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.     

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.     

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.

     

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.     

Electrophysiological responses of carrot psyllids (Trioza apicalis), in different phases of their life cycle,to volatile carrot and conifer compounds

Carrot psyllids (Trioza apicalis) pose a constant threat to carrot production in parts of Europe, and treatments with chemical insecticides are common. To be able to develop alternative control tactics, more knowledge about the psyllid's host-finding behaviour and underlying physiology is needed. Using single-sensillum recordings from overwintered and non-overwintered males and females, we found essentially identical responses for the two groups and for both sexes. Using six compounds emanating from carrots or conifers, the psyllids' overwintering plants, and extracts of carrot leaves, five different olfactory sensory neuron classes could be distinguished from our high-quality recordings, viz. #1 responding strongly and exclusively to terpinene-4-ol, #2 responding strongly and most often exclusively to nonanal, #3 responding moderately strongly to terpinolene, #4 responding strongly to (Z)-3-hexenal and most often weaker to terpinolene, #5 responding exclusively to carrot extract.     

Using physical barriers to prevent carrot fly (Psila rosae (Fabricius)) damage in domestic production

A field experiment was used to assess the effectiveness of different barriers in protecting garden‐scale carrot production from carrot fly (Psila rosae (Fabricius)) damage. Some of the vertical barriers tested were found to provide a useful method of protecting early season carrots from carrot fly in terms of the percentage of carrots free from damage but, under cumulative pest pressure of several generations of carrot fly, such barriers were found to provide insufficient protection. Gardeners should therefore completely cover their carrot crop to attain an acceptable level of control, and this was found to be especially important for carrots harvested later in the season. There were positive effects of some barrier types on yield which may be due, at least in part, to the protection given by the barriers to carrot seedlings.     

Guilty by association: an evaluation of millipedes as pests of carrot and sweet potato

An evaluation of the pest potential of millipede species occurring in Ontario sweet potato and carrot fields was conducted in response to recent grower concerns about the presence of millipedes in close proximity to damaged vegetables. This study is the first North American survey of millipedes on arable soils and the first evaluation of North American millipede damage to sweet potatoes and carrots. Through field surveys, Cylindroiulus caeruleocinctus was found to be the dominant millipede species in Ontario sweet potatoes and carrots. Fields were surveyed over the growing season, and the factors important to each species’ abundance were evaluated using Minimum AIC Estimation (MAICE). Post‐harvest damage assessments were performed, and MAICE analysis was used to determine which arthropod and environmental parameters were most important in explaining damage to sweet potatoes and carrots. Wireworm (Elateridae) abundance was consistently found to explain root damage better than C. caeruleocinctus abundance, and it is concluded that the majority of field‐observed damage was caused by wireworms. C. caeruleocinctus was negatively correlated with both wireworms and damage in carrot fields and is not likely to be a pest of that vegetable. However, abundance of C. caeruleocinctus in sweet potatoes was positively correlated with both wireworms and damage. This species may cause some damage to sweet potato tubers under field conditions, but management tactics should focus on wireworms as the primary source of damage.     

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.     

Periodicity of the outbreaks of the carrot psyllid (<Emphasis Type="Italic">Trioza apicalis</Emphasis>) cannot be explained by sunspot activity

The periodicity of the fluctuations in the attacks of the carrot psyllid Trioza apicalis in long-term monitoring was studied by analysis of data of previous authors. The occurence of only one generation in the year shows that peaks of attack cannot arise suddenly in one year, but are prolonged over several years, as are the troughs of attack. This is the cause of the long-term fluctuation, which seems to be periodic. The statement of Ozols, that the period of the fluctuations of carrot psyllid was connected with climatic conditions via sunspot activity, was not evident statistically.     

The complementary effects of plant resistance and the choice of sowing and harvest times in reducing carrot fly (Psila rosae) damage to carrots

The benefits of combining a partially-resistant carrot cultivar with different sowing and lifting dates to reduce carrot fly, Psila rosae, damage were investigated at Wellesbourne in 1983 and 1984-85. The partially-resistant cv. Sytan was less damaged and supported fewer insects than the susceptible cv. Danvers on all lifting dates. The estimated reduction of carrot fly larvae on Sytan compared with Danvers ranged from 33 to 95%. Nine combinations of sowing and lifting dates provided more than 75% marketable roots of Sytan compared with only three combinations of dates for Danvers. An early June sowing of both cultivars provided roots of a marketable size with the least attack. More than 90% of Sytan roots were still marketable in December and fewer insects were produced by the end of the season on these roots than on those sown earlier. In addition, sowing in June decreased the number of pupae produced on cv. Danvers by 10 times compared with earlier sowings. Combining partial resistance with specific sowing and lifting times enabled satisfactory yields of marketable carrots to be obtained in a field infested by high populations of carrot fly.     

