Effect of host deprivation on the foraging behavior of the Asian citrus psyllid parasitoid Tamarixia radiata: observations from the laboratory and the field

The Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Liviidae), is a significant citrus pest and the parasitoid Tamarixia radiata (Waterston) (Hymenoptera: Eulophidae) has been released in various citrus‐producing areas in classical biological control programs targeting D. citri. We investigated the effect of host deprivation on the foraging behavior and patch utilization by T. radiata. In the laboratory, females deprived of hosts for 3 days tended to leave patches of 12 nymphs without parasitizing hosts during the ca. 30 min they spent in the patch before leaving. Moreover, half of these females failed to host feed, and those that did host feed, on average, needed more than 15 min to complete feeding. Conversely, non‐host‐deprived females parasitized on average three nymphs before leaving patches without host feeding during the ca. 39 min they spent in the patch. These laboratory observations were compared to mass‐reared female T. radiata that were released onto colonies of D. citri nymphs infesting citrus in the field. Release vials were provisioned with honey and these females had no opportunities to host feed over the 1‐ to 2‐day containment period prior to release. When introduced onto D. citri colonies, 68% T. radiata females abandoned D. citri patches prior to probing hosts, in part, because Argentine ants, Linepithema humile (Mayr) (Hymenoptera: Formicidae), tending colonies disturbed searching parasitoids. These results from laboratory and field studies are discussed in the context of classical biological control, with the aim of understanding how to manipulate host availability and ant activity so establishment rates and impact of T. radiata can be improved.     

Presence and abundance of Diaphorina citri in Murraya paniculata in urban areas free of huanglongbing in Brazil

Asian citrus psyllid (ACP), Diaphorina citri Kuwayama (Hemiptera: Liviidae), is the vector of the bacterium Candidatus Liberibacter sp., a quarantine pathogen in citrus production areas such as Australia, Europe, and northeast Brazil, associated with huanglongbing (HLB). The psyllids’ preferred host is Murraya paniculata (L.) Jacq. (Rutaceae), an ornamental plant native to Asia and Oceania, and commonly found in urban areas next to citrus groves around the world. As there are insecticide application restrictions for urban areas, monitoring and use of biological control to suppress ACP are essential for an area-wide HLB management strategy, especially for production areas predominantly composed of small citrus farms. For this, it is necessary to understand the occurrence cycles of ACP and vegetative flush of the ornamental host. This study characterized the occurrence cycles of M. paniculata flush shoot and accumulated rainfall, and the association with ACP presence (proportion of monitored trees) and abundance (per tree) in a Brazilian urban area free of HLB. A 3-year time series was constructed using spectral and co-spectral analysis. Spectral analysis showed the occurrence of at least seven flush shoot cycles of M. paniculata, nearly 10 ACP presence and abundance cycles, and monthly cycles of accumulated rainfall. Cycles of ACP presence were associated with ACP abundance, with ACP presence cycles occurring around 7 days before ACP abundance cycles and the correlation and co-spectral analyses indicated an almost simultaneous occurrence of the main cycles of M. paniculata flush shoots and ACP occurrence. These findings will facilitate the development of an ACP biological control program based on parasitoid releases in urban areas in HLB-free citrus groves.     

In vitro egg hatching of Diaphorina citri,the vector of Huanglongbing

Citrus greening (Huanglongbing, HLB) is a destructive disease associated with the uncultivable, phloem-limited, gram-negative bacteria Candidatus Liberibacter spp., which affects citrus crops and other Rutaceae species. HLB is rapidly transmitted by the Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Liviidae). We developed an artificial medium on which D. citri eggs can hatch and first-instar nymphs can feed. The medium could be used to study insect physiology and screen molecules that may interfere with egg hatching and nymph development.     

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.     

Effect of host‐plant and infection with ‘Candidatus Liberibacter asiaticus’ on honeydew chemical composition of the Asian citrus psyllid,Diaphorina citri

