Distribution and population development of Nasonovia ribisnigri (Homoptera: Aphididae) in iceberg lettuce

A field study was conducted to determine the distribution and development of aphid Nasonovia ribisnigri (Mosley) (Homoptera: Aphididae) populations in iceberg lettuce, Lactuca sativa L. 'Salinas'. Lettuce plants were transplanted and caged individually in the field and inoculated with apterous N. ribisnigri at 0, 1, 2, 3, and 4 wk after transplanting in spring and fall 2002. Plants were harvested 15-50 d after inoculations; numbers of alates and apterous N. ribisnigri were counted or estimated on each leaf for each plant. Inoculations during all 5 wk of plant development resulted in successful colonization of lettuce heads. Results indicated that head formation did not reduce the risk of colonization by N. ribisnigri to iceberg lettuce; plants were susceptible to colonization by N. ribisnigri throughout their development. For later inoculations, N. ribisnigri populations were relatively smaller, and aphids were found mostly within the heads. For earlier inoculations, N. ribisnigri populations were larger, and within-plant distributions shifted toward frame leaves. The shift of population distributions toward frame leaves correlated significantly with increases in N. ribisnigri population density. For most inoculations, more aphids were present on wrapper leaves than on other leaves. The proportion of alates did not vary significantly with population density. Population development of N ribisnigri also correlated significantly with heat unit accumulation. Yellow sticky cards were used to monitor alates in each cage. Catches of N. ribisnigri alates on yellow sticky cards were significantly correlated with total numbers of alates as well as with total population sizes on individual lettuce plants.     

Oxygenated phosphine fumigation for control of Nasonovia ribisnigri (Homoptera: Aphididae) on harvested lettuce

Low temperature regular phosphine fumigations under the normal oxygen level and oxygenated phosphine fumigations under superatmospheric oxygen levels were compared for efficacy against the aphid, Nasonovia ribisnigri (Mosley), and effects on postharvest quality of romaine and head lettuce. Low temperature regular phosphine fumigation was effective against the aphid. However, a 3 d treatment with high phosphine concentrations of > or = 2,000 ppm was needed for complete control of the aphid. Oxygen greatly increased phosphine toxicity and significantly reduced both treatment time and phosphine concentration for control of N. ribisnigri. At 1,000 ppm phosphine, 72 h regular fumigations at 6 degrees C did not achieve 100% mortality of the aphid. The 1,000 ppm phosphine fumigation under 60% O2 killed all aphids in 30 h. Both a 72 h regular fumigation with 2,200 ppm phosphine and a 48 h oxygenated fumigation with 1,000 ppm phosphine under 60% O2 were tested on romaine and head lettuce at 3 degrees C. Both treatments achieved complete control of N. ribisnigri. However, the 72 h regular fumigation resulted in significantly higher percentages of lettuce with injuries and significantly lower lettuce internal quality scores than the 48 h oxygenated phosphine fumigation. Although the oxygenated phosphine fumigation also caused injuries to some treated lettuce, lettuce quality remained very good and the treatment is not expected to have a significant impact on marketability of the lettuce. This study demonstrated that oxygenated phosphine fumigation was more effective and less phytotoxic for controlling N. ribisnigri on harvested lettuce than regular phosphine fumigation and is promising for practical use.     

Responses of Nasonovia ribisnigri (Homoptera: Aphididae) to susceptible and resistant lettuce

