Climate Change and Phenology: Empoasca fabae (Hemiptera: Cicadellidae) Migration and Severity of Impact

Climate change can benefit individual species, but when pest species are enhanced by warmer temperatures agricultural productivity may be placed at greater risk. We analyzed the effects of temperature anomaly on arrival date and infestation severity of potato leafhopper, Empoasca fabae Harris, a classic new world long distance migrant, and a significant pest in several agricultural crops. We compiled E. fabae arrival dates and infestation severity data at different states in USA from existing literature reviews and agricultural extension records from 1951–2012, and examined the influence of temperature anomalies at each target state or overwintering range on the date of arrival and severity of infestation. Average E. fabae arrival date at different states reveal a clear trend along the south-north axis, with earliest arrival closest to the overwintering range. E. fabae arrival has advanced by 10 days over the last 62 years. E. fabae arrived earlier in warmer years in relation to each target state level temperature anomaly (3.0 days / °C increase in temperature anomaly). Increased temperature had a significant and positive effect on the severity of infestation, and arrival date had a marginal negative effect on severity. These relationships suggest that continued warming could advance the time of E. fabae colonization and increase their impact on affected crops.     

Effect of dietary amino acids on the size and alary polymorphism of Aphis fabae

Aphis fabae was reared on synthetic diets omitting individual amino acids and amino acid groups. Methionine and histidine deletions induced apterae formation and prevented the aphids from reaching the adult stage, whereas arginine, leucine, lysine, and proline deletions induced alatae formation. The omission of alanine, cysteine, phenylalanine, proline, serine, and tyrosine reduced the size attained by adult alatae and together with methionine and histidine, these amino acids are considered to be essential for normal growth by A. fabae. A delay in parturition occurred in aphids reared on certain deficient diets and there is an association between the size attained by alatae and the delay in parturition.     

Responses of Episyrphus balteatus DeGeer (Diptera: Syrphidae) in relation to prey density and predator size

Laboratory experiments were conducted to determine the functional and numerical responses of the aphidophagous hover fly Episyrphus balteatus DeGeer (Diptera: Syrphidae) to different densities of 4th instar black bean aphids, Aphis fabae Scopoli (Homoptera: Aphididae), on broad bean, Vicia faba L. (Fabaceae). Two different-sized larvae of predators were tested in different densities of similar-sized prey to determine whether functional response parameters depended on the body sizes of predator and prey. In numerical response experiments, gravid E. balteatus females were exposed individually to different densities of 4th instars of A. fabae on cut sections of the broad bean plant, V. faba L. Logistic regression suggested a type II functional response for both larval sizes of E. balteatus. The searching efficiency (a) of the larger larvae was higher than that of the smaller ones. Prey consumption was higher, and handling time (T_h) was lower for larger larvae than smaller ones. The theoretical maximum number of A. fabae nymphs eaten by the different-sized larvae was 125 and 269 nymphs per day. Larger E. balteatus larvae are more efficient predators for aphid management strategies. The reproductive numerical response, in terms of the number of eggs laid, increased curvilinearly with increasing prey density, but the proportion of eggs laid (egg number/prey density) decreased as the initial density of prey increased.     

Aphid Parasitoid Mothers Don't Always Know Best through the Whole Host Selection Process

Parasitoid host selection behaviour has been extensively studied in experimentally simplified tritrophic systems formed by one single food chain (one plant, one herbivore and one parasitoid species). The "Mother knows best" hypothesis predicts that the preference for a plant-host complex should be positively correlated with plant quality for offspring performance. We studied the host selection behaviour of the generalist endoparasitoid Aphidius matricariae towards the black bean aphid Aphis fabae in the intercrop system including Vicia faba as a focal plant and its companion plant Camelina sativa. Dual-choice laboratory bioassays revealed that parasitoid females preferred to orientate towards (1) the plant-aphid complex over the non-infested plant whatever the complex (2) the C. sativa-A. fabae complex over the V. faba-A. fabae complex. In dual choice attack rate bioassays, parasitoid females showed more interest towards the aphids on C. sativa but paradoxically chose to oviposit more in aphids on V. faba. Ultimately, parasitoids that had developed on the V. faba-A. fabae complex exhibited better fitness parameters. By demonstrating that parasitoid females were able to discriminate the aphid host that offered the highest fitness to their offspring but selected beforehand the least suitable plant-aphid complex, we provide key insight into the disruption in their host selection behaviour potentially triggered by diverse habitats. This suggests that the "Mother knows best" hypothesis could be thwarted by increasing the complexity of the studied systems.     

