Plant diseases caused by, or associated with, phytoplasmas occur in hundreds of commercial and native plants, causing minor to extensive damage. Insect vectors, primarily leafhoppers, planthoppers, and psyllids, have been identified for relatively few phytoplasma diseases, limiting the capacity of managers to make informed decisions to protect crops and endangered indigenous plants. In the past two decades our knowledge of insect vector-phytoplasma interactions has increased dramatically, allowing researchers to make more accurate predictions about the nature and epidemiology of phytoplasma diseases. These better-characterized systems also may provide clues to the identity of insect vectors of other phytoplasma-associated diseases. We review the literature addressing the ecology of insect vectors, phytoplasma-insect ecological and molecular interactions, vector movement and dispersal, and possible management strategies with an emphasis on research from the past 20 years.

Insect vectors of phytoplasmas

Diaphorina citri Kuwayama (Hemiptera: Psyllidae) carries Candidatus liberibacter spp., the putative causal agents of Huanglongbing. D. citri reproduces and develops only on the flushing shoots of its rutaceous host plants. Here we examined whether D. citri is attracted to host plant odors and a mixture of synthetic terpenes. Tests conducted in a vertically oriented Y-tube olfactometer showed that both males and females preferentially entered the Y-tube arm containing the odor from the young shoots of Murraya paniculata (L.) Jack and Citrus limon L. Burm. f. cultivar Eureka. Only males exhibited a preference for the odor of C. sinensis L., whereas the odor of C. × paradisi MacFadyen cultivar Rio Red was not attractive to both sexes. The volatiles emitted by young shoots of grapefruit cultivar Rio Red, Meyer lemon (Citrus × limon L. Burm.f.), and M. paniculata were analyzed by gas chromatograph-mass spectrometry. The samples were comprised of monoterpenes, monoterpene esters, and sesquiterpenes. The number of compounds present varied from 2 to 17, whereas the total amount of sample collected over 6 h ranged from 5.6 to 119.8 ng. The quantitatively dominant constituents were (E)-β-ocimene, linalool, linalyl acetate, and β-caryophyllene. The attractiveness of a mixture of synthetic terpenes, modeled on the volatiles collected from M. paniculata, was evaluated in screened cages in a no-choice test. At three observation intervals, significantly more individuals were trapped on white targets scented with the mixture than on unscented targets. These results indicate the feasibility of developing D. citri attractants patterned on actual host plant volatiles.

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Responses of the Asian Citrus Psyllid to Volatiles Emitted by the Flushing Shoots of Its Rutaceous Host Plants

Diaphorina citri Kuwayama (Hemiptera: Psyllidae) is an important worldwide pest of citrus that vectors bacteria (Candidatus Liberibacter spp.) responsible for huanglongbing (citrus greening disease). We examined the behavioral responses of mated and unmated D. citri of both sexes to odors from host plants in a Y-tube olfactometer, with and without visual cues. The host plants tested were 'Duncan' grapefruit (Citrus paradisi Macfayden), sour orange (Citrus aurantium L.), navel orange (C. sinensis L.), and Murraya paniculata L. Jack. Responses varied by plant species, psyllid sex and mating status, and the presence of a visual cue. Evidence of attraction generally was stronger in females and in mated individuals of both sexes relative to virgins. The presence of a visual cue typically enhanced attractiveness of olfactory cues; in no case did unmated individuals show evidence of attraction to host plant odors in the absence of avisual cue. In the absence of visual cues, mated females and males showed evidence of attraction only to odors from sour orange and navel orange, respectively. Psyllids exhibited anemotactic responses when assayed with plant odors alone but showed strong evidence of attraction only when olfactory and visual cues were combined, suggesting that olfactory cues facilitate orientation to host plants but may be insufficient alone. Antennal responses to citrus volatiles were confirmed by electroantennogram. The results reported here provide evidence that D. citri uses olfactory and visual cues in orientation to host plants and suggest the possibility of using plant volatiles in monitoring and management of this pest.

https://bioone.org/journals/Environmental-Entomology/volume-38/issue-1/022.038.0128/Roles-of-Olfactory-Cues-Visual-Cues-and-Mating-Status-in/10.1603/022.038.0128.pdf

Roles of olfactory cues, visual cues, and mating status in orientation of Diaphorina citri Kuwayama (Hemiptera: Psyllidae) to four different host plants.