Problems in field selection for resistance to carrot fly (Psila rosae) in carrot cv. Long Chantenay

In field trials between 1973 and 1982 families of carrots of cv. Long Chantenay were assessed for their resistance to carrot fly (Psila rosae). In some but not all years, families selected for their observed resistance in earlier trials seemed more resistant than the parent line. In more than half the trials there was an association between carrot fly damage and root density, there being less damage on those families from which more roots were harvested. Thus, family selection within cv. Long Chantenay did not lead to a consistent improvement in resistance to carrot fly. Alternative strategies for achieving plant resistance to this pest are discussed.     

Moderating Night Radiative Cooling Reduces Frost Damage to Metrosideros polymorpha Seedlings Used for Forest Restoration in Hawaii

Winter frosts caused by radiative cooling were hypothesized to limit successful reintroduction of Hawaiian plants other than Acacia koa to alien‐dominated grasslands above 1700 m elevation. We determined, in the laboratory, the temperature at which irreversible tissue damage occurred to Metrosideros polymorpha leaves. We also conducted a field study of this species to determine if (1) leaf damage was correlated with sub‐zero leaf temperatures, (2) radiative cooling could be moderated by canopies of A. koa, and (3) low soil temperatures contributed to seedling damage. The last was evaluated by thermally buffering seedlings with water‐filled bladders placed at their base to keep roots warm, or by installing a radiation shield to reduce early morning transpiration when water uptake from cold soils would be least. Leaf temperatures were monitored between midnight and 7:00 a.m. using fine‐wire thermocouples, and leaf damage was recorded monthly. In the laboratory, supercooling protected leaves from mild sub‐zero temperatures; irreversible tissue damage occurred at about ?8°C. In the field, leaf damage was strongly correlated with degree‐hours below freezing. Unprotected seedlings suffered the greatest leaf damage. Those sheltered under A. koa trees rarely experienced temperatures below ?3°C, and damage was minimal. Shaded and thermally buffered seedlings suffered less damage than unprotected plants, probably due to elevated leaf temperatures rather than improved water relations. Using A. koa or artificial devices to reduce radiative cooling during winter nights should enhance establishment of M. polymorpha in high‐elevation rangeland.     

Effect of concomitant application of Pseudomonas fluorescens and Purpureocillium lilacinum in carrot fields infested with Meloidogyne hapla

Root-knot nematode, Meloidogyne hapla remains a major limiting factor to obtain the estimated yield and quality of carrots in many countries. Effective use of nematode antagonistic bio-agents is a potentially important component of the eco-friendly agro-farming. The effect of seed treatment (ST) with liquid Pseudomonas fluorescens at 100 ml/kg seeds and soil drenching (SD) with Purpureocillium lilacinum at 5 l/ha, singly and jointly, was studied to minimise the damage caused by M. hapla in carrot plants under field conditions. The concomitant application of P. fluorescens ST + P. lilacinum SD reduced 70% of second stage juvenile (J2) population in soil, 71% of female population in root and 74% of egg numbers in roots. The carrot plants from P. fluorescens ST + P. lilacinum SD plots were 36% taller with 39% more leafs and 30% longer leaves than untreated plants. The yield was also 29% higher in concomitant application. There was no significant difference in the root colonisation of P. fluorescens and P. lilacinum in solo and combined treatments. It concludes that the concomitant application of P. fluorescens ST and P. lilacinum SD is more effective to suppress M. hapla infection and enhance the yield of carrot.     