Morphogenetic effects of precocenes on three aphid species

The disruptive effects of precocenes I, II and III on metamorphosis were assessed in apterous viviparae of Acyrthosiphon pisum, Aphis fabae and Megoura viciae. Prenatally applied precocene I had no effect, precocene II caused supernumerary moulting (metathetely) in M. viciae but precocene III induced both precocious adult development (prothetely) and metathetely in all three species. the latter compound also promoted precocious adult development in alate virginoparae, males and ovipara-producers of M. viciae. However, gynoparae of A. fabae, and oviparae of M. viciae and A. pisum were resistant to this action. When topically applied to young adults of A. fabae or M. viciae none of the precocenes caused alate progeny to be produced but all did so in A. pisum. However, the previous supposition that precocene II promotes wing development because it decreases juvenile hormone titres should be viewed with caution as: (a) Precocene II was more potent than precocenes I and III when inducing wing formation but did not provoke precocious adult development, an overt indication of low juvenile hormone titres. (b) Precocene I and III were equally effective in inducing alate progeny but only the latter provoked precocious adult development. (c) Attempts to prevent or reduce the alata-inducing property of precocene II with juvenile hormone I were unsuccessful.     

Between plant and diurnal variation in quantities and ratios of volatile compounds emitted by Vicia faba plants

Ratios of volatile phytochemicals potentially offer a means for insects to recognise their host-plant species. However, for this to occur ratios of volatiles would need to be sufficiently consistent between plants and over time to constitute a host-characteristic cue. In this context we collected headspace samples from Vicia faba plants to determine how consistent ratios of key volatile phytochemicals used in host location by one of its insect pests, the black bean aphid, Aphis fabae, were. These were (E)-2-hexenal, (Z)-3-hexen-1-ol, 1-hexanol, benzaldehyde, 6-methyl-5-hepten-2-one, octanal, (Z)-3-hexen-1-yl acetate, (R)-linalool, methyl salicylate, decanal, undecanal, (E)-caryophyllene, (E)-β-farnesene, (S)-germacrene D, and (E, E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene, which had previously been found to be electrophysiologically and behaviourally active to A. fabae. Although the quantities of volatiles produced by V. faba showed large between plant and diurnal variation, correlations between quantities of compounds indicated that the ratios of certain pairs of volatiles were very consistent. This suggests that there is a host-characteristic cue available to A. fabae in the form of ratios of volatiles.     

Characterization of microsatellite loci from the solitary sweat bees Lasioglossum leucozonium and Lasioglossum oenotherae (Hymenoptera,Halictidae)

Microsatellite loci were isolated from two solitary sweat bees: the polylectic Lasioglossum leucozonium (10 loci) and the oligolectic Lasioglossum oenotherae (9 loci) (Hymenoptera, Halictidae). All loci were polymorphic with high observed heterozygosities (0.07–0.75 for L. leucozonium; 0.06–0.92 for L. oenotherae). These loci will be used to study the consequences of diet specialization on the population and conservation genetics of bees.     

Effect of temperature on distribution and success of introduction of an Empoasca fabae (Homoptera: Cicadellidae) isolate of Erynia radicans (Zygomycetes: Entomophthoraceae)

Empoasca fabae is a serious leafhopper pest of agriculturally important crops in the midwestern and northeastern United States. The geographic distribution of Erynia radicans, a fungal pathogen of E. fabae, led us to examine the effects of temperature on tn vitro and in vivo growth and conidial germination of E. radicans. In addition, we examined the effects of temperature on the establishment of E. radicans in the field. E. radicans grew at constant temperatures of 28°C and below, both in vivo and in vitro, but did not grow at 30°C or above. Conidial germination followed a similar pattern; however, E. radicans survived exposure periods of up to 24 hr at 32°C in vivo. E. radicans did not cycle through a caged population of E. fabae in a growth chamber at 22°C despite the occurrence of infections immediately following fungal release. E. radicans did not become established after introduction into field populations of E. fabae at three sites in Illinois. We observed initial infections of leafhoppers at two of these sites and evidence suggests that horizontal transmission occurred at one of them. Epizootics, however, did not occur despite high populations of leafhoppers. Temperatures exceeded the laboratory thresholds for growth of E. radicans at each of the three sites during the first week after release, but for different durations.     

