Interference between parasitoids [Hym.: Aphidiidae] and fungi [Entomophthorales] attacking cereal aphids

In field populations of cereal aphids parasitism levels declined through the season as fungal infection increased. In laboratory trials the fungusErynia neoaphidis Remaudiere & Hennebert took 3 to 4 days to kill the rose-grain aphid,Metopolophium dirhodum (Walker), whereas the parasitoidAphidius rhopalosiphi De Stefani-Perez took 8 to 9 days at 20°C. When aphids were infected by the fungus less than 4 days after being parasitized the parasitoids were prevented from completing their development. Conversely, when infection occurred more than 4 days after parasitization development of the fungus was significantly impaired. There was no histological evidence that the fungus invaded the tissues of the parasitoid when both attacked the same aphid. Interference between parasitoids and fungal pathogens must be taken into account when estimating the impact of these mortality agents on pest populations.     

In vitro rearing ofLysiphlebus fabarum [Hym.: Braconidae]

In vitro rearing of the aphid endoparasitoidLysiphlebus fabarum (Marshall) (Hymenoptera, Braconidae) was attempted. Successful permanent cultures ofAphis fabae Sc. andMyzus persicae Sulz. cells were not obtained. Therefore, parasitoid larvae were reared in 2 unnatural media rone of which included cells ofCeratitis capitata Wied. (Diptera, Trypetidae). A group of larvae was reared in a substrate to which parasitoid teratocytes had been added. SinceLysiphlebus fabarum females did not oviposit into paraffin droplets including the substrates, the larvae were directly transferred from parasitized aphids into the rearing media. Several larvae reached the final instar, but only 2 out of the 48 tested in the 3 substrates became adults. The meaning of teratocytes inin vitro rearing of Aphidiine, Braconids is discussed. This work was supported by a grant from the italian Ministry of Education (M.P.I. 40%).     

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.     

Life history of the tick parasitoid Ixodiphagus hookeri (Hymenoptera: Encyrtidae) in Kenya

We conducted laboratory and field experiments to elucidate the life history of Ixodiphagus hookeri, a parasitoid of the ixodid tick Amblyomma variegatum in Western Kenya. Ixodiphagus hookeri females oviposited in unfed host nymphs as well as engorged nymphs, but rarely in engorged larvae. While I. hookeri developed to adults in engorged nymphs, the eggs laid in unfed nymphs disappeared within 2 days after oviposition. As temperature increased, development time of I. hookeri from oviposition to adult emergence in engorged nymphs decreased from 46 days at 23 °C to 35 days at 28 °C, and their immature survival in engorged nymphs decreased from 67% at 23 °C to 22% at 28 °C. No parasitoid adult emerged from hosts at 30 °C. Individual hosts parasitized by single females produced 42–53 adult wasps, 73% of which were females. As a typical pro-ovigenic species, I. hookeri females had an average of 84 mature eggs at emergence and lived only for a few days. When laboratory-reared, unfed nymphs of A. variegatum were attached to cattle for 4–9 days in subsistence farmers’ fields in Western Kenya, 25% of the engorged nymphs and 4% of the unfed nymphs on cattle were parasitized by I. hookeri, demonstrating that I. hookeri females search for and oviposit in A. variegatum nymphs on cattle. Unlike other strains of I. hookeri that overwinter as eggs in unfed nymphs, I. hookeri could continuously reproduce throughout the year in Western Kenya.     

Oviposition behaviour ofEphedrus cerasicola [Hym.: Aphidiidae] parasitizing different instars of its aphid host

The parasitoidEphedrus cerasicola Starý oviposited in all 4 nymphal instars and in newly moulted adults ofMyzus persicae (Sulzer). The different host categories were offered with no choice. The duration of an oviposition increased with the age of nymphs, being about 13, 18, 21, 22, and 17 s from 1 st instars to adults, respectively. Observations of number of stabbing attacks prior to oviposition, percent of the encounters not resulting in oviposition, time from first encounter to oviposition, handling time and aphid defensive behaviour also indicated that 1 st instarM. persicae are most easily parasitized. The behaviour ofE. cerasicola in encounters with unparasitized and parasitized hosts, suggested that the parasitoid could discriminate. In encounters with parasitized 1 st to 4th instar aphids,E. cerasicola used only the antennae in 80% of the encounters that resulted in discrimination.     

