustain fewer aphids. Might parasitism of Russian wheat aphid byAphelinus albipodusHayat & Fatima andDiaeretiella rapaeMcIntosh be affected differently by these plant types? When presented the plants separately and based on parasitism rate relative to aphid density, the largerD. rapaewas more effective in parasitizing relatively high densities of aphids within curled leaves of Morex than relatively low densities of aphids on uncurled leaves of STARS-9301B. Parasitism byA. albipodusdid not significantly differ among the plants. When given a choice of plants, approximately equal rates of parasitism occurred on the two plant lines for both parasitoid species, and parasitism byD. rapaewas greater thanA. albipodus.These data indicate that using parasitoid size as an indicator of success in a physically restricted environment may be misleading, when considered in a plant environment responsive in several manners to aphids (chlorosis, curling, and ability to sustain Russian wheat aphid). We expect that use of resistant barley will result in decreased parasitoid abundance as aphid densities decrease. However, parasitism rates are expected to be approximately equal on resistant and susceptible barley. In this system, plant resistance and biocontrol are compatible management strategies.     

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.     

Evaluation of four aphidiine parasitoids for biological control ofAphis gossypii

Four aphidiine parasitoid species (Hymenoptera: Braconidae) were evaluated with respect to their potential to controlAphis gossypii Glover (Homoptera: Aphididae) in glasshouse cucumbers. In a laboratory experiment thirty cotton aphids were offered to individual females for two hours.Aphidius matricariae Haliday parasitized less than six percent of the aphids and was ruled out as potential biological control agent.Ephedrus cerasicola Stary andLysiphlebus testaceipes Cresson parasitized 23 and 26 percent of the aphids, respectively.Aphidius colemani Viereck parasitized 72 to 80 percent of the aphids. With the latter three species, experiments were performed in small glasshouses with cucumbers (Cucumis sativus L. cv. ‘Aramon’). As in the laboratory testA. colemani performed best; significantly more colonies were found and parasitization rates in the colonies were higher byA. colemani than byE. cerasicola andL. testaceipes. Because of the good correspondence between laboratory and glasshouse experiments, it is suggested that bad performance of an aphid parasitoid species in a simple laboratory trial might be sufficient evidence to disregard this species for further tests.     

Effects of cold storage on life-history traits of Aphidius matricariae

Aphidius matricariae Haliday (Hymenoptera: Braconidae) is a polyphagous solitary endoparasitoid, attacking more than 40 species of aphids. This parasitoid is an important commercial product of many companies that produce biological control agents. Storage at low temperature increases the shelf life of many biocontrol agents, allowing companies to provide a steady and sufficient supply of insects for biocontrol programs. In the current study, the effects of cold storage of 1-day-old host mummies with A. matricariae for various time periods (5, 10, 15, 20, and 30 days) at 5 °C on the parasitoid’s key life-history traits were investigated. Parameters assessed after storage included adult emergence rate, offspring sex ratio, adult longevity, oviposition period, fecundity, and life-table parameters (R₀, r, λ, T, and DT). Our results showed that the mummies of A. matricariae could be stored at 5 °C for 5 days without loss of quality and for 10–15 days with minimal reduction in quality (e.g., some reduction in adult longevity and R₀). If parasitoids were stored for >15 days, quality was more strongly affected. In conclusion, A. matricariae pupae could be stored at 5 °C for up to 15 days without significant negative post-storage effects on fitness of the parasitoid. These results could be used to improve the planning of mass rearing and mass release of A. matricariae in augmentative biological control programs.     

Sex pheromones in the cereal aphid parasitoidsPraon volucre andAphidius rhopalosiphi

Laboratory and field experiments provided evidence for the release of sex pheromones by virgin femalePraon volucre Haliday andAphidius rhopalosiphi De Stefani-Perez (Hymenoptera: Braconidae, Aphidiinae). In Petri dish biosassays, rubber or vermiculite models treated with crude virgin female extracts were frequently approached by males and elicited rapid wing-fanning behaviour and copulation attempts. Delta-shaped water traps containing live virgin females caught large numbers of conspecific males when placed in winter wheat crops. Trapping slightly below crop height resulted in higher catches than trapping above the crop canopy.     

Additions and Corrections to the Check-List of the Aphidiid- Wasp Subfamily Aphidiinae (Hymenoptera,Aphidiidae) from the North-West of Russia

New material of the aphidiid-wasp subfamily Aphidiinae (Hymenoptera, Aphidiidae) from the North- Western region of Russia is reported. Aphidius eglanteriae Haliday, 1834 is recorded from this region for the first time. The following corrections to the preceding publication of 2017 have been made: 2 correctly identified specimens of Pauesia abietis (Marshall, 1896) were erroneously given also among the material of P. pini (Haliday, 1834), and 4 specimens of P. similis Starý, 1966 were misidentified as P. pini.     

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.