Nymphs and alates of aphid Nasonovia ribisnigri (Mosley) (Homoptera: Aphididae) were tested on 10 lettuce cultivars with N. ribisnigri resistance gene Nr and 18 cultivars without the resistance gene in various bioassays. Bioassays used whole plants, leaf discs, or leaf cages to determine susceptibility of commercial lettuce cultivars to N. ribisnigri infestation and to evaluate screening methods for breeding lettuce resistance to N. ribisnigri. Resistant and susceptible plants were separated in 3 d when using whole plant bioassays. Long-term (> or =7 d) no-choice tests using leaf cages or whole plants resulted in no survival of N. ribisnigri on resistant plants, indicating great promise of the Nr gene for management of N. ribisnigri. Effective screening was achieved in both no-choice tests where resistant or susceptible intact plants were tested separately in groups or individually and in choice tests where susceptible and resistant plants were intermixed. Leaf discs bioassays were not suitable for resistance screening. All lettuce cultivars without the resistance gene were suitable hosts for N. ribisnigri, indicating the great importance of this pest to lettuce production and the urgency in developing resistant lettuce cultivars to manage N. ribisnigri.     

Prevalence of Pandora neoaphidis (Zygomycetes: Entomophthorales) infecting Nasonovia ribisnigri (Hemiptera: Aphididae) on lettuce crops in Argentina

Lettuce crops, Lactuca sativa, organically produced in La Plata, Argentina, were sampled in order to determine the prevalence of fungal diseased aphids. Nasonovia ribisnigri was the only aphid detected and its occurrence was highly variable. The fungal pathogen Pandora neoaphidis (Entomophthoromycotina: Entomophthorales) was the only pathogen detected. We recorded a maximum of 34.2 aphids per plant and the highest rate of fungal prevalence was 56.6% (n = 30) (aphids infected/total aphids). Infected aphids were observed in all sampling sites. No differences of infection rates were detected between the center and the edge of crops. Host density was an important factor determining infection. The majority of host population was comprised of nymphs which were the most infected in terms of individuals per habitat unit (lettuce plant), but considering the proportion of infected aphids per stage of development, the prevalence of infection in nymphs and adults was similar.     

Mechanisms of insecticide resistance in the aphid Nasonovia ribisnigri (Mosley) (Homoptera: Aphididae) from France.

Nasonovia ribisnigri, a main pest of salad crops, has developed resistance to various insecticides in southern France, including the carbamate pirimicarb and the cyclodiene endosulfan, two insecticides widely used to control this aphid. Here we have investigated the mechanisms of resistance to these two insecticides by studying cross-resistance, synergism, activity of detoxifying enzymes, and possible modifications of the target proteins. Resistance to pirimicarb was shown to be mainly due to a decreased sensitivity of the target acetylcholinesterase; this modification conferred also, resistance to propoxur but not to methomyl and the two tested organophosphates (acephate and paraoxon). Endosulfan resistance was associated with a moderate level of resistance to dieldrin, and resistance to both insecticides was due, in part, to increased detoxification by glutathione S-transferases (GST). The endosulfan resistant strain displayed the same amino acid at position 302 of the Rdl gene (GABA receptor) as susceptible aphids (e.g. Ala), indicating that the Ala to Ser (or to Gly) mutation observed among dieldrin resistant strains of other insect species was not present.     

Temperature thresholds and thermal requirements for development of Nasonovia ribisnigri (Hemiptera: Aphididae)

Early detection of Nasonovia ribisnigri (Mosley) (Hemiptera: Aphididae) on lettuce is of primary importance for its effective control. Temperature thresholds for development of this pest were estimated using developmental rates [r(T)] at different constant temperatures (8, 12, 16, 20, 24, 26, and 28 degrees C). Observed developmental rates data and temperature were fitted to two linear (Campbell and Mu?iz and Gil) and a nonlinear (Lactin) models. Lower temperature threshold estimated by the Campbell model was 3.6 degrees C for apterous, 4.1 degrees C for alates, and 3.1 degrees C for both aphid adult morphs together. Similar values of the lower temperature threshold were obtained with the Mu?iz and Gil model, for apterous (4.0 degrees C), alates (4.2 degrees C), and both adult morphs together (3.7 degrees C) of N. ribisnigri. Thermal requirements of N. ribisnigri to complete development were estimated by Campbell and Mu?iz and Gil models for apterous in 125 and 129 DD and for both adult morphs together in 143 and 139 DD, respectively. For complete development from birth to adulthood, the alate morph needed 15-18 DD more than the apterous morph. The lower temperature threshold determined by the Lactin model was 5.3 degrees C for alates, 2.3 degrees C for apterous, and 1.9 degrees C for both adult morphs together. The optimal and upper temperature thresholds were 25.2 and 33.6 degrees C, respectively, for the alate morph, 27 and 35.9 degrees C, respectively, for the apterous morph, and 26.1 and 35.3 degrees C, respectively, for the two adult morphs together. The Campbell model provided the best fit to the observed developmental rates data of N. ribisnigri. This information could be incorporated in forecasting models of this pest.     