The Asian citrus psyllid (ACP), Diaphorina citri Kuwayama (Hemiptera: Liviidae), transmits the citrus greening pathogen ‘Candidatus Liberibacter asiaticus’ (CLas) by feeding on citrus phloem sap. Because phloem sap is rich in sugars but low in amino acids, ACP sucks large quantities and excretes most of it as honeydew. We studied the chemical composition of ACP honeydew on various host plants. Honeydew samples were analyzed with gas chromatography–mass spectrometry. Fourteen sugars, 13 amino acids, and six organic acids were detected in the honeydew of ACP. Sugars composed about 95% of the total compounds. Sucrose and trehalose were the predominant sugars, composing about 58 and 23% of the total sugars, respectively. Proline, asparagine, aspartic acid, and glutamic acid were the most abundant amino acids in ACP honeydew. The host plant and its infection with CLas had some effect on the honeydew composition. Glucose, chiro‐inositol, myo‐inositol, inositol, maltose, and turanose were lower in honeydew collected from CLas‐infected citrus compared to that collected from non‐infected trees. In CLas‐infected citrus (pineapple sweet orange, Citrus sinensis L. Osbeck) and Bergera koenigii (L.) Spreng. [curry leaf tree (both Rutaceae)] honeydews, valine, alanine, serine, glutamine, glycine, and the organic acids were lower than in honeydew from healthy citrus. Mannose, galactose, inositol, mannitol, an unknown disaccharide, and proline were higher in the honeydew collected from B. koenigii than in honeydew collected from healthy citrus (pineapple sweet orange), whereas fructose, chiro‐inositol, myo‐inositol, trehalose, and lactic acid were lower. The findings of this study help us understand the metabolism and the nutrient needs of ACP that transmits CLas, the pathogen of huanglongbing in citrus.     

Feeding behavior of Diaphorina citri and its transmission of ‘Candidatus Liberibacter asiaticus’ to citrus

Huanglongbing (HLB), also known as citrus greening, is currently the most destructive disease of citrus, responsible for huge economic losses in the world's major citrus production areas. The Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Liviidae), transmits ‘Candidatus Liberibacter asiaticus’ (Clas), the pathogen responsible to cause HLB. Understanding of vector, pathogen, and host plant interactions is important for the management of this vector‐disease complex. We used the direct‐current electrical penetration graph (DC‐EPG) system to evaluate feeding behavior of Clas‐infected D. citri adults, and their potential to transmit the pathogen to healthy citrus, Citrus reticulata Blanco cv. Sunki (Rutaceae), following a 24‐h inoculation access period. Plants were tested for the presence of Clas by qPCR 6 months after inoculation. Findings suggest that inoculation was associated with salivation into the phloem sieve elements (waveform E1). The minimum feeding time for successful transmission by a single adult was 88.8 min, with a minimum E1 duration of 5.1 min. Regression analysis indicated a significant relationship between E1 duration and transmission efficiency. The adults successful in transmitting Clas to healthy citrus were able to penetrate and feed in the phloem much earlier than those which did not transmit. The minimum duration of E1 for a female was shorter than that of a male, but transmission was higher. However, durations of other EPG parameters were not significantly different between male and female. Feeding by single Clas‐infected D. citri adults on 6‐month‐old plants (Sunki) resulted in 23% HLB‐positive plants 6 months after inoculation. Multiple nymphs or adults could transmit the pathogen more efficiently than individual adults in the field, and further enhance the severity of the disease. Effective tactics are warranted to control D. citri and disrupt transmission of Clas.     

Temporal response and attraction of Diaphorina citri to visual stimuli

As the vector of the global disease of citrus greening or huanglongbing, Asian citrus pysllids, Diaphorina citri Kuwayama (Hemiptera: Liviidae), are the greatest threat to the worldwide citrus industry. Critical to management of D. citri and huanglongbing is optimization of surveillance methodologies. Although phytophagous insects may find host plants by multimodal cues, some appear to primarily use visual cues. In this study, we examined the behavior of Asian citrus psyllids toward light from light‐emitting diodes (LEDs) in the insect visible spectrum. The periodicity of attraction of psyllids to visual cues was evaluated in the field (yellow sticky traps) and laboratory (multi‐colored LEDs) with a strong peak of activity during the afternoon in both the field and the laboratory (both 14:00 to 18:00 hours). In laboratory evaluations of psyllids to differently colored LEDs, strongest attraction was to LEDs emitting ultraviolet (390 nm), green (525 nm), and yellow (590 nm) light. Male and female psyllids did not differ significantly in their responses to visual cues. These findings provide the basis for formulating better traps that reflect UV and yellow light and potentially incorporate UV LEDs for monitoring psyllids and a better understanding of Asian citrus psyllid visual behavior.     

Sedge and rush-feeding psyllids of the subfamily Liviinae (Insecta: Hemiptera: Psylloidea): a review

The jumping plant-lice or psyllids belonging to the subfamily Liviinae are reviewed. Nineteen species are recognized in a single genus Lima Latreille. Three new species, craivfordi sp. nov., lobata sp. nov. and manitobensis sp. nov., are described. The identities of the existing species have been widely confused and full lists of synonymies are given where appropriate. It is re-emphasized that the type species of Livia, Psylla juncorum Latreille, is a synonym of Chermes junci Schrank, a point made by Laing (1951) but ignored by subsequent authors. The latter name has priority. A taxonomic key for the identification of the species is given and each species is described, diagnosed and illustrated. Supporting information is given on geographical distribution, host-plant association and general biology. Evolutionary relationships within Livia are discussed.