Parasitism byEphedrus cerasicola [Hym.: Aphidiidae] developing in different stages ofMyzus persicae [Hom.: Aphididae]

The parasitoidEphedrus cerasicola Stary oviposited in the 4 nymphal instars and in newly moulted apterous adults ofMyzus persicae (Sulzer). Development and reproduction of unparasitized and parasitized aphids at 21°C were compared. Unparasitized aphids developed to adults in 6.5 days and started to reproduce after 7 days. Longevity varied between 7 and 42 days. Net reproductive rate (R₀) was 40.7. In contrast to older nymphs, aphids parasitized in the 1 st instar almost never reached the adult stage before mummification. Aphids parasitized in 2nd, 3rd and 4th instar and as newly moulted adults produced respectively 0.07 %, 2 %, 23 % and 32 % of offspring produced by unparasitized aphids. Corresponding reproductive periods were 1, 1.4, 3 and 4 days. Host age at parasitization had a slight effect on the parasitoid's developmental rate and had no effect on egg or pupal survival, or on the sex ratio of the emerging parasitoids.     

Mating or ovipositing? A crucial decision in the life history of the cabbage aphid parasitoid Diaeretiella rapae (M’Intosh)

1. The reproductive fitness of a parasitoid depends on its mating and ovipositing success. Virgin haplodiploid females can reproduce, but produce only males, and may diminish fitness by producing more male offspring than required. Therefore, females must decide on whether to mate or oviposit first. 2. This study was conducted to assess the mating versus ovipositing decision and its impact on the reproductive fitness of Diaeretiella rapae (Hymenoptera: Aphididae), an endoparasitoid of the cabbage aphid Brevicoryne brassicae (Hemiptera: Aphididae). 3. When newly emerged females were given a choice between mating and ovipositing, about 62% of D. rapae females preferred to mate before ovipositing. Those females who oviposited before mating parasitised only 10% of the available aphids. After mating, females superparasitised their hosts with fertilised eggs, which resulted in a highly female‐biased sex ratio in the offspring. 4. Mating success was very high (91%) in the presence of hosts (cabbage aphid nymphs) compared with that in the absence of aphids. However, mating success was not influenced by the quality (size) of the hosts present in the mating arena, despite a parasitoid preference for larger hosts during oviposition. The time between pairing and mating was also shorter in the presence of host aphids. The mean number of aphids parasitised and the parasitism rate were significantly greater after mating.     

Predator and parasitoid attacking ant-attended aphids: effects of predator presence and attending ant species on emerging parasitoid numbers

Interaction between a predator and a parasitoid attacking ant-attended aphids was examined in a system on photinia plants, consisting of the aphid Aphis spiraecola, the two ants Lasius japonicus and Pristomyrmex pungens, the predatory ladybird beetle Scymnus posticalis, and the parasitoid wasp Lysiphlebus japonicus. The ladybird larvae are densely covered with waxy secretion and are never attacked by attending ants. The parasitoid females are often attacked by ants, but successfully oviposit by avoiding ants. The two ants differ in aggressiveness towards aphid enemies. Impacts of the predator larvae and attending ant species on the number of parasitoid adults emerging from mummies per aphid colony were assessed by manipulating the presence of the predator in introduced aphid colonies attended by either ant. The experiment showed a significant negative impact of the predator on emerging parasitoid numbers. This is due to consumption of healthy aphids by the predator and its predation on parasitized aphids containing the parasitoid larvae (intraguild predation). Additionally, attending ant species significantly affected emerging parasitoid numbers, with more parasitoids in P. pungens-attended colonies. This results from the lower extent of interference with parasitoid oviposition by the less aggressive P. pungens. Furthermore, the predator reduced emerging parasitoid numbers more when P. pungens attended aphids. This may be ascribed to larger numbers of the predator and the resulting higher levels of predation on unparasitized and parasitized aphids in P. pungens-attended colonies. In conclusion, a negative effect of the predator on the parasitoid occurs in ant-attended aphid colonies, and the intensity of the interaction is affected by ant species.     

