Tetrastichine aphid hyperparasitoids (Hymenoptera: Eulophidae) in Japan

A small collection of aphid hyperparasitic species of Tetrastichinae obtained by rearing mummified aphids in Japan were examined. In addition to the two already known species, three more species were confirmed to occur in Japan. A key to these five Japanese species and their hosts (primary parasitoids, aphids and plants) are provided. The modes of hyperparasitism and host associations of tetrastichine aphid hyperparasitoids are discussed.     

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.     

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.     

Leaf temperature of soybean grown under elevated CO2 increases Aphis glycines (Hemiptera: Aphididae) population growth

Abstract Plants grown under elevated carbon dioxide (CO₂) experience physiological changes that influence their suitability as food for insects. To determine the effects of living on soybean (Glycine max Linnaeus) grown under elevated CO₂, population growth of the soybean aphid (Aphis glycines Matsumura) was determined at the SoyFACE research site at the University of Illinois, Urbana‐Champaign, Illinois, USA, grown under elevated (550 μL/L) and ambient (370 μL/L) levels of CO₂. Growth of aphid populations under elevated CO₂ was significantly greater after 1 week, with populations attaining twice the size of those on plants grown under ambient levels of CO₂. Soybean leaves grown under elevated levels of CO₂ were previously demonstrated at SoyFACE to have increased leaf temperature caused by reduced stomatal conductance. To separate the increased leaf temperature from other effects of elevated CO₂, air temperature was lowered while the CO₂ level was increased, which lowered overall leaf temperatures to those measured for leaves grown under ambient levels of CO₂. Aphid population growth on plants grown under elevated CO₂ and reduced air temperature was not significantly greater than on plants grown under ambient levels of CO₂. By increasing Glycine max leaf temperature, elevated CO₂ may increase populations of Aphis glycines and their impact on crop productivity.     

Life history and morphological plasticity of the soybean aphid,Aphis glycines

The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is a pest of soybean, Glycine max (L.) Merr. (Fabaceae), from eastern Asia that was first reported in North America in 2000. The influence of temperature on plasticity of life history and morphological traits of the soybean aphid has not been tested despite observable differences in population growth and morphology among isolates in laboratory colonies. Therefore, we used three isolates of the aphid to test whether lifespan, growth rate, fecundity, and morphology were plastic at 16, 24, and 28 °C. Population size of the aphid was influenced by temperature, probably because two reproductive traits, maximum number of offspring in 1 day and total fecundity, were plastic and increased in successive generations at 24 °C. All morphological traits were plastic, including lengths of body parts, number of antennal segments and caudal hairs, and color of siphunculi and body, and they were differentially influenced by isolate and temperature. Knowledge about the life history and morphology of the soybean aphid may help identify its capacity for phenotypic plasticity in heterogeneous temperatures and identify how temperature influences its survival, population growth, and diversity.     

Development and parasitism by Aphelinus certus (Hymenoptera: Aphelinidae), a parasitoid of Aphis glycines (Hemiptera: Aphididae)

Since its introduction in 2000, the soybean aphid (Aphis glycines Matsumura) has been a serious pest of soybean in North America. Currently, insecticide application is the only recommended control method. However, a number of natural enemies have the potential to regulate soybean aphid populations. In 2007, Aphelinus certus Yasnosh, a soybean aphid parasitoid native to Asia, was found in commercial soybean fields in Ontario. This is the first record of this species in North America. To evaluate the potential biological control services provided by A. certus for soybean aphid management, temperature-dependent developmental parameters and functional response to soybean aphid were determined. A. certus is capable of completing its development between temperatures of 15.3 and 30.2°C. The lower thresholds of development for the egg-mummy and mummy-adult life stages were determined to be 9.1 and 11.6°C, respectively. The lethal temperature of development for the egg-mummy and mummy-adult life stages were 29.5 and 31.0°C, respectively. In this temperature range, A. certus did not exhibit temperature-dependent mortality; however, parasitism rate increased with temperature. A. certus exhibited a type II functional response to the soybean aphid.     