Laboratory and semi-field evaluation of Beauveria bassiana (Ascomycota: Hypocreales) against the lettuce aphid,Nasonovia ribisnigri (Hemiptera: Aphididae)

The lettuce aphid, Nasonovia ribisnigri (Mosley), is an economically important pest of lettuce worldwide. The entomopathogenic fungus Beauveria bassiana strain GHA has recently been reported as a potential biocontrol candidate for use against the lettuce aphid. This study provides information on the mortality inflicted by B. bassiana when applied against different life stages of the lettuce aphid under laboratory conditions and how fungus infection affects the aphid fecundity. In addition, temporal changes in persistence of fungus inoculum applied to foliage of young lettuce plants under semi-field conditions was analysed. Immature life stages were generally the least susceptible to fungal infection and the susceptibility of all stages was dose-dependent, with the highest mortality occurring at the highest dose. B. bassiana significantly affected the rate of nymph production by the lettuce aphid, with the highest effect seen when the alatoid fourth instar of N. ribisnigri was inoculated with B. bassiana. The persistence of B. bassiana conidia on lettuce foliage was not influenced by leaf position. Within 5 days, the cumulative percentage decline in the conidial population was 38% which declined further to 92% and 99% on day 11 and 20 post-spraying, respectively. In accordance, the infectivity to second instar lettuce aphid nymphs of B. bassiana conidia deposited on leaves declined according to an exponential decay model predicting an intercept of 0.59 ± 0.03 (S.E), a reduction in aphid mortality at a rate of 11% with each increasing day after fungal application and a fungus half-life of 6.34 ± 0.69 days.     

Ultralow oxygen treatment for postharvest control of western flower thrips on broccoli

Laboratory studies were conducted to develop ultralow oxygen (ULO) treatment for controlling western flower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), on broccoli at a low temperature of 1 degree C. Complete control was achieved in 5 d at 0.003% oxygen. Oxygen level affected efficacy of ULO treatment. At a higher oxygen level of 0.03%, 6-d treatment killed -85% of thrips, and 10-d treatment killed all thrips. The 5-d ULO treatment with 0.003% oxygen was successfully tested on iced commercial broccoli of several cultivars without any noticeable negative effects on shelf-life and postharvest quality. The ULO treatment provided a safe and effective alternative to methyl bromide fumigation for postharvest control of western flower thrips on exported broccoli for industrial development.     

A survey of syrphid predators of Nasonovia ribisnigri in organic lettuce on the central coast of California

