Short feeding period of carrot psyllid (Trioza apicalis) females at early growth stages of carrot reduces yield and causes leaf discolouration

Overwintered adult carrot psyllids [Trioza apicalis Förster (Homoptera: Psylloidea: Triozidae)] damage carrot [(Daucus carota ssp. sativum L.) (Apiaceae)] seedlings by phloem feeding on the leaves. The aim of this study was to investigate the carrot root and shoot growth in relation to carrot psyllid density during early growth stages. One, two, or three carrot psyllids were allowed to feed on carrot seedlings for 3 days. Leaf damage was measured at the 8‐leaf stage, and root, leaf fresh weight, and number of true leaves were measured at harvest. Both the age of the carrot seedling at infestation and the psyllid density had a significant effect on leaf damage at the 8‐leaf stage: seedlings damaged at the cotyledon stage exhibited more leaf damage than seedlings damaged at the 1‐leaf stage. A higher psyllid density significantly reduced the carrot root weight at harvest. The significant interaction of psyllid density with seedling age indicates that differently aged carrot seedlings responded differently to feeding: one psyllid feeding for 3 days at the cotyledon stage caused a significant yield loss, whereas three psyllids were needed to cause the same impact at the 1‐leaf stage. Carrot leaf weight at harvest was not reduced by carrot psyllid feeding: leaves recovered from the damage but roots did not. Our results confirm the farmers’ observations that a trap replacement period of 1 week for carrot psyllid monitoring is too long, especially at the cotyledon stage. Severe leaf discolouration on damaged carrots was observed at harvest. The possible reasons for this discolouration, such as toxin excreted in psyllid saliva or plant pathogenic mycoplasma infection, are discussed.     

Effects of carrot psyllid (Trioza apicalis) feeding on carrot yield and content of sugars and phenolic compounds

Carrot psyllid, Trioza apicalis, is a serious pest of carrot in Northern Europe, as it can significantly damage young carrot seedlings in a period as short as 3 days. This study was conducted to investigate effects of carrot psyllid feeding at different plant growth stages on carrot yield and to assess changes in content of sugars, phenolics and related compounds in carrot roots resulting from the psyllid feeding. In addition, reflectance of carrot leaves was measured to assess the intensity of discolouration in damaged leaves. Results showed that carrot yield was significantly reduced by a 3‐day carrot psyllid feeding period when the seedlings were exposed to psyllids at 1‐ or 2‐leaf stage. However, at 4‐leaf stage feeding by one carrot psyllid did not reduce yield. Sucrose concentration in the damaged roots was significantly decreased, whereas concentrations of some phenolic compounds were significantly increased. The reflectance of leaves of damaged carrots differed significantly from those of undamaged control leaves. These observations indicate that carrot psyllid damage has potential to lower not only the carrot yield, but also the carrot crop quality. No phytoplasma was detected in the carrots exposed to psyllids, but recently, T. apicalis has been associated with ‘Candidatus Liberibacter solanacearum’. The role of carrot psyllid feeding and the psyllid‐associated bacterium in the damage formation are discussed.     

Spreading of Trioza apicalis and development of “Candidatus Liberibacter solanacearum” infection on carrot in the field conditions

Carrot cultivation in Europe is suffering from infections with “Candidatus Liberibacter solanacearum” (CLso), a psyllid‐transmitted bacterial pathogen. In this study, field experiments were carried out in Finland to separately measure the effects of psyllid feeding damage and CLso infection on the carrot root growth and to reveal the dynamics of the spreading of CLso within the field. Most of the experiments were carried out during the summers 2016 and 2017, and a follow‐up sampling was performed in 2018. Carrot psyllid (Trioza apicalis) flight activity was monitored and carrots were sampled at 25 points within the field. Early in the season a clear spatial correlation was found between the sampling sites showing the psyllid feeding damage, that is, leaf‐curling, up to the range of 40–60 m, indicating aggregation behaviour of the psyllids. No CLso infections were detected in the first sampling, which was performed before the psyllid flight peak in both years. Later, a positive correlation between the psyllid feeding damage and the CLso titre was observed. An increase in the CLso titre occurred approximately a month after the psyllid flight peak, and this increase correlated with the accumulating effective temperature sum. In 2016, both the psyllid feeding damage and CLso infection had a significant effect on the carrot root weight. The effect of CLso titre on root weight was nonlinear, that is, it intensified rapidly at the highest bacterial titres. During the colder summer of 2017 the CLso titres did not reach high enough levels in the plants to cause substantial visible symptoms and root growth reduction. Thus, it seems that in the Nordic conditions the effect of CLso infection on carrot yield is strongly dependent on the weather conditions during the growing season.     