Oviposition behaviour, influence of experience on host size selection, and niche overlap of the solitary Leptomastix epona and the gregarious Pseudaphycus flavidulus, two endoparasitoids of the mealybug Pseudococcus viburni

Oviposition behaviour and host size selection of the solitary parasitoid Leptomastix epona(Walker) and the gregarious Pseudaphycus flavidulus(Brèthes) [both Hymenoptera: Encyrtidae] were examined on five size classes of the mealybug Pseudococcus viburni(Signoret) [Hemiptera: Pseudococcidae]. The host size classes mostly consisted of one stage (first, second, third instar nymph, young adult and preovipositing adult) and were presented together to wasps of either parasitoid species. Both parasitoid species locate the host by drumming the surface of the patch with the antennae. Leptomastix eponaseems to use mainly the antennae to examine the host but P. flavidulusmay accept or reject a host for oviposition after antennation or insertion of the ovipositor. Leptomastix eponaattempts oviposition in all the host stages from second instar nymphs but P. flavidulusincludes first instar. Both parasitoid species select mainly larger hosts (>1 mm, third instar nymphs) to oviposit but P. flavidulusis able to parasitize more second instar nymphs compared to L. epona. Female wasps of L. eponamay host feed on small mealybugs (second and third instar nymphs) that they do not use for oviposition. Oviposition experience of either parasitoid species for 24 hours does not influence host size selection on patches with hosts of similar mixed sizes. Oviposition decisions are independent of the host sizes of the preceding ovipositions. Implications about stability of a single parasitoid – host system and the success of biological control of the mealybug were discussed in respect of the developmental refugia of the two parasitoid species. Niche overlap of the two parasitoid species was discussed with a view to giving an insight into a single or multiple introduction.     

桃蚜脱皮对球孢白僵菌毒力的影响

室内测定了球孢白僵菌Beauveria bassiana BBSG8702菌株对桃蚜Myzus persicae 若蚜的毒力,并分析了若蚜脱皮与白僵菌有效侵染之间的关系。在21℃、1×10⁶/mL孢子浓度下, 1～4龄若蚜感菌后的累积死亡率分别为10.1%、2.1%、3.1%和40.2%,明显低于同样条件下成蚜的感菌死亡率(98.4%)。在若蚜各龄感菌死亡的个体中,1～4龄中分别有8.1%、50.0%、44.4%和98.0%的若蚜在死亡前发育到成蚜,且都能产下正常发育的后代。若蚜的感菌死亡率与接菌后到第一次脱皮的时间密切相关,脱皮早则感菌死亡率低,反之亦然。但试验中也发现有部分若蚜特别是低龄若蚜感菌后未完成第一次脱皮便死亡。观察了桃蚜在1、4龄早期感染球孢白僵菌后的发育、存活和生殖情况,结果表明：1、4龄早期若蚜接菌后第一次脱皮的时间早于未接菌若蚜,但提前幅度少于5%,在羽化为成蚜之前被致死的概率分别只有4.1%和0,在羽化为成蚜后8天内的生殖率与未接菌蚜虫的无明显差异。这些结果表明,若蚜的脱皮,尤其当蚜虫在低龄若蚜时受感染后的多次脱皮,可有效地摆脱球孢白僵菌分生孢子的侵染,降低该菌的毒力。     

Influence of aphid size,age and behaviour on host choice by the parasitoid wasp Ephedrus californicus: a test of host-size models

Summary When host quality varies, parasitoid wasps are expected to oviposit selectively in high-quality hosts. We tested the assumption underlying host-size models that, for solitary species of wasps, quality is based on host size. Using Ephedrus californicus, a solitary endoparasitoid of the pea aphid, we evaluated the influence of aphid size (= mass), age and defensive behaviours on host selection. Experienced parasitoid females were given a choice among three classes of 5-day-old apterous nymphs: small aphids that had been starved daily for 4 h (S4) and 6 h (S6) respectively, and large aphids permitted to feed (F) normally. Wasps attacked more, and laid more eggs in, small than large aphids (S6>S4>F). This rank-order for attack did not change when females could choose among aphids of the same size that differed in age; however, wasps oviposited in all attacked aphids with equal probability. Host size did not influence parasitoid attack rates when aphids were anaesthetized so that they could not escape or defend themselves. As predicted by host-size models, wasp size increased with host size (F>S4; S6), but large wasps required longer to complete development than their smaller counterparts (S4E. californicus reflects a trade-off between maximization of fitness gains per egg and the economics of search-time allocation. Because large aphids are more likely to escape parasitization, a wasp must balance her potential gain in fitness by ovipositinng in a high-quality (large) aphid against her potential cost in terms of lost opportunity time if the attack fails.     