Organic lettuce, Lactuca sativa L., producers on California's Central Coast rely on endemic syrphid flies (Diptera: Syrphidae) to suppress populations of Nasonovia ribisnigri Mosley (Homoptera: Aphididae) and other aphids affecting lettuce. Growers are using various forms of habitat manipulation to enhance biological control. We surveyed syrphids collected from organic romaine in and around the Salinas Valley from March through September 2005 to gain a better understanding of the species responsible for aphid suppression and to examine possible implications for biocontrol. The primary species of syrphid fly reared were Toxomerus marginatus (Say) (39%), Platycheirus stegnus (Say) (27%), Sphaerophoria sulfuripes (Thomson) (13%), and Allograpta obliqua (Say) (10%). Syrphus opinator Osten Sacken (2%), Toxomerus occidentalis (Curran) (1.3%), and Eupeodes volucris Osten Sacken (1%) were less common. Sphaerophoria pyrrhina Bigot, Scaeva pyrastri (L.), Platycheirus obscurus Say, Allograpta exotica Wiedemann, and Eupeodes americanus Wiedemann each made up <1% of the syrphids reared. T. marginatus and Sphaerophoria sulfuripes were commonly collected from romaine plants with few or no detectable aphids. P. stegnus was observed to deposit in clusters of eggs, and was only reared in significant numbers from highly infested fields. Approximately 5% of syrphid larvae overall were parasitized by either Diplazon sp. (Hymenoptera: Ichneumonidae) or Pachyneuron sp. (Hymenoptera: Pteromalidae).     

Rearing history affects behaviour and performance of two virulent Nasonovia ribisnigri populations on two lettuce cultivars

Many aphid species have become virulent to host‐plant resistance, which limits the sustainability of insect resistance breeding. However, when this adaptation to resistant plants is associated with fitness costs for the aphids, virulence can be lost in the absence of resistant plants. For two populations of the lettuce aphid, Nasonovia ribisnigri (Mosely) (Hemiptera: Aphididae), we evaluated whether virulence to Nr‐gene‐based resistance was lost on a susceptible lettuce, Lactuca sativa L. (Asteraceae), and assessed possible costs of virulence. The feeding behaviour and performance of these aphids, reared and tested on susceptible and resistant lettuce, were investigated. The rearing plant affected feeding behaviour and performance of the aphids. Temporary reduction and long‐term loss of virulence were found. The total duration of phloem intake was shorter after being reared on susceptible lettuce and tested on resistant lettuce. In addition, one population had a lower survival on resistant lettuce after being reared on susceptible lettuce. There were also indications of fitness costs of the virulence in both populations.     

Trophic impacts of a rolled-rye cover crop on the lettuce aphid (Nasonovia ribisnigri) and associated insect fauna in cultivated Histosols

Cultivated peatland (Histosol) in Southern Québec (Canada) is a rapidly declining non-renewable resource used to grow most Canadian lettuce (Lactuca sativa L., Asteraceae). Rolled-rye (Secale cereale L., Poaceae) cover crop is one of the conservation practices proposed to reach a more sustainable lettuce production, but the overall impact on the agroecosystem remains poorly studied in Histosols. We assessed multiple effects of rolled-rye cover crop on the trophic chain associated with the lettuce aphid, Nasonovia ribisnigri (Mosley) (Hemiptera: Aphididae), a major pest of lettuce. During one growing season and through two consecutive lettuce crops, we monitored in situ the impacts of rolled-rye cover crop on insect fauna and lettuce quality. We used visual scouting and yellow pan traps to assess plant colonization by N. ribisnigri, its natural enemies, and alternative prey. Exclusion cage experiments were also conducted to measure aphid fitness and population growth. Under greenhouse conditions, following cover crop removal, we examined potential lingering effects of rye within the soil on lettuce plants and N. ribisnigri. In situ experiments showed that rolled-rye cover crop has the potential to inhibit N. ribisnigri field colonization and recruit natural enemies and alternative prey in the first lettuce crop. Rye also reduced aphid fitness as well as lettuce foliar amino acid concentration and weight. For the second lettuce crop, an almost 50% reduction in N. ribisnigri abundance was observed with the use of rolled-rye cover crop. In greenhouse experiments, no persistent effect of rye was observed on the quality of lettuce grown with soil collected under a cover crop, nor on the fitness of aphids inoculated on these lettuces. This study highlights the diversity of trophic effects rolled-rye cover crop may have on lettuce production in Histosols and the potential of rolled-rye cover crop as a cultural practice to reduce aphid populations. Mechanisms at play while underlining agronomic challenges regarding proper rye termination must be further explored to maintain high-performing lettuce yields.     