Assessment of the efficiency of different control programs to reduce Trioza apicalis Först. (Triozidae: Hemiptera) feeding damage and the spread of “Candidatus Liberibacter solanacearum” on carrots (Daucus carota ssp. sativus L.)

The control of carrot psyllid Trioza apicalis Förster largely relies on chemical measures, and the current integrated pest management (IPM) strategy is based on pest scouting. The number of active ingredients available for psyllid control will further decline in the coming years. The need for alternative control measures is therefore urgent. In this work the efficiency of different control programs including a kaolin particle film and plant-derived, crude saponin extract, chemical control, insect net and IPM (kaolin in combination with insecticides) programs to reduce psyllid feeding damage, reproduction and the spread of “Candidatus Liberibacter solanacearum” (CLso) in carrots was studied. Each year in 2016–2018, four replicates of each treatment were randomised in a row-column design on a commercial carrot farm. After the treatments were executed, the psyllid nymphs and eggs were counted. At the harvest, the carrot roots and shoots were weighed, damages assessed, and samples were taken for CLso detection from 50 plants at each replicate. Kaolin treatment alone and in combination with insecticides effectively reduced the number of psyllid nymphs and eggs in all the years studied. Saponin was applied only on the first year, since it significantly increased the number of T. apicalis eggs compared to other treatments. The insect net was superior to other treatments in all the studied aspects in all the years. Under normal weather conditions, the highest root weight was harvested under the insect net, followed by the chemical control program consisting of pyrethroids, kaolin treatment, untreated control and saponin treatment. During extreme weather conditions, chemical control programs were not effective at protecting the carrots from psyllid feeding, which was reflected as low root yield. In all years, the carrot leaf damage percent negatively correlated with the root weight. Similarly, the shoot:root ratio increased as the leaf-curling percentage rose, which was even pronounced under drought stress. The effect of climatic stress should be considered when developing IPM strategies.     

Essential oil composition in leaves of carrot varieties and preference of specialist and generalist sucking insect herbivores

• 1 The carrot psyllid Trioza apicalis and Lygus rugulipennis can cause serious damage to cultivated carrots, especially at the seedling stage. The essential oil composition in leaves of several carrot varieties was studied in relation to oviposition acceptance by sucking insect herbivores that have different feeding strategies. Of the insect species studied, T. apicalis is a carrot specialist, T. anthrisci is an Apiaceae specialist, and L. rugulipennis is a generalist.
• 2 The oil composition differed significantly between leaves from different carrot varieties (Flakkeer 2, Nantura, Parano, Napoli, Panther, Splendid, Nantes 3 Express).
• 3 There were no differences in the mean numbers of eggs laid by T. apicalis or T. anthrisci on different varieties, but L. rugulipennis laid fewer eggs on the Panther variety than on Nantes 3 Express.
• 4 There was a negative linear correlation between limonene concentration and number of eggs laid by T. apicalis, confirming that limonene is a repellent to the carrot psyllid. Results suggest that only particular compounds influence the preference of the carrot psyllid, and these compounds may not be the main components in the essential oil of carrots.
• 5 A positive correlation was found between myrcene concentration and number of eggs laid by T. anthrisci. Essential oil composition did not explain egg‐laying preference of L. rugulipennis.
• 6 The results indicate that essential oil composition of carrot varieties affects host preference of Apiaceae specialists more than that of generalists.

