Stylet activities and potato virus Y vector efficiencies by the aphids Brachycaudus helichrysi and Drepanosiphum platanoidis

Stylet penetration activities of two aphid species were recorded electrically and compared with their efficiency of potato virus Y transmission. B. helichrysi (Kltb.) acquired the virus during 15% of single penetrations on infected leaves. These acquisitions were associated with the occurrence of cell membrane puncture by stylets, recorded during 44% of the penetrations. D. platanoidis (Schrank) punctured membranes during only 8% of penetrations, and its acquisition efficiency was less than 1%. The frequency with which aphids puncture cell membranes appears to partially determine their vector efficiency.     

FACTORS AFFECTING THE SPREAD OF APHID-BORNE VIRUSES IN POTATO IN EASTERN SCOTLAND: I. OVERWINTERING OF POTATO APHIDS, PARTICULARLY MYZUS PERSICAE (SULZER)

Three species of potato aphids, Myzus persicae (Sulzer), Macrosiphum euphorbiae (Thomas) and Aulacorthum solani (Kltb.), overwinter in eastern Scotland, primarily as apterae on perennial, glasshouse, frame and brassica crops. Brassica crops are the commonest hosts of overwintering Myzus persicae , the principal vector of potato leaf roll and Y viruses, and these crops are concentrated in the market-gardening areas of the Lothians and Moray. Although crops of savoy cabbage and brussels sprout often carried numerous M.persicae during the winter, spring cabbage, cabbage for seed and broccoli seem the most important overwintering hosts because they usually persist until mid-May, long enough to allow the development and dispersal of alatae to spring-planted crops. Many alatae dispersed during July and August from crops colonized in spring. Although M. persicae overwintered as eggs on peach and viviparously on plants in glasshouses, the influence of such sites, which are generally distributed throughout the main seed-potato growing areas of Angus, Perth and Fife, was local and unless numerous M. persicae survive the winter on weeds, the market-garden area of the Lothians is probably the most important source from which this aphid disperses in spring and early summer to colonize potato crops in eastern Scotland.     

FACTORS AFFECTING THE SPREAD OF APHID-BORNE VIRUSES IN POTATO IN EASTERN SCOTLAND: II. INFESTATION OF THE POTATO CROP BY POTATO APHIDS, PARTICULARLY MYZUS PERSICAE (SULZER)

Surveys in the years 1954-56 showed that potato crops in most districts of eastern Scotland were infested by the aphids Myzus persicae (Sulz.), Macrosiphum euphorbiae (Thomas) and Aulacorthum solani (Kltb.). Crops in different districts became infested by Myzus persicae at different times and to different extents, and these differences seemed consistent between years. Crops in the Edinburgh area were colonized between mid-May and mid-June, whereas crops in north Perthshire escaped infestation until the end of July or mid-August. The time and degree of infestation by M. persicae seems correlated with distance from sites where this aphid overwinters. Trap records show that many alate M. persicae disperse from outdoor brassica and early potato crops in the Edinburgh area between mid-July and mid-August, a period during which potato crops in Fife, Angus and Perthshire usually become infested. The freedom of crops in the better seed-producing areas from widespread infection by potato leaf roll and Y viruses is probably associated with lateness of aphid infestation rather than scarcity of aphid vectors.     

Quantitative studies on the uptake and retention of potato leafroll virus by aphids in laboratory and field conditions