Sequestration of polyacetylenes by the parasite Orobanche hederae (Orobanchaceae) from its host Hedera helix (Araliaceae)

Orobanche hederae Duby and its host Hedera helix L. were collected in the North Italian Trentino-Südtirol region and analyzed for their content of polyacetylenes. Both, the host plant (Hedera) and the parasite (Orobanche) contained the polyacetylene falcarinol and two of its dehydroderivatives. The contents of polyacetylenes in Hedera decrease from roots via stems to leaves and contents in Orobanche are only about one-tenth of the contents in the Hedera roots it parasites on. Moreover, relative contents of the more polar polyacetylenes are higher in Orobanche than in Hedera, implying a bias toward the sequestration of more polar compounds.     

Some effects of benomyl and carbendazim on Aphis fabae and Acyrthosiphon pisum on field bean (Vicia faba)

Field bean plants were treated with benomyl in a glasshouse, then nymphs of Aphis fabae and Acyrthosiphon pisum were caged on the second pinnate leaf. Soil drenches at concentrations of 150 and 75 μg benomyl/ml or above increased mortality of A. fabae and A. pisum respectively; 250 μg a.i./ml increased mortality and decreased progeny production of alate A. fabae. The effect on mortality persisted for at least 16 days after treatment. Foliar sprays increased mortality at concentrations of 75 μg a.i./ml and above (A. fabae). Field populations of A. pisum were reduced when bean plants were drenched or sprayed at a concentration of 250 μg a.i./ml and A. fabae populations were reduced by drenches but not by foliar sprays. A commercial formulation of carbendazim (Bavistin) increased aphid mortality whereas the formulation medium did not. Under the experimental conditions, benomyl affected the distribution of both species on young bean plants but did not induce a repellent effect; aphids preferred untreated leaves. Mortality and preference tests, and a field experiment, indicated that A. pisum was affected more than A. fabae.     

An instantly damping oscillator model for photoperiodic time measurement in the aphid Aphis fabae

It is assumed that a non-repetitive photoperiodic clock, or “hourglass”, could be circadian based, and described as an instantly damping circadian oscillator. A model for an instantly damping oscillator is developed in the present paper and tested on photoperiodic morph determination in the black bean aphid, Aphis fabae. The kinetics of the clock are presented in the form of phase resetting curves which plot the phase of the oscillation at lights-on against the phase at lights-off. Other components of the model, that is a “counter”, that accumulates and integrates photoperiodic information contained in a number of light-dark cycles up to a threshold value for induction to occur, and an influence of the circadian system on the induction process, are as previously described in the “hourglass timer-oscillator counter” model of photoperiodic induction of diapause in the spider mite, Tetranychus urticae. It is shown that night-length measurement in A. fabae can be described by means of an instantly damping oscillator: the phase resetting curves are based on a number of photoperiodic experiments and resemble the phase resetting curves determined for overt circadian rhythms in other insects. However, the results do not distinguish between a photoperiodic clock based on a damped circadian oscillator or a non-circadian hourglass mechanism.     

Population studies on the active stages of the black bean aphid, Aphis fabae Scop., on its winter host Euonymus europaeus L

Autumn populations of Aphis fabae Scop, on the primary host Euonymus europaeus L. were little affected by natural enemies, most of which had begun to hibernate before the aphid populations developed. The size of the population in spring was usually determined by the number of overwintering eggs on a bush. The fundatrices hatched about 3–6 weeks before natural enemies became common. The growth of large A. fabae populations was first halted by the effects of intra-specinc competition, notably by the production and departure of emigrant alatae and by adult apterae reproducing more slowly. Later, natural enemies, especially Adalia 2-punctata (L.), Syrphidae and the parasite Trioxys sp. (near angelicae), multiplied and accelerated the decline in the aphid populations, which usually disappeared in June leaving many immature natural enemies. Larval A. 2-punctata began to eat parasitized aphids and cannibalized other larvae and pupae. The small populations of A. fabae that develop from few overwintering eggs are at greater risk from natural enemies than are large ones. Intraspecific competition still slowed population increase, because most aphids remained crowded on the few originally colonized twigs. Such populations produced very few emigrant alatae before they were exterminated by the combination of T. angelicae with specific and non-specific predators. Adult Cantharidae killed many of the aphids, especially in hedgerow habitats, where they were abundant. Coccinellidae, Anthocoridae and syrphid larvae, and the adults of nonspecific predators, notably Cantharidae, prevented recolonization of E. europaeus throughout July and August. Leaves of E. europaeus may remain physiologically suitable for A. fabae throughout July but begin to deteriorate in August when A. fabae kept on them become less fecund. Experiments using exclusion techniques provided evidence that natural enemies which attack A. fabae on E. europaeus and on summer hosts cause the common 2-year cycle of aphid abundance. Individual E. europaeus differ consistently in the extent to which they are colonized by A. fabae. Conditions are discussed that should govern the choice of E. europaeus bushes on which the A. fabae populations can be used as sensitive indicators of later crop infestations.     

