Laboratory and Field Trials to Identify Sustainable Chemical Control Strategies for Trioza erytreae in European Citrus Orchards

Trioza erytreae (Del Guercio) is one of the psyllid insect vectors of the causal agents of huanglongbing. This paper proposes an assessment of the effectiveness of several pesticides with and without a pine oil-based organic adjuvant, in order to contain the spread and population of this pest and reduce the side effects on the Tamarixia dryi parasitoid. Five insecticides and their combinations with pine oil were sprayed against T. erytreae on citrus trees under semi-field and field conditions. The effect of the same treatments was assessed on T. dryi under laboratory conditions. All insecticides, except for acetamiprid, increased their effectiveness when combined with pine oil under both conditions. Cyantraniliprole, dimethoate, and their respective combinations with the organic adjuvant showed the highest efficacies against T. erytreae. Under laboratory conditions, dimethoate reported the most negative effect on T. dryi activity whereas cyantraniliprole and its combination with pine oil yielded a low toxicity effect on this parasitoid. Our results recommend the development of an integrated control approach for citrus growers based on an insecticide rotation program, preventing the emergence of pest resistance to one substance. In this sense, other insecticides, such as lambda-cyhalothrin with pine oil adjuvant or acetamiprid, could be considered.

Insights into the origin of the invasive populations of Trioza erytreae in Europe using microsatellite markers and mtDNA barcoding approaches

The African citrus psyllid Trioza erytreae is one of the major threats to citrus industry as the vector of the incurable disease known as huanglongbing (HLB) or citrus greening. The psyllid invaded the northwest of the Iberian Peninsula 6 years ago. The invasion alarmed citrus growers in the Mediterranean basin, the largest citrus producing area in Europe, which is still free of HLB. Before our study, no research had been carried out on the genetic diversity of T. erytreae populations that have invaded the Iberian Peninsula and the archipelagos of the Macaronesia (Madeira and the Canary Islands). In this study, combining microsatellites markers and mtDNA barcoding analysis, we characterize the genetic diversity, structure and maternal relationship of these new invasive populations of T. erytreae and those from Africa. Our results suggest that the outbreaks of T. erytreae in the Iberian Peninsula may have derived from the Canary Islands. The populations of T. erytreae that invaded Macaronesia and the Iberian Peninsula are likely to have originated from southern Africa. We anticipate our results to be a starting point for tracking the spread of this invasive pest outside of Africa and to be important for optimizing contingency and eradication plans in newly invaded and free areas.

Host plant preference of Trioza erytreae on lemon and bitter orange plants

Trioza erytreae, the African citrus psyllid, is a vector of Candidatus Liberibacter spp., the causal agent of the citrus greening disease or Huanglongbing (HLB). The spread of the vector throughout the Iberian Peninsula has been continuous since its introduction in mainland Spain in 2014. The patterns of host preference and feeding behaviour largely depend on olfactory cues. Understanding these patterns is crucial to prevent further dispersion and develop management measures against the pest. In this work, a series of settlement, olfactometric, probing, and feeding experiments were conducted to assess the host preference of T. erytreae for lemon or bitter orange plants. The settlement experiment provided evidence on the preference of both sexes of T. erytreae for lemon plants, whereas males did not show any significant choice pattern in the case of the olfactometric assays. Forty EPG variables were analysed to describe and compare the probing and feeding behaviour of T. erytreae on lemon and bitter orange plants. The EPG variables indicated that T. erytreae has some difficulties in accepting the phloem of bitter orange plants. This suggests that lemon plants would be a better source for the acquisition of Candidatus Liberibacter asiaticus (CLas) by T. erytreae since the psyllid spends much longer periods feeding from the phloem on lemon than on bitter orange.