Enzyme-linked immunosorbent assay (ELISA) was adapted for the efficient detection and assay of potato leafroll virus (PLRV) in aphids. Best results were obtained when aphids were extracted in 0.05 M phosphate buffer, pH 7.0, and the extracts incubated at 37 °C for 1 h before starting the assay. Using batches of 20 green peach aphids (Myzus persicae), about 0.01 ng PLRV/aphid could be detected. The virus could also be detected in single aphids allowed a 1-day acquisition access period on infected potato leaves. The PLRV content of aphids depended on the age of potato source-plants and the position of source leaves on them. It increased with increase in acquisition access period up to 7 days but differed considerably between individual aphids. A maximum of 7 ng PLRV/aphid was recorded but aphids more usually accumulated about 0.2 ng PLRV per day. When aphids were allowed acquisition access periods of 1–3 days, and then caged singly on Physalis floridana seedlings for 3 days, the PLRV content of each aphid, measured subsequently, was not strongly correlated with the infection of P. floridana. The concentration of PLRV in leaf extracts differed only slightly when potato plants were kept at 15, 20, 25 or 30 °C for 1 or 2 wk, but the virus content of aphids kept on leaves at the different temperatures decreased with increase of temperature. PLRV was transmitted readily to P. floridana at all temperatures, but by a slightly smaller proportion of aphids, and after a longer latent period, at 15 °C than at 30 °C. The PLRV content of M. persicae fed on infected potato leaves decreased with increasing time after transfer to turnip (immune to PLRV). The decrease occurred in two phases, the first rapid and the second very slow. In the first phase the decrease was faster, briefer and greater at 25 and 30 °C than at 15 and 20 °C. No evidence was obtained that PLRV multiplies in M. persicae. These results are compatible with a model in which much of the PLRV in aphids during the second phase is in the haemocoele, and transmission is mainly limited by the rate of passage of virus particles from haemolymph to saliva. The potato aphid, Macrosiphum euphorbiae, transmitted PLRV much less efficiently than M. persicae. Its inefficiency as a vector could not be ascribed to failure to acquire or retain PLRV, or to the degradation of virus particles in the aphid. Probably only few PLRV particles pass from the haemolymph to saliva in this species. The virus content of M. euphorbiae collected from PLRV-infected potato plants in the field increased from early June to early July, and then decreased. PLRV was detected both in spring migrants collected from the plants and in summer migrants caught in yellow water-traps. PLRV was also detected in M. persicae collected from infected plants in July and August, and in trapped summer migrants, but their PLRV content was less than that of M. euphorbiae, and in some instances was too small for unequivocal detection.     

THE EFFECT OF DIFFERENT HOST PLANTS OF POTATO VIRUS C IN DETERMINING ITS TRANSMISSION BY APHIDS

A stock of potato virus C derived from Edgecote Purple potatoes in 1945 was not then transmitted by aphids, although more than 2000 aphids were used in conditions optimal for transmitting the serologically related potato virus Y. This stock of virus C has been propagated continuously since, by manual inoculation in a series of Nicotiana glutinosa and N. tabacum , and in 1955 it was transmitted by the aphid Myzus persicae (Sulz.): about one in twenty of the aphids transmitted it compared with one in two for potato virus Y.
Virus C derived from the Edgecote Purple potatoes in 1955 was not transmitted by aphids; both stocks of virus C produced only local lesions in Majestic potato leaves, and gave similar symptoms in tobacco.
When inoculated to Majestic potatoes and then returned to tobacco plants, potato virus C usually ceased to be aphid transmitted and did not recover this property in any of the subsequent subcultures.
Transmission from stock by aphids did not isolate a strain of virus C which was any more readily transmitted by aphids, indeed, for the first two or three subcultures, aphids usually transmitted more readily from plants inoculated manually. But the few isolates which remained aphid transmissible, after a second passage through potato, were rather readily transmitted.
These results suggest that the ability of a virus to be aphid transmitted is, at least in part, determined by the host plant in which it is multiplying, but the nature of the changes which determine this ability are unknown.     

THE SPREAD OF VIRUS DISEASES TO SINGLE POTATO PLANTS BY WINGED APHIDS

Young potato plants in pots exposed in the open near plots of potatoes for limited periods at intervals during the summer, became infested with large numbers of winged aphids only during warm, calm and dry weather. Although visited by aphids during May and June, when much of the spread of viruses occurred in nearby potato crops, few of the potted plants became infected. Most potted plants became infected in July when alate aphids were leaving neighbouring potato crops. Widely different proportions of the exposed plants became infected in different years; in two of the three years, many more plants were infected with virus Y than with leaf roll virus.     

Shoot-feeding Aphids Promote Development of Gremmeniella abietina, the Fungal Pathogen Causing Scleroderris Canker Disease in Conifers

We tested experimentally whether shoot feeding aphids Cinara pinea (Mordv.) can promote the development of Gremmeniella abietina (Lagerb.) Morelet, a fungus which causes Scleroderris canker disease in conifers. Pine seedlings were infested with aphids at two different times, and subsequently inoculated with conidia of G. abietina at two different times. The degree of infestation was classified into three groups based on the number of aphids/seedling: none, one (low level), and three (high level). Because of parthenogenetic reproduction, the number of aphids increased during the summer, so we also used aphid numbers to explain the development of the symptoms. Necrosis caused by G. abietina was more prevalent in seedlings infested by aphids in June, and inoculated with fungus in July. Expressed as percents of the total length of the shoots, the necrosis had advanced 50%, 70%, and 95% with no, low, and high aphid levels, respectively. Canker formation was significantly greater when G. abietina conidia were inoculated in July, compared to August. In August, there were no statistically significant differences in the intensity of disease between aphid infestation levels, but the mean number of aphids was related to disease intensity. In the spring following infection, seedlings with aphids had more dead and fewer healthy terminal buds compared to seedlings without aphids.     