     

Anatomy of an outbreak: the biology and population dynamics of a Cardiaspina psyllid species in an endangered woodland ecosystem

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Biology and epidemics of Candidatus Liberibacter species,psyllid‐transmitted plant‐pathogenic bacteria

Candidatus Liberibacter species are Gram‐negative bacteria that live as phloem‐limited obligate parasites in plants, and are associated with several plant diseases. These bacteria are transmitted by insects called psyllids, or jumping plant lice, which feed on plant phloem sap. Citrus huanglongbing (yellow shoot) or citrus greening disease is associated with three different species of Ca. Liberibacter – Ca. L. asiaticus, Ca. L. africanus and Ca. L. americanus – all originally found on different continents. Ca. L. asiaticus is the most severe pathogen, spread by Asian citrus psyllid Diaphorina citri and causing devastating epidemics in several countries. Ca. L. africanus occurs in Africa where it is spread by the African citrus psyllid Trioza erytreae. Ca. Liberibacter solanacearum is associated with diseases in several solanaceous plants, and transmitted by potato psyllid Bactericera cockerelli. Zebra chip disease is causing large damage in potato crops in North America. In Europe Ca. Liberibacter solanacearum is associated with diseases of the Apiaceae family of plants, carrot and celery, and transmitted by psyllids Trioza apicalis and Bactericera trigonica. When Ca. Liberibacter is suspected as the disease agent, the diagnosis is confirmed by DNA‐based detection methods. Ca. Liberibacter‐associated plant diseases can be controlled by using healthy plant propagation material, eradicating symptomatic plants, and by controlling the psyllid populations spreading the disease.     

Carrot psyllid (Trioza apicalis) winter habitats – insights in shelter plant preference and migratory capacity

Abstract:  The carrot psyllid ( Trioza apicalis ) is a serious pest in carrot-growing areas in northern and parts of central Europe. The psyllids overwinter as adults on conifers and during summer feed and lay eggs on carrot plants ( Daucus carota ssp. sativus ), thereby destroying the crop. To investigate the migratory capabilities and preferences for different shelter plant species of the carrot psyllid, we made an inventory study of its winter habitats in three carrot-growing regions in southern Sweden. Norway spruce ( Picea abies ) was the preferred conifer over Scots pine ( Pinus sylvestris ) and juniper ( Juniperus communis ). We found psyllids on trees up to 1 km from the carrot fields, which was the largest distance sampled. The regression of catch numbers over distance was non-significant, however all samples containing more than seven psyllids were collected within 250m distance from the fields. There was no obvious pattern between catch directions and the prevailing wind directions of the preceding migratory period. Our study did not show any differences between males and females with respect to migration or shelter species preferences.     

Discrimination among host plants (Leucaena species and accessions) by the psyllid pest Heteropsylla cubana and implications for understanding resistance

Abstract 1 The herbivorous bug Heteropsylla cubana Crawford (Homoptera: Psyllidae) is a pest of the cattle fodder crop Leucaena (Leguminosae: Mimosoideae). The interaction between the psyllid and three varieties of its Leucaena host plant was investigated in relation to the apparent resistance of some Leucaena varieties (Leucaena leucocephala, Leucaena pallida and their hybrids) to attack. 2 Field trials demonstrated that adult psyllids distinguished among the different varieties of Leucaena over a distance, and were attracted to L. leucocephala in significantly higher numbers than to L. pallida or to the hybrid. Pesticide treatment increased the attractiveness of Leucaena plants, even of those deemed to be psyllid resistant. Numbers of psyllid eggs and nymphs, sampled in the field, reflect the arrival rates of adults at the three plant varieties. 3 Wavelength reflectance data of the three Leucaena varieties were not significantly different from one another, suggesting that psyllids cannot discriminate among the three plants using brightness or wavelength cues. There was a differential release of caryophyllene among the three varieties. Release of caryophyllene in L. leucocephala and the hybrid appeared to be influenced by environmental conditions. 4 Experiments demonstrated that caryophyllene (at least on its own) did not influence the behaviour of leucaena psyllids in relation to leucaena plants. 5 The results suggest that host plant volatiles cannot be dismissed as significant in the interaction between the leucaena psyllid and its Leucaena host plants. Further avenues for investigation are recommended and these are related to novel ways of understanding resistance in insect plant inter‐relationships.     