Feeding and Oviposition Behaviour of Trioza erytreae (Hemiptera: Triozidae) on Different Citrus Rootstock Material Available in Europe

Trioza erytreae (Del Guercio, 1918) (Hemiptera: Triozidae) is a vector of Candidatus Liberibacter spp., the causal agent of Huanglongbing disease (HLB). This study evaluates the preference of T. erytreae in different citrus seedlings. Thus, six different non-grafted citrus rootstocks were used for these experiments: (a) Carrizo citrange; (b) Citrus macrophylla; (c) ‘Cleopatra’ mandarin; (d) Forner-Alcaide No. 5; (e) Forner-Alcaide No. 517, and (f) Poncirus trifoliata (‘Flying Dragon’). The behaviour and survival of this psyllid was evaluated through the feeding preference of T. erytreae adults for different rootstocks (in a choice trial under greenhouse conditions) and oviposition and survival of T. erytreae adults on the different citrus material (in a no-choice trial under laboratory conditions). Trioza erytreae showed a clear preference for hosting and feeding on C. macrophylla, and Carrizo citrange was the most suitable rootstock for insect reproduction and survival followed by C. macrophylla. Conversely, Poncirus trifoliata was the least attractive rootstock to T. erytreae adults in the greenhouse trial and led to significantly lower T. erytreae survival. Our results suggest that conventional citrus rootstocks, such as Carrizo citrange and C. macrophylla, could increase T. erytreae populations.

Does the African Citrus psyllid, Trioza erytreae (Del Guercio) (Hemiptera: Triozidae), Represent a Phytosanitary Threat to the Citrus Industry in Mexico?

The African citrus psyllid, Trioza erytreae (Del Guercio) (Hemiptera: Triozidae), is a vector of Candidatus Liberibacter africanus (CLaf), a pathogen that causes huanglongbing (HLB) in Africa. Trioza erytreae has invaded areas of Asia and Europe and has threatened citrus production due to its biological habits and the transmission of CLaf. Mexico is a country where citrus production has a vital role from the economic and social point of view. Therefore, ecological niche modeling (ENM) was used to determine if Mexico has the environmental availability that will allow T. erytreae invasion. We analyzed whether or not the distribution of Casimiroa edulis La Llave (Rutaceae) in the country could be a factor that enables the dispersal of T. eytreae. The environmental connectivity between five points of entry into the country (two ports and three airports) was explored to determine possible routes of dispersal of T. erytrae. The results showed that Mexico has wide availability for the invasion of the African citrus psyllid, which coincides with essential citrus areas of the country and with the distribution of C. edulis. Of the entry points studied, the Port of Veracruz showed nearby areas with environmental connectivity. Preventive monitoring measures for T. erytreae in Mexico should focus on Veracruz state because it has an entry point, ideal environmental availability, citrus areas, and specimens of C. edulis.

Engineered Orange Ectopically Expressing the Arabidopsis β-Caryophyllene Synthase Is Not Attractive to Diaphorina citri, the Vector of the Bacterial Pathogen Associated to Huanglongbing

Huanglongbing (HLB) is a destructive disease, associated with psyllid-transmitted phloem-restricted pathogenic bacteria, which is seriously endangering citriculture worldwide. It affects all citrus species and cultivars regardless of the rootstock used, and despite intensive research in the last decades, there is no effective cure to control either the bacterial species (Candidatus Liberibacter spp.) or their insect vectors (Diaphorina citri and Trioza erytreae). Currently, the best attempts to manage HLB are based on three approaches: (i) reducing the psyllid population by intensive insecticide treatments; (ii) reducing inoculum sources by removing infected trees, and (iii) using nursery-certified healthy plants for replanting. The economic losses caused by HLB (decreased fruit quality, reduced yield, and tree destruction) and the huge environmental costs of disease management seriously threaten the sustainability of the citrus industry in affected regions. Here, we have generated genetically modified sweet orange lines to constitutively emit (E)-β-caryophyllene, a sesquiterpene repellent to D. citri, the main HLB psyllid vector. We demonstrate that this alteration in volatile emission affects behavioral responses of the psyllid in olfactometric and no-choice assays, making them repellent/less attractant to the HLB vector, opening a new alternative for possible HLB control in the field.