Methods of Recording Aphid Populations for Use in Research on Potato Virus Diseases

Methods of counting aphids infesting potato crops are reviewed and discussed. The results of an aphid survey in different parts of England during 1946 and of counts at Rothamsted during 1947 are given and used to illustrate methods of expressing the counts; the extent of virus spread in 1946 showed no close correlation with aphid numbers. It is concluded that an estimate of the number of aphids per plant is better for virus disease research than the number per 100 leaves. A method of estimating the number of aphids per plant with tolerable accuracy is described, but it is concluded that for most surveys a method which does not necessitate the counting of the aphids is adequate. Such a method, based on the percentage of leaves infested, is described.     

The effects of temperature on the availability and acquisition of potato leafroll luteovirus by Myzus persicae

The concentration of potato leafroll luteovirus (PLRV) did not differ in potato plants with secondary infections grown at 15°C or 27°C. Detached leaves of plants grown at 15°C or 27°C were used as sources of PLRV for peach-potato aphids (Myzus persicae Sulz.) both at 15°C and 27°C. At comparable temperature during virus acquisition, aphids which fed on leaves of plants kept previously at 15°C contained more viral antigen detected by ELISA than aphids which fed on leaves of plants grown at 27°C. The aphids which acquired PLRV at 27°C contained evidently more viral antigen than those which acquired PLRV at 15°C. The greatest amount of PLRV was found in the aphids which acquired the virus at 27°C from the leaves of plants kept at 15°C. The ability of M. persicae to transmit PLRV to Physalis ftoridana Rydb. generally decreased with decrease in the amount of PLRV in vectors.     

QUANTITATIVE STUDIES ON THE TRANSMISSION OF CABBAGE BLACK RING SPOT VIRUS BY MYZUS PERSICAE (SULZ.)

Factors affecting the transmission of cabbage black ring spot virus by Mysus persicae (Sulz.) were studied quantitatively using the local lesions produced on tobacco leaves. Aphids prevented from feeding for 15 min. or more, before feeding for a few minutes on an infected plant, caused more infections than unfasted aphids. Fasted aphids acquired virus from infected plants in feeding times as short as 10 sec., and infected healthy plants in test-feeding times of 5 sec. Increasing test-feeding times to 30 min. increased the numbers of infections. Increasing infection- feeding times from 10 sec. to 5 min. had little effect, but increasing to more than 5 min. greatly reduced the number of transmissions. This reduction was partly offset if the aphids were prevented from feeding continuously while on the infected plants. With undisturbed infection-feeding periods of 15 min. or longer, previously fasted aphids caused no more infections than unfasted aphids.
Infective aphids lost their ability to produce lesions more rapidly when feeding than when fasting.
Winged and wingless aphids were equally efficient vectors.     

Seasonal Phenology and Species Composition of the Aphid Fauna in a Northern Crop Production Area

Background

The species diversity of aphids and seasonal timing of their flight activity can have significant impacts on crop production, as aphid species differ in their ability to transmit plant viruses and flight timing affects virus epidemiology. The aim of the study was to characterise the species composition and phenology of aphid fauna in Finland in one of the northernmost intensive crop production areas of the world (latitude 64°).

Methodology/Principal Findings

Flight activity was monitored in four growing seasons (2007–010) using yellow pan traps (YPTs) placed in 4–8 seed potato fields and a Rothamsted suction trap. A total of 58,528 winged aphids were obtained, identified to 83 taxa based on morphology, and 34 species were additionally characterised by DNA barcoding. Seasonal flight activity patterns analysed based on YPT catch fell into three main phenology clusters. Monoecious taxa showed early or middle-season flight activity and belonged to species living on shrubs/trees or herbaceous plants, respectively. Heteroecious taxa occurred over the entire potato growing season (ca. 90 days). Abundance of aphids followed a clear 3-year cycle based on suction trap data covering a decade. Rhopalosiphum padi occurring at the end of the potato growing season was the most abundant species. The flight activity of Aphis fabae, the main vector of Potato virus Y in the region, and Aphis gossypii peaked in the beginning of potato growing season.

Conclusions/Significance

Detailed information was obtained on phenology of a large number aphid species, of which many are agriculturally important pests acting as vectors of plant viruses. Aphis gossypii is known as a pest in greenhouses, but our study shows that it occurs also in the field, even far in the north. The novel information on aphid phenology and ecology has wide implications for prospective pest management, particularly in light of climate change.     