Feeding disruption of potato psyllid,Bactericera cockerelli,by imidacloprid as measured by electrical penetration graphs

The potato psyllid, Bactericera cockerelli (Sulc) (Hemiptera: Triozidae), is a serious pest of potatoes that can cause yield loss by direct feeding and by transmitting a bacterial pathogen, Candidatus Liberibacter psyllaurous (also known as Candidatus L. solanacearum), which is associated with zebra chip disease of this crop. Current pest management practices rely on the use of insecticides for control of potato psyllid to lower disease incidences and increase yields. Imidacloprid is typically applied at potato planting, and it remains unknown if imidacloprid has any effect on potato psyllid feeding behavior. Thus, our specific objectives of this study were to determine and characterize the effects of imidacloprid treatment (0.11 ml l^?1) to potato plants on adult potato psyllid feeding behavior 1, 2, and 4 weeks post‐application. Electrical penetration graph (EPG) recordings of potato psyllid feeding revealed six EPG waveforms, which include non‐probing (NP), intercellular stylet penetration (C), initial contact with phloem tissue (D), salivation into phloem sieve elements (E1), phloem sap ingestion (E2), and ingestion of xylem sap (G). The number of NP events and the duration of individual NP events significantly increased on plants treated with imidacloprid compared with untreated controls. Potato psyllids exhibited significant decreases in the number of phloem salivation events on plants treated with imidacloprid. Waveform durations and waveform durations per event for E2 and G were significantly decreased for psyllids on plants treated with imidacloprid compared with untreated controls. These data suggest that the effective use of imidacloprid to reduce transmission of Ca. Liberibacter psyllaurous is related to the negative effects of imidacloprid on psyllid feeding.     

Root disturbance of common ash, Fraxinus excelsior (Oleaceae), leads to reduced foliar toughness and increased feeding by a folivorous weevil, Stereonychus fraxini (Coleoptera, Curculionidae)

Abstract.

• 1 Bioassays were carried out to examine differences in the feeding of a folivorous weevil, Stereonychus fraxini De Geer, on leaves from ash saplings with undamaged roots, and those with damaged roots. Beetles ate significantly more of the leaves of root-damaged saplings in a choice experiment.
• 2 A separate study of the effect of root damage on leaf toughness was carried out on a second group of ash saplings. Saplings with damaged roots had less tough leaves than control saplings. Decreased leaf toughness in hypothesized as a mechanism to explain the preference of weevils for leaves from damaged trees.
• 3 Both chemical and physical changes may occur in the tissues of ash trees in response to environmental stress such as drought and root damage.
• 4 Root damage caused by agricultural disturbance is hypothesized as a mechanism making mature ash trees in hedgerow ecosystems more susceptible to insect herbivores.

     

Relationship between the concentration of chlorogenic acid in carrot roots and the incidence of carrot fly larval damage

Chlorogenic acid (1·24-3·36 mg/g) was identified as the main phenolic component in the peel of carrots by hplc analysis. The higher the concentration of chlorogenic acid in different cultivars the greater the susceptibility to carrot fly larval damage. Increases in concentration were found both after carrot fly damage and after carrots had overwintered in the field. The presence and location of chlorogenic acid was confirmed in sections of carrot tissues, mounted in 0·05 M ammonia solution by viewing them using a u.v.-epifluorescent microscope. The importance of phenolic compounds and their function in the production of insect cuticle is discussed in relation to the different concentrations of chlorogenic acid and resistance to carrot fly in carrots.     

Influences of leaf age and type,non‐host volatiles,and mineral oil deposits on the incidence,distribution, and form of stylet tracks of Diaphorina citri

Psyllids produce saliva that gels to form a protective sheath around their stylets. This saliva can be visualized as stylet tracks, and we have used the presence of tracks to study the feeding behaviour of Diaphorina citri Kuwayama (Hemiptera: Liviidae). Both single and branched tracks were produced by nymphs and adults, and the tracks made by males and females did not differ. Tracks dissipated from calamondin leaves within a 7‐day post‐feeding period after adults fed for 2 days and numbers of tracks declined with increasing maturity of calamondin leaves. In the six host plants studied, most psyllids fed abaxially from midribs and most probes traversed or terminated in the tissue (midrib, lateral vein, minor vein, or mesophyll) above which the stylets entered the leaf or leaflet. The number of tracks and landings were recorded on the six hosts in choice tests. More tracks were found in leaves or leaflets of orange jasmine, wampee, and trifoliate orange than in sour orange, calamondin, and lemon. Orange jasmine is considered a preferred host of D. citri, and this is in agreement with the number of tracks found in this study, but not the number of landings. Trifoliate orange is considered a poor host of D. citri, which, in this study, is reflected in the low number of landings, but not in the numbers of tracks. Our results indicate that the presence of adult psyllids on a plant may not reflect its host status, and that the presence of stylet tracks should also be determined in host preference studies. When calamondin leaves were paired with leaves of guava, billygoat weed, or greenleaf desmodium, the presence of volatiles from these plants reduced feeding by adults on calamondin and suggests that understoreys of billygoat weed or desmodium in orchards may also reduce feeding. A negative, exponential relationship between numbers of tracks per leaf and the concentrations of an agricultural mineral oil applied to leaf surfaces was found. This reduction in feeding, in conjunction with reductions in oviposition, has practical implications for suppressing psyllid populations in orchards.     

