Development of semiochemical-based tools for the management of the African citrus triozid (ACT) Trioza erytreae Del Guercio (Hemiptera: Triozidae)

Abstract

Citrus fruits are one of the world’s major fruit crops, ranking first in trade value among all fruits and significantly contributing to global food and nutritional security. In Africa, South Africa is the leading producer of citrus with an annual production of 2.4 million tons whereas the leading producers in East Africa are: the United Republic of Tanzania and Kenya with an annual output of about 500,000 and 190,000 tons, respectively in 2017. The reason for this low production is attributed to the incidence of the African citrus triozid (ACT), Trioza erytreae Del Guercio (Hemiptera: Triozidae) and other pests and diseases. In Kenya, T. erytreae is considered the most important pest only after aphids, Toxoptera citricidus Kirklady. Though T. erytreae causes death of young shoots, it is considered economically important because it vectors “Candidatus” Liberibacter africanus (CLaf), causative bacteria of the citrus greening disease (CGD). Citrus greening disease and its Asian counterpart, Huanglongbing (HLB) vectored by the Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Liviidae) are the most economically important diseases of citrus worldwide. Since the greening disease has no known cure, management is mainly aimed at the vector. Using behavioural assays and chemical analysis, the interaction between T. erytreae and Citrus jambhiri Lush. (Sapindales: Rutaceae), a common host plant was studied. Nine- and three- component blends comprising limonene, sabinene and β-ocimene, the most abundant terpenes in rough lemon volatiles, were identified from the healthy host plant as a potential arrestment/short-range host location cue for T. erytreae. However, a six-component blend lacking in these three components elicited an avoidance response in both sexes. Trioza erytreae-infested host plants were unattractive to T. erytreae. On the other hand, Tamarixia dryi Waterston (Hymenoptera: Eulophidae), the nymphal parasitoid of T. erytreae was attracted to both uninfested and infested host plants, when they were presented simultaneously with plain air. However, when presented with uninfested and infested host plants simultaneously, it preferred the latter. Chemical analysis of T. erytreae-infested plants revealed the induction of Methyl N-methylanthranilate (MNMA) and methyl anthranilate (MeA). Thus, these compounds could be responsible for the observed avoidance by T. erytreae, suggesting, that citrus plant is able to defend itself against herbivory. (E)-β-Caryophyllene was upregulated in CLaf-infected plants and it was shown to increase attraction of T. erytreae to the infected plants. Additionally, methyl salicylate (MeSA), (E)-4,8-dimethyl-1,3,7-nonatriene (DMNT), p-ethyl acetophenone and geranyl acetone, among other compounds were induced in the diseased plants. The effect of non-host plants volatiles, lemongrass (Cymbopogon citratus (DC) Stapf (Poales: Poaceae)), garlic (Allium sativum L. (Asparagales: Amaryllidaceae)) and guava (Psidium guajava L. (Myrtales: Myrtaceae)) were screened against T. erytreae responses using a newly developed cage assay. Results showed that garlic and guava but not lemongrass odours, possessed repellent effect against triozids, thus can be potential border plants which can be used to manage T. erytreae in citrus nurseries or orchards. These findings help to better understand the chemical ecology of the triozid and its interspecific relationships with host and non-host plants. Identified kairomones and repellent crops can be useful in a push-pull strategy against the pest.