Wheat containing snowdrop lectin (GNA) does not affect infection of the cereal aphid <Emphasis Type="Italic">Metopolophium</Emphasis><Emphasis Type="Italic">dirhodum</Emphasis> by the fungal natural enemy<Emphasis Type="Italic">Pandora neoaphidis</Emphasis>

Studies were carried out to determine if susceptibility of the cereal aphid Metopolophium dirhodum to the fungus Pandora neoaphidis was affected by wheat expressing snowdrop lectin (GNA). Aphid infection did not differ significantly between the transgenic GNA and non-transformed lines (91 and 82%, respectively). Fecundity also did not differ between aphids on the two lines, and was ca. 18 nymphs adult⁻¹. Time to infection was ca. 5 days for M. dirhodum on both lines in two of three assays. Our results indicate that wheat expressing GNA would not compromise the efficacy of P. neoaphidis as a biocontrol agent.     

Effect of wheat resistance, the parasitoid Aphidius rhopalosiphi, and the entomopathogenic fungus Pandora neoaphidis, on population dynamics of the cereal aphid Sitobion avenae

The influence of wheat (Triticum aestivumL.) resistance, the parasitoid Aphidius rhopalosiphiDe Stephani-Perez (Hymenoptera: Braconidae) and the entomopathogenic fungus Pandora neoaphidis(Remaudière et Hennebert) Humber (Zygomycetes: Entomophthorales) on the density and population growth rate of the cereal aphid Sitobion avenae(F.) (Hemiptera: Aphididae) was studied under laboratory conditions. Partial wheat resistance was based on hydroxamic acids, a family of secondary metabolites characteristic of several cultivated cereals. The partial resistance of wheat cultivar Naofén, the action of the parasitoid and the joint action of the parasitoid and fungus, reduced aphid density. The lowest aphid densities were obtained with the combination of the parasitoid and the fungus, but wheat resistance under these circumstances did not improve aphid control. Significant reductions of population growth rate (PGR) of aphids were obtained with the joint action of wheat resistance and natural enemies. In particular, the combined effects of parasitoids and fungi showed significantly lower PGR than the control without natural enemies in both wheat cultivars. Our results support the hypothesis that wheat resistance and the utilization of biological control agents could be complementary strategies in an integrated pest management program against cereal aphids.     

Parasitoid-host relationship betweenTrioxys (Binodoxys) Indicus [Hymenoptera: Aphidiidae] andAphis Craccivora [Hemiptera: Aphididae]. VI. Impact of males on the number of progeny of the parasitoid reared on certain host plants

The present paper elucidates the impact of males on the reproductive rate ofTrioxys (Binodoxys) indicus reared on the aphids ofCajanus cajan, Dolichos lablab andSolanum melongena host plants. The F₁ offspring increases with the increase of parasitoid number. This increase is maximum inC. cajan followed byD. lablab andS. melongena reared aphids. The presence of male parasitoids caused a significant decrease in the emergence of F₁ generation.      

Alaboratory evaluation ofAnthocoris nemorum andA. nemoralis [Hem.: Anthocoridae] as predators ofPhorodon humuli [Hom.: Aphididae]

Anthocoris nemorum (L.) andA. nemoralis (F.) were reared on apterous hop aphids,Phorodon humuli (Schrank), at 20±0.5°C.A. nemorum andA. nemoralis killed an average of 255 and 174 aphids respectively during nymphal development, and the adults killed 37 and 33 per day respectively. Small anthocorid nymphs selectively killed small aphids but adult anthocorids and 5th instar nymphs killed aphids of every size. Mean development times from emergence to final moult were 22 and 16 days forA. nemorum andA. nemoralis respectively.     

Importation,colonization and establishment ofAnagyrus indicus [Hym.: Encyrtidae] onNipaecoccus viridis [Hom.: Pseudococcidae] in Jordan

Anagyrus indicus Shafeeet al. was collected on the island of Guam and released in the Jordan River Valley of Jordan in order to regulateNipaecoccus viridis (Newstead) on citrus.A. indicus was originally released in February 1984 and became colonized by April of the same year. It also dispersed by natural means up to 61 km following the original release and colonized that same year on infestedZizyphus sp. By spring of 1985 it became the dominant parasitoid attackingN. viridis. Another parasitoid,Anagyrus kamali Moursi, was collected in Jordan in June of 1985 for the first time. This latter parasitoid apparently moved into the Jordan River Valley by means of natural dispersal from a neighboring country. Infestations ofN. viridis have been greatly reduced in areas whereA. indicus became established. This paper reports the results of research only. Mention of a proprietary product does not constitute an endorsement for its use by USDA.     