The impact of insecticide resistance in the currant-lettuce aphid, Nasonovia ribisnigri, on pest management in lettuce

Abstract 1 This paper reports on experiments to determine how two different insecticide resistance phenotypes in the aphid Nasonovia ribisnigri (Mosley), which is a major pest of lettuce, change its susceptibility to pyrethroid insecticides and the carbamate pirimicarb. 2 A novel statistical approach determined how the effectiveness of different insecticides was changed by the two resistance phenotypes. This compared the between‐plant distribution of aphid numbers, as opposed to the mean number of aphids per plant. 3 Results from field cage experiments showed that the effect of the resistances differed. Pyrethroid resistance resulted in lower mortality immediately after application of pyrethroids, whereas resistance to pirimicarb shortened the time over which the chemical was effective. 4 The results of laboratory bioassays suggested that these two resistances were not found together in N. ribisnigri. However, the results reported here contradict this assertion. 5 Experiments with insecticide residues showed that reproduction of resistant N. ribisnigri was greater than that of susceptible N. ribisnigri on plants with ageing insecticide residues, even in circumstances where mortality of resistant and susceptible clones of N. ribisnigri were similar. 6 If more than a few aphids are found on a plant then a whole consignment can be rejected for processing. The results reported here suggest that the effect of both insecticide resistances in N. ribsinigri will be to increase the proportion of lettuce heads with an unacceptable number of aphids on them, leading to increased rejection of plants for processing.     

Ultralow oxygen treatment for control of Latrodectus hesperus (Araneae: Theridiidae) on harvested table grapes

The spider Latrodectus hesperus Chamberlin & Ivie (Araneae: Theridiidae) was subjected to low and ultralow oxygen (ULO) treatments at different temperatures. Complete control of the spiders was achieved in 24-h ULO treatments with 0.5% O2 or lower at 1 degrees C and in a 24-h low oxygen (2%) treatment at 15 degrees C. Oxygen level and temperature greatly affected spider mortality. At 1 degrees C, as oxygen level was decreased from 2 to 0.5%, spider mortality increased from 0 to 100%. At 2% O2, as temperature was increased from 1 to 15 degrees C, spider mortality increased from 0 to 100%. Grape clusters from two table grape (Vitis spp.) cultivars, 'Thompson Seedless' and 'Flame Seedless', were subjected to the 24-h ULO treatment with 0.5% O2 at 1 degrees C. The ULO treatment had no negative effects on grape quality. Because of the relatively short treatment time, effectiveness at low storage temperature and the easily attained oxygen level, we conclude that the ULO treatment have good potential to be implemented commercially for control of black widow spiders on harvested table grapes.     

Feeding behaviour and performance of different populations of the black currant‐lettuce aphid,Nasonovia ribisnigri,on resistant and susceptible lettuce

When crops are bred for resistance to herbivores, these herbivores are under strong selection pressure to overcome this resistance, which may result in the emergence of virulent biotypes. This is a growing problem for crop species attacked by aphids. The Nr‐gene in lettuce confers near‐complete resistance against the black currant‐lettuce aphid, Nasonovia ribisnigri (Mosely) (Hemiptera: Aphididae). Since 2007, populations of N. ribisnigri have been reported in several locations in Europe to infest resistant lettuce varieties that possess the Nr‐gene. The objective of this study was to analyse the behaviour and level of virulence of several N. ribisnigri populations observed to have colonized Nr‐locus‐containing lettuce lines. We analysed the stylet penetration and feeding behaviour, and the performance of these N. ribisnigri populations on resistant and susceptible lettuce lines. Large variation in the degree of virulence to the Nr‐locus‐containing lettuce lines was found among populations of the Nr:1 biotype. The German population was highly virulent on the Nr‐containing resistant lettuce lines, and showed similar feeding behaviour and performance on both the susceptible and resistant lettuces. The French population from Paris was the second most virulent, though reproduction on the resistant lines was reduced. The French population from Perpignan and a population from Belgium, however, showed reduced performance and feeding rate on the resistant compared to the susceptible lettuces. The lettuce background in which the Nr‐gene is expressed influences the level of resistance to the various Nr:1 aphid populations, because the performance and feeding behaviour differed between the aphids on the cultivars (romaine lettuce) compared to the near‐isogenic lines (butterhead/iceberg lettuce). This study also shows that being able to feed on a plant not automatically implies that a population can successfully develop on that plant, because aphids showed phloem ingestion during the 8‐h recording period on resistant lettuce, but were not able to survive and reproduce on the same lettuce line.     