Does pirimicarb affect the voracity of the euriphagous predator, Coccinella undecimpunctata L. (Coleoptera: Coccinellidae)?

Pirimicarb is considered a selective and effective insecticide for the control of aphids and whiteflies. Coccinella undecimpunctata L. is a euriphagous predator autochthonous to the Azores, which feeds preferentially on aphids. The voracity of 4th instars and adults (males and females) of C. undecimpunctata using Aphis fabae Scopoli or Aleyrodes proletella L. as preys was evaluated in laboratory, as well as the impact of pirimicarb on the feeding performance using A. fabae as prey. In the absence of chemical treatment and when the prey was A. proletella, satiation lower limits were estimated on a density of 200 individuals in a 24-h period, for 4th instars, adult females and males of C. undecimpunctata. With A. fabae, satiation was attained when 200, 150 and 100 aphids were provided to 4th instars, adult females and males, respectively. C. undecimpunctata exhibited a type II functional response for both prey species. Fourth instars displayed a lower handling time than the adults; handling times of the adults where higher when A. fabae was the prey and attack rates were sex-dependent, that is, attack rate of females was higher on A. fabae while of males was higher on A. proletella. Voracity of C. undecimpunctata was not significantly affected by pirimicarb; therefore, the use of this insecticide can constitute a complementary component for the integrated management of A. fabae.     

Biological traits and life table parameters of variegated lady beetle, <Emphasis Type="Italic">Hippodamia variegata</Emphasis> (Coleoptera: Coccinellidae) on three aphid species

The aphidophagous ladybird beetle, Hippodamia variegata (Goeze) (Coleoptera: Coccinellidae), is a dominant predator in various crop systems. Its life history was studied when fed on three aphid prey, viz. Aphis gossypii Glover, Aphis fabae Scopoli and Macrosiphum rosae (L.), under laboratory conditions, 25 ± 1 °C, 65 ± 5 % RH and a photoperiod of 16L:8D. The immature development period was shortest (15.2 days) when A. gossypii was used as prey and longest (18.9 days) on A. fabae. Adult coccinellids had the shortest longevity on A. fabae (64.8 days). The higher and lower mean daily fecundity was recorded for A. fabae (12.4 eggs) and M. rosae (6.2 eggs), respectively. The highest (291.0 eggs) and lowest (183.2 eggs) net reproduction rates (R ₀) were observed on A. fabae and M. rosae, respectively. Mean generation time (T) on rose aphid was significantly longer (33.4 days) than on the two other preys. The intrinsic rate of increase (r _m) was affected by the R ₀ value, and it was highest on A. fabae (0.183) and lowest on M. rosae (0.156). Based on r _m as an index of suitability of prey species, A. fabae was the most suitable prey for H. variegata. Our finding may provide basic information for developing aphid biological control programs.     

Application of benzothiadiazole and Trichoderma harzianum to control faba bean chocolate spot disease and their effect on some physiological and biochemical traits