Establishment of <Emphasis Type="Italic">Psyllaephagus parvus</Emphasis> and <Emphasis Type="Italic">P. perplexans</Emphasis> as serendipitous biological control agents of Eucalyptus psyllids in southern California

The free-living lemon gum psyllid, Cryptoneossa triangula Taylor, and the lerp-forming spotted gum psyllid, Eucalyptolyma maideni Froggatt (Hemiptera: Psyllidae) are invasive pests of eucalypts in California. In 2007, Psyllaephagus parvus Riek (Hymenoptera: Encyrtidae) was discovered parasitizing spotted gum psyllids and Psyllaephagus perplexans Cockerell was collected from lemon gum psyllids. While neither parasitoid species was purposely introduced, presence of the parasitoids was significantly associated with reduced intensity and duration of population peaks for both psyllid species. Spring peaks were reduced more than fall peaks. We estimated minimum rates of parasitism from the ratio of mummies to live nymphs. Higher parasitism was recorded in coastal than inland locations during the spring, while parasitism was similar for coastal and inland populations in the fall. Logistic regression models suggest parasitoids were the determining factor of psyllid population densities, although physical parameters, such as irrigation, may affect psyllid or parasitoid populations.     

Seasonal biology and abundance of Psyllaephagus pistaciae,a biocontrol agent of the common pistachio psylla Agonoscena pistaciae

The solitary endoparasitoid Psyllaephagus pistaciae Ferrière (Hymenoptera: Encyrtidae), is the most widely distributed biological control agent of the common pistachio psyllid, Agonoscena pistaciae Burckhardt and Lauterer (Hemiptera: Psylloidea), in Iran. The pupation and overwintering sites of diapausing parasitoids and the psyllid were studied for 2 years using emergence traps in pistachio orchards in Rafsanjan, Iran. The psyllid mummies containing the overwintering parasitoid adhered to pistachio leaves and were carried on these leaves away from the tree when they latter senesced. The present results verified that plant litter which included dried grasses and old pistachio leaves tended to support a greater population of adult winter-form psyllid and psyllid mummies during the winter through early spring than other options examined. Adult parasitoids appeared in the field in early April, about 30 days after the emergence of adult psyllids, but almost at the same time as the hatching of the first generation psyllid nymphs in early April. Rates of parasitism of CPP were generally low throughout most of the year, ranging from 1 to 5%, but rose in late autumn to about 11%. Results suggest that the density of P. pistaciae is not great enough to keep pace with the psyllid populations in these orchards. They explain why growers consider it necessary to apply pesticides for this pest. However, this parasitoid undoubtedly does play an important role in the natural control of A. pistaciae late in the growing season, particularly in non-sprayed orchards. Conservation of these natural enemies should be one of the objectives in the development of sustainable pest management programs.     

Establishment of Asian citrus psyllid (<Emphasis Type="Italic">Diaphorina citri</Emphasis>) primary cultures

The Asian citrus psyllid (AsCP), Diaphorina citri Kuwayama (Hemiptera: Psyllidae), is a highly competent vector of the phloem-inhabiting bacterium Candidatus Liberibacter asiaticus associated with the citrus disease huanglongbing (HLB). Commonly referred to as citrus greening disease in the USA, HLB causes reduced fruit yields, quality, and ultimately tree death and is considered the most serious citrus disease. HLB has become a major limiting factor to the production of citrus worldwide. Studies of HLB have been impeded by the fact that C. Liberibacter has not yet been cultured on artificial nutrient media. After being acquired by a psyllid, C. Liberibacter asiaticus is reported to replicate within the psyllid and is retained by the psyllid throughout its life span. We therefore hypothesized that C. Liberibacter asiaticus could be cultured in vitro using psyllid cell cultures as the medium and investigated the establishment of a pure culture for AsCP cells. Several commercially available insect cell culture media along with some media we developed were screened for viability to culture cells from AsCP embryos. Cells from psyllid tissues adhered to the plate and migration was observed within 24 h. Cells were maintained at 20°C. We successfully established primary psyllid cell cultures, referred to as DcHH-1, for D. citri Hert-Hunter-1, with a new media, Hert-Hunter-70.     