Enhanced proliferation and efficient transmission of Candidatus Liberibacter asiaticus by adult Diaphorina citri after acquisition feeding in the nymphal stage

We carried out a quantitative detection of Candidatus Liberibacter asiaticus, the bacterium associated with the disease of huanglongbing, in the vector psyllid Diaphorina citri by using a TaqMan real‐time PCR assay. The concentration of the bacterium was monitored at 5‐day intervals for a period of 20 days after psyllids were exposed as fifth instar nymphs or adults to a Ca. L. asiaticus‐infected plant for an acquisition access period of 24 h. When adults fed on Ca. L. asiaticus‐infected plant, the concentration of the bacterium did not increase significantly and the pathogen was not transmitted to any citrus seedlings. In contrast, when psyllids fed on infected plant as nymphs, the concentration of the pathogen significantly increased by 25‐, 360‐ and 130‐fold from the initial acquisition day to 10, 15 and 20 days, respectively. Additionally, the pathogen was successfully transmitted to 67% of citrus seedlings by emerging adults. Our data suggested that multiplication of the bacterium into the psyllids is essential for an efficient transmission and show that it is difficult for adults to transmit the pathogen unless they acquire it as nymphs.     

Plant volatiles and density-dependent conspecific female odors are used by Asian citrus psyllid to evaluate host suitability on a spatial scale

We investigated how chemical cues derived from female Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Liviidae) and their host plants affect host acceptance choices by conspecifics. In four-choice cage and two-choice olfactometer assays, female psyllids avoided conspecific female cues in a density-dependent manner. However, odors from citrus plants actively damaged by psyllid feeding were attractive to conspecific females. When odors from feeding-damaged plants were presented simultaneously with odors from female D. citri, attraction of female conspecifics was no longer observed as compared with a clean air control in olfactometer assays. In subsequent experiments, D. citri females were released within arenas that contained actively feeding-damaged or non-damaged (control) citrus plants, each with previously psyllid-infested and uninfested young leaves. D. citri development is linked to the presence of these newly emerging leaves which is the only site of nymphal development. Female D. citri were initially attracted by the actively damaged plants as compared with non-damaged controls. After acceptance of plants that were actively damaged by feeding, D. citri females preferentially chose and settled on uninfested young leaves as compared with previously infested young leaves. A herbivore-induced plant volatile attractant and a female-specific odor repellent appear to be complementary foraging cues providing psyllids with information at two spatial scales: (1) the whole plant level for choosing a plant potentially harboring male conspecifics for mating, and (2) the within plant level to reduce intra-conspecific competition by identifying previously exploited resources.     

Zebra chip disease incidence on potato is influenced by timing of potato psyllid infestation, but not by the host plants on which they were reared

Abstract  The Zebra chip (ZC) syndrome is an emerging disease of potato and a major threat to the potato industry. The potato psyllid, Bactericerca cockerelli (Sulc) is believed to be a vector of the ZC pathogen, which is now thought to be Candidatus Liberibacter, a bacterium. To further understand the relationship between potato psyllid infestation and ZC disease expression, healthy potato plants at different growth stages (4, 6 and 10 weeks after germination) were exposed separately to potato psyllids that were separately reared on four solanaceous hosts plants (potato, tomato, eggplant or bell pepper) for more than 1 year. ZC symptoms, leaf rates and total nonstructural carbohydrate accumulation in leaves and tubers of healthy and psyllid-infested plants were monitored and recorded. Typical ZC symptoms were observed in leaves and tubers of all plants exposed to potato psyllids regardless of the host plant on which they were reared. This was also accompanied by significant reductions in net photosynthetic rate. Caged potato plants without exposure to potato psyllids (uninfested controls) did not show any ZC symptom in both foliage and in harvested tubers. Foliage damage and ZC expression were most severe in the potato plants that were exposed to potato psyllids 4 weeks after germination compared to plants infested at later growth stages. Tubers from potato psyllid-infested plants had significantly higher levels of reducing sugars (glucose) and lower levels of starch than those in healthy plants, indicating that potato psyllid infestation interfered with carbohydrate metabolism in either leaves or tubers, resulting in ZC expression.