Feeding behavior and performance of Nasonovia ribisnigri on grafts,detached leaves,and leaf disks of resistant and susceptible lettuce

Aphids are dependent on the phloem sap of plants as their only source of nutrients. Host‐plant resistance in lettuce, Lactuca sativa L. (Asteraceae), mediated by the Nr gene is used to control the lettuce aphid Nasonovia ribisnigri (Mosely) (Hemiptera: Aphididae). The resistance is located in the phloem; however, the exact mechanism of resistance is unknown. In this study, we investigated whether the resistance factor (or factors) is synthesized in the root or in the shoot. The feeding behavior and performance of avirulent N. ribisnigri were studied on grafts of resistant and susceptible lettuce. In addition, the persistence of resistance in excised lettuce tissue was measured, by studying the feeding behavior and performance of N. ribisnigri on detached leaves and leaf disks of resistant lettuce. It appears that the resistance factor encoded by the Nr gene is produced in the shoots: aphid feeding was reduced on resistant shoots grafted on susceptible roots, whereas aphids were able to feed on grafts of susceptible shoots on resistant roots. Partial loss of resistance was observed after detachment of leaves and excision of leaf disks from resistant plants. Aphids fed longer on excised resistant plant tissue compared with intact resistant plants; however, compared with excised plant tissue of the susceptible cultivar, the time spent on feeding was shorter, indicating resistance was not completely lost. Our findings caution against the use of excised leaf material for aphid resistance bioassays.     

Mitochondrial DNA sequences of greenbug (Homoptera: Aphididae) biotypes

Sequence comparisons were made for 738-bp of mtDNA cloned from seven greenbug, Schizaphis graminum, biotypes (B, C, E, F, G, H and I) obtained from laboratory colonies maintained by USDA-ARS, Stillwater, OK. These sequences include parts of the genes for 16S ribosomal subunit (16S rRNA), tRNA^leu, tRNA^ser, cytochrome b (cytb) and NADH dehydrogenase (ND) subunits one and four. Sequence data revealed considerable variation in 86 (12%) nucleotide sites over the 738-bp sequenced among the seven greenbug biotypes. Nucleotide invariance was observed within the seven greenbug biotypes from both the laboratory colonies and field collected biotype E greenbugs from Kansas, Nebraska, Oklahoma, and Texas.     

Mitochondrial DNA sequences of greenbug (Homoptera: Aphididae) biotypes

Sequence comparisons were made for 738-bp of mtDNA cloned from seven greenbug, Schizaphis graminum, biotypes (B, C, E, F, G, H and I) obtained from laboratory colonies maintained by USDA-ARS, Stillwater, OK. These sequences include parts of the genes for 16S ribosomal subunit (16S rRNA), tRNAleu, tRNAser, cytochrome b (cytb) and NADH dehydrogenase (ND) subunits one and four. Sequence data revealed considerable variation in 86 (12%) nucleotide sites over the 738-bp sequenced among the seven greenbug biotypes. Nucleotide invariance was observed within the seven greenbug biotypes from both the laboratory colonies and field collected biotype E greenbugs from Kansas, Nebraska, Oklahoma, and Texas.