Chemosensory responses to foods by an herbivorous acrodont lizard, <Emphasis Type="Italic">Uromastyx aegyptius</Emphasis>

Actively foraging lizards use the lingual-vomeronasal system to identify prey by chemical cues, but insectivorous ambush foragers do not. The major clade Iguania includes numerous herbivores and omnivores; among them, two iguanid and one agamine species identify plant and animal foods by tongue flicking, and data suggest that the leiolepidine Uromastyx acanthinurus may as well. We conducted experiments on chemosensory response to food by the herbivorous U. aegyptius. When chemical stimuli were presented on cotton balls in experiment 1, the lizards exhibited greater responsiveness (tongue-flick attack scores) to chemical stimuli from crickets and a preferred plant food (dandelion flowers) than from deionized water. When chemical stimuli were on ceramic tiles in experiment 2, the lizards exhibited greater total tongue flicks to cricket stimuli than to any other stimuli, and to dandelion than to deionized water. Lizards bit more frequently in response to cricket and dandelion cues than to stimuli from a nonpreferred plant (carrot) and deionized water. Tongue-flick attack scores were greater in response to cricket and dandelion stimuli than to carrot or water stimuli. These findings are consistent with the hypothesis that herbivores, even those having ambush-foraging ancestors, use chemical cues to identify potential foods. The data support the hypothesis that chemosensory responses correspond to diet. Because most lizards are generalist predators, studies of herbivorous species can provide important information on possible evolutionary adjustment of chemosensory response to dietary shifts. Electronic Publication     

Exploitation of the resistance to carrot fly in the wild carrot species Daucus capillifolius

Under field conditions a wild Daucus species from Libya, D. capillifolius, supported less than one tenth as many carrot flies (Psila rosae) as the susceptible carrot cultivar Danvers Half Long 126. Breeding lines developed from crosses between D. capillifolius and three different carrot types were grown in a series of field experiments at Wellesbourne between 1980 and 1989. Each year selections were made for agronomic quality and/or for increased resistance to carrot fly. The programme produced lines which for size, shape and colour represented most of the commercially-important carrot types. Some of these lines were also significantly more resistant to carrot fly than selections from the partially-resistant cv. Sytan. However, the best lines were not as resistant as the wild parent. The highest quality resistant lines were sold to seed companies for variety production.     

Differences in the relative resistance of two carrot cultivars to carrot fly attack over five seasons

A comparison was made over five seasons of carrot fly (Psila rosae) damage on two carrot cultivars, Sytan and Danvers, which represented the extremes of resistance discovered in screening trials at Wellesbourne. Plants were harvested regularly during the seasons and at each harvest the number and weight of roots was recorded and carrot fly damage was assessed using various techniques; in 1979-80 the numbers of carrot fly larvae and pupae in and around root samples were counted. The experiments confirmed repeatedly the relative resistance of cv. Sytan compared with Danvers. The estimated reduction in carrot fly larvae on Sytan relative to Danvers in early November in four seasons ranged from 40% to 67%. When tested against first generation carrot fly attack the reduction in larvae on Sytan was 54%. There were 45% fewer mines per root on Sytan resulting in less damage at each harvest in all seasons. Larvae took longer to develop on Sytan than Danvers and 18% more plants of Sytan survived carrot fly attack. Differences in seedstock, season, sowing time, generation of carrot fly, plant size and density did not account for observed differences in damage between the two cultivars. The studies indicated satisfactory practical techniques for assessing carrot fly damage in cultivar screening trials.     

Characterization of the electrical penetration graphs of the psyllid Bactericera trigonica on carrots