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.     

Larvicidal activity of lectins onLucilia cuprina: mechanism of action

Foraging behaviour and host-instar preference of young and old females of the solitary aphid parasitoid,Lysiphlebus cardui Marshall (Hymenoptera: Aphidiidae), were studied in the laboratory. The analysis of interactions between parasitoids and different stages ofAphis fabae cirsiiacanthoidis Scop. (Homoptera: Aphididae) revealed that encounter rates between aphids and parasitoid females and defence reactions of the aphids influenced the degree to which a particular aphid age class is parasitized. Encounter rates between hosts and parasitoid females depended on the foraging pattern of the parasitoid, which varied with age. In mixed aphid colonies patch residence time increased with parasitoid age. Furthermore, younger parasitoids (≦1 day old) laid more eggs into second and third instars, while older parasitoids (≧4 days old) did not show distinct host instar preferences. It is suggested that the oviposition behaviour ofL. cardui is influenced by the physiological state, i.e. the age of the wasp.     

Biological control ofAphis pomi [Hom.: Aphididae] ofAphidoletes aphidimyza [Dip.: Cecidomyiidae]; a predator-prey model

Predation ofAphis pomi DeGeer [Hom.: Aphididae] byAphidoletes aphidimyza (Rondani) [Dipt.: Cecidomyiidae] was simulated in Michigan apple orchards using a computer and output validated against field data collected from sleeve cages enclosing aphid infested apple terminals. Lower and upper temperature thresholds for development were 2.9 and 35°C for nymphs ofA. pomi with a mean immature developmental period of 162.3 heat units. Median survivorship of adultA. pomi was 364.3 heat units with an average fecundity of 60.7 offspring per female.A. aphidimyza egg and larval lower threshold and developmental periods were 10.5 and 25.5, 8.1°C and 65.5 heat units, respectively. Larval functional response showed Type II behavior with a y-asymptote of 45 aphids killed per predator. Multiple generation model runs performed under different initial predator: prey densities indicated that current critical predator: prey ratios used in the field for control decisions may underestimate predator efficacy.      

Life history ofAphis gossypii on cucumber: influence of temperature, host plant and parasitism

Life table data forAphis gossypii Glover (Homoptera: Aphididae), an important pest in glasshouse cucumber crops, were studied at 20, 25 and 30°C on two cucumber cultivars (Cucumis sativus L.) in controlled climate cabinets. The development time on the cucumber cv. ‘Sporu’ ranged from 4.8 days at 20°C to 3.2 days at 30°C. Immature mortality was approximately 20% and did not differ between temperatures. Most mortality occurred during the first instar. Reproduction periods did not differ among temperatures, but at 25 and 30°C more nymphs were produced (65.9 and 69.8 nymphs/♀, respectively) than at 20°C (59,9 nymphs/♀) because of a higher daily reproduction. Intrinsic rate of increase was greatest at 25°C (r _m =0.556 day⁻¹). At 20 and 30°C the intrinsic rate of increase was 0.426 and 0.510, respectively. On cv. ‘Aramon’, the development time ofA. gossypii was approximately 20% longer at all temperatures. Immature mortality did not differ between the two cultivars. The intrinsic rate of increase on cv. ‘Aramon’ was 15% smaller than on cv. ‘Sporu’. The use of cucumber cultivars partially resistant to aphids is discussed in relation to biological control of cotton aphid in glasshouses. Development time and immature mortality on leaves of the middle and upper leaf layer of glasshouse grown cucumber plants (cv. ‘Aramon’) were comparable to development in the controlled climate cabinets. On the lower leaves immature mortality was much higher (approximately 82%) than on leaves of the middle (24.0%) and upper leaf layer (24.5%). Reproduction was less on the lower leaf layer (45.9, 70.5 and 70.1 nymphs/♀ on leaves of the lower, middle and upper leaf layer, respectively). Aphids, successfully parasitized byAphidius colemani Viereck (Hymenoptera: Braconidae) only reproduced when they were parasitized after the third instar. Fecundity was 0.1 to 0.9 and 10.5 to 13.3 nymphs/♀ for aphids parasitized in the fourth instar or as adults, respectively. Reproduction of aphids that were stung but survived the attack was lower than for aphids not stung. Average longevity of these aphids was equal to the longevity of aphids not stung byA. colemani.