Response of potato aphid (Homoptera: Aphididae) to synthetic potato-derived Colorado potato beetle (Coleoptera: Chrysomelidae) attractant and natural potato odor

A recently synthesized kairomone blend, based on the volatiles produced by potato (Solanum spp.) plants, has been demonstrated to be attractive to both adult and larval stages of the Colorado potato beetle, Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae). It was subsequently formulated in a viscous inert carrier for field applications and showed potential for aggregating beetles in treated areas of the field. We investigated effects of this kairomone formulation on the potato aphid, Macrosiphum euphorbiae (Thomas) (Homoptera: Aphididae). The response of both winged and wingless adults to natural potato foliage and synthetic kairomone was tested in a Y-tube olfactometer. Aphid response to untreated potato foliage, foliage treated with the kairomone blend, and foliage treated with blank inert carrier also was tested in petri dishes. In addition, aphid densities on field plots treated with kairomone and blank inert carrier were compared with the control plots. The untreated potato foliage was found to be attractive to wingless, but not winged, potato aphids. In the olfactometer, the foliage treated with synthetic Colorado potato beetle kairomone was not attractive to either winged or wingless aphids. In petri dishes, aphids avoided leaflets treated with both kairomone formulation and its blank carrier. There was no statistical difference between any treatments compared in the field.     

Canopy development of a determinate and an indeterminate cultivar of Vicia faba L. under contrasting plant distributions and densities

Field experiments were conducted in 1987 and 1988 to quantify differences in canopy formation between an indeterminate and a determinate genotype of Vicia faba L., grown at two plant densities and three spatial distributions. The number of stems per unit area produced by determinate plants was related to the growth rate before flowering. Leaf production per stem per unit of thermal time was similar in both plant types, but twice as many leaves per stem were produced by the indeterminate cultivar. The indeterminate cultivar produced fewer and smaller leaves in the warmer and drier weather of 1988 than in 1987. The determinate genotype produced similar sizes and numbers of leaves in both years, but fewer tillers developed in 1988 than in 1987. Accordingly, leaf mass per unit ground area was greater in 1987 than in 1988 in both genotypes. Except during early flowering, relationships between leaf mass and leaf area were constant, with higher specific leaf areas in the determinate than the indeterminate genotype. Shoot dry matter partitioning into leaves was identical in both years for indeterminate plants, but differed in determinate ones.
It is concluded that canopy development is regulated through individual leaf weight and leaf number per stem in non-tillering indeterminate, and by stem numbers per unit area in tillering determinate plants.     

Effect of host-plant manipulation by a gall-inducing insect on abundance of herbivores on chestnut trees

We investigated plant-mediated effects of the stem gall wasp, Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae), on other herbivores on the chestnut tree Castanea crenata. In the early season, leaves emerged earlier and in greater numbers on galled shoots than on ungalled shoots. On galled shoots the leaf to shoot biomass ratio was lower and the leaves were physically different. In May and June the concentration of nitrogen in leaves was higher on galled shoots than on ungalled shoots. In July, the water content of leaves was lower on galled shoots. In May and June, the number of aphids, Myzocallis kuricola Matsumura (Homoptera: Aphidoidea), on leaves was higher on galled shoots than on ungalled shoots, but the opposite was true at the end of July. Laboratory experiments showed that aphid fecundity and body weight decrease were higher in May and June when aphids fed on leaves on a galled shoot than when they fed on those on ungalled shoots. In contrast, aphid performance in July was greater on ungalled leaves than on galled leaves. Our findings suggest that gall initiation in a chestnut tree affected aphid performance by affecting host plant quality.     

The role of refuge areas in the phenology of Rhopalosiphum padi in low rainfall cropping areas of South Australia

Extensive surveys of possible aphid habitats in South Australia indicated that irrigated perennial grass pastures in the Mount Lofty Ranges and Lower Murray Valley were summer refuges for Rhopalosiphum padi (L.) (Hemiptera: Aphididae). Large numbers of aphids build up in these pastures each year during autumn (April and May) with numbers peaking in May. The size of the May peak was related to the number of aphids surviving the summer. The proportions of alates were highest in May and August/September. Both peaks coincided with a photoperiod of between 11.2 and 11.5 h, and partial correlations suggested that aphid density, photoperiod and temperature were all significant determinants of alate production.     