The psyllid Bactericera trigonica Hodkinson (Hemiptera: Triozidae) is a carrot and celery pest recently described as a vector of the plant pathogenic bacterium Candidatus Liberibacter solanacearum (Lso) on Apiaceae. Detailed information on vector stylet penetration activities is essential in the study of Lso transmission. In this study we used the electrical penetration graph (EPG) technique, characterized waveforms produced during the various stylet penetration activities in carrot leaves, and correlated them with stylet tracks and salivary sheath termini on plant tissues as well as with Lso inoculation. In addition, the effect of Lso in B. trigonica on the stylet penetration activities was tested. The EPG waveforms identified were: waveforms C1 and C2 detected in the mesophyll, waveforms D, E1, and E2 near or in the phloem sieve elements, and waveform G in the xylem vessels. A waveform pattern not previously reported for psyllids was the ‘pseudo‐potential drop’ (pseudo‐pd), characterized by sudden voltage dips similar to potential drops. However, the lowered voltage appeared to be inverted when the plant voltage is negative, indicating that it is caused by an increased resistance period and not due to a cell puncture. A direct correlation is shown between the waveform E1 and salivation into phloem sieve elements by B. trigonica as the inoculation of Lso occurred in a period as short as 30 s of E1; Lso transmission occurred in 17 of 35 plants (48%). Stylet activities during waveforms C or D had no consequences on the inoculation of Lso. In conclusion, Lso infection directly affects the probing behaviour of B. trigonica by increasing the total duration of C and D waveforms, but not variables related to phloem salivation (Lso inoculation) or ingestion (Lso acquisition). The reported information here is fundamental for identifying the psyllid vector traits of behaviour associated with transmission of Lso to Apiaceae.     

The effects of time of sowing and harvest on carrot biochemistry and the resistance of carrots to carrot fly

Two carrot cultivars which represented contrasting levels of resistance to carrot fly, Psila rosae, were grown in a replicated field experiment at Wellesbourne in 1984–85. Seed was sown on five occasions between April and August 1984 and the crop harvested after a minimum growth in the field of 16 wk on seven occasions between August 1984 and February 1985. A highly significant correlation (r = -0.78; P > 0.001) between the levels of carrot fly damage and the concentration of chlorogenic acid in the roots enabled a model to be formulated to predict the relative predisposition to carrot fly larval damage; high levels of chlorogenic acid early in the season predisposed roots to severe attack when they were older.     

Large‐scale climatic variability affects the dynamics of tropical skipjack tuna in the Western Pacific Ocean

The role of climate variability in determining the fluctuations of fish populations had been a traditional problem in ecology. In this paper, we studied the role of the Southern Oscillation Index (SO) and the Pacific Decadal Oscillation (PDO) on the population dynamics of the western stock of the skipjack tuna Katsuwonus pelamis. Our analysis was based in three sequential steeps: a diagnostic approach to deduce what kind of population dynamic model should be more appropriate, the modelling of capture per unit of effort data through a logistic model, and the use of population dynamic theory for analyzing the effect of exogenous perturbations. We find that direct and one‐year lagged negative PDO effects and one‐year lagged negative SO effects were needed to explain annual tuna fluctuations. Models including the combined effects of these climatic indexes explain 80% of the variance in tuna fluctuations. In addition, these models provided very accurate predictions of independent skipjack tuna observed dynamics. This result is encouraging because the inherent variability in CPUE data and the not well determined link between climate and ecological processes. Finally, this study demonstrates that simple models can offer reasonable explanations and accurate predictions of tuna fluctuations, provided they are based on a sound theoretical framework.     

Identification of Alternative Hosts of the Fastidious Bacterium Causing Citrus Greening Disease

Citrus greening is a severe disease caused by a fastidious bacterium (GFB) residing in the sieve tubes of its hosts. It is an epidemic disease and is spread by insect vectors. In Asia, the Asian citrus psyllid (Diaphorina citri Kuwayama) is the vector for GFB. For the epidemiological study, an investigation of alternative hosts of GFB was made. Four suitable hosts of the Asian psyllid that are considered as possible alternative hosts of GFB were investigated on graft‐inoculation tests. The multiplication of GFB in plants was monitored by dot hybridization using a GFB‐specific DNA probe developed previously by us. The results demonstrate that GFB can replicate in Chinese box orange (Severinia buxifolia) and wood apple (Limonia acidissima), but not in common jasmin orange (Murraya paniculata var, paniculata) and curry leaf (Murraya euchrestifolia), Chinese box orange is a good host in which GFB replicates as well as it does in its citrus hosts. Wood apple is a transient host in which GFB exists temporarily and disappears several months later. Common jasmin orange and curry leaf are not hosts of GFB as they showed no detectable signals in dot hybridization tests throughout 1 year of experimentation.