Reproductive compatibility and genetic variation between two strains of Aphelinus albipodus (Hymenoptera: Aphelinidae), a parasitoid of the soybean aphid, Aphis glycines (Homoptera: Aphididae)

Aphelinus albipodus Hayat and Fatima is a potential biological control agent of the soybean aphid, Aphis glycines Matsumura, which is a newly introduced soybean pest in the United States. We compared the reproductive compatibility and molecular genetic variation between two geographic strains of A. albipodus. One strain was collected from soybean aphids in Japan and the other recovered from Russian wheat aphid, Diuraphis noxia (Mordvilko), in the western U.S., populations of which were established with parasitoids imported from Eurasia. We present results of crossing experiments between the two strains, genetic differences based on RAPD-PCR markers, rDNA ITS1 and ITS2 gene sequences, and presence of Wolbachia in the two strains using PCR amplification of the wsp gene. We found no reduction in the production of females in reciprocal crosses between strains, but a significant reduction in fecundity when F₁ females stemming from one of the reciprocal crosses were backcrossed to males from either source. The two strains differed by 3.4% in the rDNA ITS1 sequence and by presence/absence of one RAPD-PCR marker from a total of 20 RAPD primers screened, but their rDNA ITS2 sequences were identical. We used restriction enzyme analysis to separate the strains by differential digestion of the ITS1 PCR product. Wolbachia was present in 100% of males and females of both strains of A. albipodus.     

Patterns of diversity for aphidiine (Hymenoptera: Braconidae) parasitoid assemblages on aphids (Homoptera)

We used aphids (Aphidae) as a representative hemimetabolous host family to investigate patterns of parasitoid (Aphidiine) assemblage size. The aphidiine assemblages from 477 aphid species were used to estimate average assemblage size and the influence of eight ecological and taxonomic variables. Aphids species support an average of 1.7 aphidiine species. Aphid subfamily and invasion status (native or exotic) were the most important determinants of parasitoid richness, explaining 28% of the deviance in aphidiine assemblage size. Aphids within the largest aphid subfamily, the Aphidinae, support larger parasitoid assemblages than those in other subfamilies. Parasitoid diversity was also highest on exotic aphid hosts (within the Aphidinae) and on hosts in developed habitats (agricultural or urban), though the latter effect is weak. Patterns related to aphid food plant architecture were influenced by an interaction with aphid invasion status; parasitoid diversity drops with increasing architectural complexity on exotic aphids, whereas the diversities on native aphid hosts are similar on different plant types. Weak effects were also found for aphid food plant alternation (whether or not aphids switch hosts seasonally) and climate (annual range in temperature); alternating aphids support more parasitoids than non-alternating hosts, and parasitoid assemblage size is lowest in warm climates. Taxonomic isolation of aphids at the generic level showed no significant relationship with parasitoid diversity. Finally, in contrast to parasitoid assemblages on holometabolous hosts, sample size effects were weak for aphids, possibly due to the narrow host ranges of aphidiines. Received: 22 November 1997 / Accepted: 7 March 1998     

Testing soybean antibiosis to three clones of soybean aphid, Aphis glycines (Hemiptera: Aphididae) using sprouts and leaflets

Antibiosis of eight soybean cultivars to three clones of soybean aphids (Aphis glycines Matsumura) was evaluated using both soybean sprouts and leaflets. Overall, the performance of soybean aphid was better on sprouts than on leaflets. We confirmed previous reports that Dowling and Jackson cultivars exhibited strong resistance to a clone of soybean aphids from the US, but not to either Japanese or Indonesian clones. The USA clone had delayed development, fewer offspring, and low emergence rates on these two cultivars. However, abnormal offspring were only investigated on the Tachinagaha cultivar. We confirmed that Bay and Himeshirazu cultivars were strongly resistant to the Japanese aphid clone; aphids produced fewer offspring and deformed offspring on Bay and had delayed development and a low rate of emergence on Himeshirazu. None of the eight soybean cultivars were resistant to the Indonesian clone, although abnormal offspring were produced on Jackson, Adams, and Tachinagaha cultivars. These data suggest that there are genetic differences among the three tested clones of soybean aphid and that the characteristics of local soybean aphid clones must be considered when developing resistant soybean cultivars for a given geographic area.     

Flight performance of the soybean aphid, Aphis glycines (Hemiptera: Aphididae) under different temperature and humidity regimens

The soybean aphid, Aphis glycines (Matsumura), is native to eastern Asia and has recently invaded North America, where it is currently the most important insect pest of soybeans. The soybean aphid has spread rapidly within North America, presumably through a combination of active and passive (wind-aided) flight. Here, we studied the active flight potential of A. glycines under a range of environmental conditions using an aphid flight mill. Winged (alate) A. glycines were tested on a specially designed 32-channel, computer-monitored flight mill system. Aphids that were 12-24 h old exhibited the strongest flight behavior, with average flight durations of 3.3-4.1 h, which represented flight distances of 4.6-5.1 km. After the age of 72 h, A. glycines flight performance rapidly declined. The optimum temperature range for flight was 16-28 degrees C, whereas optimum relative humidity was 75%. Our findings show that A. glycines posseses a fairly strong active flight aptitude (ability and inclination) and point to the possibility of flight initiation under a broad range of environmental conditions. These results have the potential to aid forecasting and management protocols for A. glycines at the landscape level.     