The effect of parasitism by Aphelinus abdominalis and drought on the walking movement of aphids

The effect of simulated plant stress and parasitism by Aphelinus abdominalis (Dalman) on the mobility of four species of aphids was investigated. The aphids were placed on water stressed potted plants or on excised leaf segments on dry or moist filter-paper in Petri dishes. Winter wheat (Triticum aestivum) was infested with Metopolophium dirhodum (Walker), Sitobion avenae (F.) and Rhopalosiphum padi (L.) (segments only), aubergine (Solanum melongena) leaf segments with Macrosiphum euphorbiae (Thomas). The aphids that moved off the plants were removed and their development stage determined at 24-h (drought-stressed plants) or 3-h (leaf segments) intervals. On intact plants, aphid larvae were reluctant to move, and only moved after moulting into adults. On cut leaves, young 1st and 2nd instar larvae were more reluctant to move than 3rd and 4th instar larvae and adults. The numbers moving were initially positively correlated with aphid population density, and in M. euphorbiae occurred mainly during the night. Depending on aphid species and parasitoid age, parasitism by A. abdominalis retarded or accelerated movement, but the differences between young and old larvae and adults persisted after parasitism. A. abdominalis lays male eggs in small hosts and female eggs in large hosts. Consequently, its sex ratio was affected by differential movement of the host aphids of the male and female parasitoids. Old larvae and adult aphids readily moved and carried off female parasitoids, while the small aphids were more likely to remain and give rise to male-biased sex ratios.     

Seasonal occurrence and relative abundance of aphids on potato plants with classical and transgenic characters of resistance to Colorado potato beetle Leptinotarsa decemlineata (Say)

The seasonal abundance and dynamics of potato-infesting aphids were studied in two seasons, on potato Solanum tuberosum L. with various types of transgenic and classical resistance to primary pests, especially the Colorado potato beetle (CPB), Leptinotarsa decemlineata (Say). The lines tested were the NewLeaf potato, a transgenic expressing the Bacillus thuringiensis CryIIIA toxin (BTT); NYL 235-4 a parental line derived from S. berthaultii (NYL) with a high density of glandular trichomes; and a transgenic line expressing oryzacystatln I (OCI), a proteinase inhibitor gene from rice; potatoes from two commercial cultivars, Superior and Kennebec, served as controls. Over the two seasons, Macrosiphum euphorbiae (Thomas) and, to a lesser extent, Myzus persicae (Sulzer) were by far the most abundant aphids observed in the experimental plots. M. persicae was observed relatively late in the season, and was most abundant on the Kennebec-OCI potato. Macrosiphum euphorbiae was more regular over seasons, and its highest densities were observed on the NYL 235-4 line. The population of M. euphorbiae showed markedly different patterns on the five lines studied, which was clearly related to potato plant phenology. Density of M. euphorbiae was observed on the NYL 235-4 line, in late July and early August.     

SOME EFFECTS OF HOST NUTRITION ON THE SUSCEPTIBILITY OF PLANTS TO INFECTION BY CERTAIN VIRUSES

Fertilizer treatments that greatly influenced the growth of tobacco and potato plants in pots had little effect on the number that became infected with potato virus Y when the plants were colonized by equal numbers of infective aphids, though the number was slightly decreased by nitrogen and increased by phosphorus.
The number of local lesions produced on leaves of tobacco and Nicotiana glutinosa by tomato aucuba mosaic and tobacco mosaic viruses was increased by additions of both nitrogen and phosphorus, provided that these also increased growth. The predominant effect of both nutrients in increasing susceptibility was indirect by increasing plant size, but over certain critical ranges both elements also increased the numbers of lesions produced per unit leaf area. Conditions of maximum susceptibility approximated closely to those producing optimal growth, and susceptibility, whether measured by lesions per half-leaf or per unit area, was decreased by a deficiency or excess of either element. Sometimes the addition of nitrogen reduced susceptibility when still increasing plant growth.     

Effects of growth regulators, CCC and B9, on some potato varieties

The effects of CCC and B 9 on the growth habit of potato differed between varieties. CCC diminished stem lengths and dry weight more than Bo because CCC was applied early when shoots emerged from the soil, but B 9 was applied about 3 weeks later when several leaves had formed. In some varieties lateral stem growth was increased by treatment and in others decreased. There was an inverse relation between main stem and lateral stem growth so that varieties with vigorous main stem growth had poor lateral growth and vice-versa. Treatment with the growth-regulators diminished leaf dry weight of main stem leaves less than leaf area, but the degree of magnitudes of the changes depended on the variety. Both regulators lessened net assimilation rate. Net assimilation rate and dry matter per unit area of leaf were inversely related, possibly because accumulation of substances in leaves decreases photosynthesis. Stolon dry weight was positively correlated with main stem leaf area. There was a direct relation between stem length and tuber dry weight, suggesting that tuber initiation occurs at different stem lengths in different varieties. Tubering was earliest in Epicure and latest in King Edward. Epicure had the greatest tuber weight and smallest stem length.