Chocolate spot disease is the most prevalent and important disease in the major faba bean growing regions in the world. Different concentrations of the abiotic inducer (0.3 and 0.5 mM benzothiadiazole) and the biotic inducer (1 × 10⁷ and 2 × 10⁷ spore/ml Trichoderma harzianum) were used alone or in combination to study their efficiency against faba bean chocolate spot disease caused by Botrytis fabae and Botrytis cinerea and their effect on some chemical analyses (phenylalanine ammonia lyase activity, total flavonoids and peroxidase isozymes, pectin and lignin content and total chlorophyll content). Application of the tested inducers as foliar treatment significantly reduced the severity of chocolate spot disease as compared with untreated infected plants. The reduction in disease severity was associated with a gradual increase in phenylalanine ammonia lyase activity. Maximum increase was recorded at 72 h after inoculation with B. fabae and B. cinerea. In addition, the levels of flavonoids in induced infected leaves recorded a sharp increase at 24 h after inoculation with B. fabae or B. cinerea. Also, pectin and lignin contents in the cell wall of induced infected plants were significantly increased as compared with untreated infected plants. Beside the induction of resistance, the tested inducers markedly increased total chlorophyll content in treated infected plants as compared with untreated infected plants. Isozymes analysis revealed that new peroxidase bands were induced only in treated faba bean leaves in response to infection with B. fabae or B. cinerea.     

Mate recognition in the Aphis fabae complex: daily rhythm of release and specificity of sex pheromones

The two subspecies of the host-alternating black bean aphid, Aphis fabae Scopoli, used in this study have different secondary host plants but reproduce sexually in autumn on the same host plant, spindle, Euonymus europaea L. In both Aphis fabae fabae Scopoli and A. f. solanella Theobald the percentage of adult mating females (oviparae) calling (releasing sex pheromone) each day increased with age up to day 8. During the course of a day the mating females of A. f. solanella called most actively early in the morning and then showed a gradual decrease in calling activity. In contrast, few A. f. fabae called early in the day and were most active around midday, after which the incidence of calling decreased slightly, with 50% still calling in the evening. In both taxa the activity of the males in the absence of mating females paralleled the calling activity of their respective females. In an olfactometer, males showed a marked preference for the sex pheromone released by conspecific females over that of the other subspecies and did not respond to the odour of spindle. Thus, as in the other species of aphids there are specific mate recognition systems in A. f. fabae and A. f. solanella, which are likely to reduce the incidence of hybridisation.     

Suitability of Aphis fabae, Myzus persicae (Homoptera: Aphididae) and Aleyrodes proletella (Homoptera: Aleyrodidae) as prey for Coccinella undecimpunctata (Coleoptera: Coccinellidae)

The suitability of Aphis fabae Scopoli, Myzus persicae Sulzer and Aleyrodes proletella L. as food sources for Coccinella undecimpunctata L. was evaluated by studying the impact of prey consumption on the predator’s population growth parameters and feeding parameters. Unlike A. proletella, A. fabae and M. persicae supported the development and reproduction of C. undecimpunctata. A. fabae and M. persicae were considered to be essential prey, whereas A. proletella was considered to be an alternative prey. Aphid species showed different degrees of suitability: M. persicae significantly decreased the pre-oviposition period and increased adult longevity, fecundity and fertility compared with A. fabae. Moreover, A. fabae represents a suitable diet for larval development, but is not a suitable food source for adult reproduction. The predator’s population growth parameters, R₀, r_m and λ were increased with M. persicae, whereas T decreased. We found that the 4th instar larvae were the most voracious, particularly when fed on M. persicae; nevertheless, with this prey daily weight gain and feeding efficiency of 4th instar larvae were similar to that of individuals fed with A. fabae.     

Larval aggregations of the blister beetle Stenoria analis (Schaum) (Coleoptera: Meloidae) sexually deceive patrolling males of their host,the solitary bee Colletes hederae Schmidt & Westrich (Hymenoptera: Colletidae)

We here report on observations on the parasitism of the solitary bee Colletes hederae Schmidt & Westrich (Hymenoptera: Colletidae) by triungulins (first instar larvae) of the European beetle Stenoria analis (Schaum) (Coleoptera: Meloidae). Our observations carried out in western France provide behavioural evidence that patrolling males of C. hederae hover in front of, and are strongly drawn to, larval aggregations of S. analis in a manner reminiscent of approaching flights to emerging, conspecific females. Not only were the male bees strongly attracted to clusters of newly hatched triungulins, but they also attempted copulation (i.e., pseudocopulation) with the latter, which regularly resulted in small groups of triungulins being transferred onto the thorax of the male bees. Decent-sized groups of triungulins were exclusively found on the thorax of male bees, which suggests that triungulins of S. analis lure only males of the targeted host species, presumably by mimicking the female pheromonal cues of C. hederae. This is to our knowledge the first record of this kind of interaction for the whole West-Palaearctic, and only the second account on sexual deception between blister beetles and wild bees described to date.