Photosynthetic responses of soybean to soybean aphid (Homoptera: Aphididae) injury

The soybean aphid, Aphis glycines Matsumara, was discovered in the United States in the summer of 2000. Since that initial discovery, the aphid has spread across northern soybean production regions. In 2001, we examined the physiological responses of soybeans to low aphids densities (fewer than 50 aphids/leaf). In this study, we determined photosynthetic rates, leaf fluorescence responses, and photosynthetic responses to variable carbon dioxide and light levels. In addition, analyses for chlorophyll content and stable carbon isotope ratios were used to differentiate potential differences in stomatal versus mesophyll limitations to photosynthesis. We observed rate reductions of up to 50% on infested leaflets, including lealets with no apparent symptoms of aphid injury (such as chlorosis). Differences in fluorescence data indicated that photoelectron transport was not impaired. These results indicate that substantial physiological impact on soybean is possible even at low aphid densities. Also, the conventional view of aphid injury acting through reductions in chlorophyll content and light-harvesting reactions of photosynthesis is not supported by our findings in this system.     

Identification and expression profiles analysis of odorant‐binding proteins in soybean aphid,Aphis glycines (Hemiptera: Aphididae)

The soybean aphid, Aphis glycines, is an extreme specialist and an important invasive pest that relies on olfaction for behaviors such as feeding, mating, and foraging. Odorant‐binding proteins (OBPs) play a vital role in olfaction by binding to volatile compounds and by regulating insect sensing of the environment. In this work we used rapid amplification of complementary DNA ends technology to identify and characterize 10 genes encoding A. glycines OBPs (AglyOBPs) belonging to 3 subfamilies, including 4 classic OBPs, 5 Plus‐C OBPs, and one Minus‐C OBP. Quantitative real‐time polymerase chain reaction demonstrated variable specific expression patterns for the 10 genes based on developmental stage and aphid tissue sampled. Expression levels of 7 AglyOBPs (2, 3, 4, 5, 7, 9, and 10) were highest in the 4th instar, indicating that the 4th nymphal instar is an important developmental period during which soybean aphids regulate feeding and search for host plants. Tissue‐specific expression results demonstrated that AglyOBP2, 7, and 9 exhibited significantly higher expression levels in antennae. Meanwhile, ligand‐binding analysis of 5 OBPs demonstrated binding of AglyOBP2 and AglyOBP3 to a broad spectrum of volatiles released by green leaf plants, with bias toward 6‐ to 8‐carbon chain volatiles and strong binding of AglyOBP7 to trans‐β‐farnesene. Taken together, our findings build a foundation of knowledge for use in the study of molecular olfaction mechanisms and provide insights to guide future soybean aphid research.     

Density and distribution of soybean aphid,Aphis glycines Matsumura (Hemiptera: Aphididae) in response to UV radiation

Increasing ultraviolet radiation (UV) has led to greater interest in its current and potential effects on organisms, including herbivorous insects. Here we report the short-term effects of UV on soybean aphids (Aphis glycines Matsumura), a common phytophagous pest of soybeans. We used two complementary approaches to examine how modifying UV radiation affects this phloem-feeding herbivore via changes to soybean aphid densities and their within plant distribution. We found that artificially adding UV in a lab setting decreased soybean aphid population size compared to a low UV control; however, blocking UV radiation in the field had minimal effects on aphid density. Further observations suggest that soybean aphid location could mediate UV effects; feeding on the underside of leaves may shield aphids from some harmful effects of UV. Our results demonstrate the potential importance of UV to insect herbivores and how behavior may influence such effects.     

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.     

Efficacy assessment of Aphidius colemani (Hymenoptera: Braconidae) for suppression of Aphis gossypii (Homoptera: Aphididae) in greenhouse-grown chrysanthemum

To assess biological control as a management tool for the cotton aphid, Aphis gossypii Glover (Homoptera: Aphididae), the efficacy of Aphidius colemani Viereck (Hymenoptera: Braconidae) for suppression of A. gossypii in greenhouse-grown chrysanthemums, Dendranthema grandiflora (Tzvelev), was compared with a pesticide standard, imidacloprid (Marathon 1% G) and an untreated check. No significant differences were found between aphid populations in the two treatments. A. colemani and imidacloprid kept aphid numbers very low, with the correspondent aphid populations exhibiting very low intrinsic rates of increase (r(m) = -0.0369 and r(m) = 0.0151, respectively), in contrast to the exponential growth of aphid populations (r(m) = 0.1085) observed on the untreated plants. Parasitism levels in A. colemani plots ranged from 48.93 to 83.38%. Esthetic damage parameters, including exuviae, honeydew, and sooty mold on leaves, were significantly different between treatments and untreated control, and damage levels were minimal with the insecticide treatment and natural enemy releases. The cost of A. colemani releases was 4.7 times greater than the cost of the imidacloprid treatment.     

Bionomics of Scymnus (Pullus) louisianae J. Chapin (Coleoptera: Coccinellidae) as a predator of the soybean aphid,Aphis glycines Matsumura (Homoptera: Aphididae)

A field population of Scymnus louisianae Chapin (Coccinellidae) was found attacking soybean aphids, Apis glycines Matsumura (Aphidae), a pest recently introduced into Kentucky. This coccinellid had not previously been found in Kentucky. A greenhouse population of S. louisianae was established and its predation on A. glycines studied under laboratory conditions. Total time to develop from egg to adult was about 20 d. About 70% of immatures survived to adulthood and they consumed approximately 100 aphid nymphs per beetle larva during the beetle's four larval instars. Adults lived for an average of 47 d (mated males) and 63 d (mated females) and, during their total adult lifetime, mated males consumed an average of 665 nymphs and mated females consumed 1261 nymphs. All developmental times and predation rates were comparable to those reported for other aphidophagous Scymnus spp. which, in conjunction with reports that Scymnus spp. are effective predators of cotton aphids, Aphis gossypii Glover, suggests that S. louisianae is a potentially important predator of A. glycines in the southern United States.     

Demography of soybean aphid (Homoptera: Aphididae) at summer temperatures

Soybean aphid, Aphis glycines Matsumura, is now widely established in soybean, Glycine max L., production areas of the northern United States and southern Canada and is becoming an important economic pest. Temperature effect on soybean aphid fecundity and survivorship is not well understood. We determined the optimal temperature for soybean aphid growth and reproduction on soybean under controlled conditions. We constructed life tables for soybean aphid at 20, 25, 30, and 35 degrees C with a photoperiod of 16:8 (L:D) h. Population growth rates were greatest at 25 degrees C. As temperature increased, net fecundity, gross fecundity, generation time, and life expectancy decreased. The prereproductive period did not differ between 20 and 30 degrees C; however, at 30 degrees C aphids required more degree-days (base 8.6 degrees C) to develop. Nymphs exposed to 35 degrees C did not complete development, and all individuals died within 11 d. Reproductive periods were significantly different at all temperatures, with aphids reproducing longer and producing more progeny at 20 and 25 degrees C than at 30 or 35 degrees C. Using a modification of the nonlinear Logan model, we estimated upper and optimal developmental thresholds to be 34.9 and 27.8 degrees C, respectively. At 25 degrees C, aphid populations doubled in 1.5 d; at 20 and 30 degrees C, populations doubled in 1.9 d.     

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.     

Application of DNA barcoding to the identification of Hymenoptera parasitoids from the soybean aphid (Aphis glycines) in China

Aphis glycines Matsumura is an important pest of soybean in Asia and North America. Hymenoptera parasitoids play a key role in the control of the soybean aphid. The correct identification of parasitoids is a critical step that precedes the assessment of their potential biological control agents. Accurate identification of the majority of the species attacking the soybean aphid often requires elaborate specimen preparation and expert taxonomic knowledge. In this study, we facilitated the identification of soybean aphid parasitoids by applying a DNA barcoding approach following a preliminary morphological identification. We generated DNA sequence data from the mitochondrial COI gene and the D2 region of 28S rDNA to assess the genetic variation within and between parasitoid species emerging from the soybean aphid in China. Fifteen Hymenoptera parasitoid species belonging to 10 genera of five families were identified with little intra‐specific variation (0.09% ± 0.06% for 28S and 0.36% ± 0.18% for COI) and large inter‐specific divergence (30.46% ± 3.42% for 28S and 20.4% ± 1.20% for COI).     

Biological parameters and thermal requirements of the parasitoid Praon volucre (Hymenoptera: Braconidae) with Macrosiphum euphorbiae (Hemiptera: Aphididae) as host

The effect of temperature on the biology of Praon volucre (Haliday, 1833) (Hymenoptera: Braconidae) in Macrosiphum euphorbiae (Thomas, 1878) (Hemiptera: Aphididae) hosts was studied and the thermal requirements of the parasitoid were determined. Experiments were carried out at 16, 19, 22, 25, and 28 ± 1°C with 70 ± 10% relative humidity and 12 h photophase. The developmental time of P. volucre males and females decreased between 16 and 23°C. The highest percentages of aphid parasitism and adult parasitoid emergence were observed at 16, 19, and 22°C. The sex ratio (expressed as % females) decreased between 16 and 23°C. Male and female longevity was high between 19 and 22°C and decreased strongly at 25°C. The lower temperature threshold for P. volucre was 5.17°C and the thermal constant was 243 degrees-days.