Flavescence doree is a serious disease for European vine growers. Indeed, Flavescence doree causes yield losses and lower grape quality. As a consequence, Flavescence doree is costly and needs advanced control strategies. For instance, in 2005, 34 million Euro was given to Italian vine growers to compensate losses due to the disease. The infection by Flavescence doree results from the association of a phytoplasma and the leafhopper vector, Scaphoideus titanus. Despite mandatory controls using insecticides, Flavescence doree is still spreading in Europe. Here, we review the biology and ecology of S. titanus to suggest improved management techniques. The main findings are as follows. (1) The long-distance spread of S. titanus is mainly due to human activities, and all European vineyards are susceptible to be colonized. (2) S. titanus is an efficient vector because it can reach a high population level and it is specific to Vitis spp. (3) Current control and prophylaxis are insufficiently effective. (4) Variation in vector populations and vector capacities lead to differential risks of plant infection. Factors driving such population variations could be modeled to improve S. titanus control. (5) Feeding behavior is a key factor in the phytoplasma–vector relationship. (6) The infection risk is mainly limited by vector control. To decrease pesticide use, a cross survey of the vector population and of the infected stocks triggers mandatory treatments. (7) Alternative sustainable methods or strategies are required to reduce insecticide use and increase control efficiency. In the short term, new models could support the establishment of more sustainable pest management operations. In the long term, innovative techniques involving symbionts, mating disruption and a push–pull strategy could improve S. titanus and Flavescence doree control with less environmental impact.

https://hal.archives-ouvertes.fr/hal-01234829/document

Biology and ecology of the Flavescence dorée vector Scaphoideus titanus : a review

Evolutionary and biological patterns can be obscured by inadequate or ill-defined terminology. An example is the generally very specific relationship between the sap-feeding hemipteran group, psyllids, and their breeding plants, commonly called host-plants. The literature is clogged with references to so called ‘hosts’, which are often merely plants on which psyllids were found accidentally, and no immature development was detected. Recently the term host has also been applied by some authors to any plant on which immature or adults feed. Here we propose a terminology to clarify associated plant definitions, and we suggest restricting the use of the term host-plant to plants on which a psyllid species completes its immature to adult life cycle. For the other plant associations we suggest the terms overwintering or shelter plant (plants on which adult psyllids overwinter and on which they may feed), food plant (plants on which adult psyllids feed, but do not breed and do not spend an extended period of time) and casual plant (plants on which adult psyllids land but do not feed).

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Psyllid host-plants (hemiptera: psylloidea): resolving a semantic problem

Chemical communication was shown to play a role in the pear psylla, Cacopsylla bidens. Electrophysiological (EAG) and behavioral responses were investigated in males and females pear psylla . Males were found to be attracted to females, and especially to those on host plants, but not to males, uninfested host plants, or plants infested with conspecific larvae. On the other hand, females were not attracted to males or females but displayed some attraction to host plants. Furthermore, females showed a preference for uninfested pear versus plants infested with conspecific larvae. The antennae of males gave highest electroantenographic response to volatiles from pears infested with females but not males, while females, responded also toward the volatiles of pear alone. These results indicate that females of C. bidens emit sex pheromones that are attractive to the males and suggest that, host volatiles may play a role in host selection by pear psylla females.

The role of chemical cues in host and mate location in the pear psylla Cacopsylla bidens (Homoptera: Psyllidae)

Hyalesthes obsoletus Signoret (Homoptera: Cixiidae) is a polyphagous planthopper that transmits stolbur phytoplasma (a causative agent of “yellows” disease) to various weeds, members of the Solanaceae, and wine grapes (Vitis vinifera L.) in Europe and the Middle East. Planthoppers were collected by hand vacuuming eight native plant species. Vitex agnus-castus L., a shrub in the Verbenaceae, hosted the largest number of H. obsoletus, although Olea europaea L. also served as a host for adults. Using a Y-olfactometer, we compared the planthoppers relative preference for V. agnus-castus, Convolvulus arvensis, and V. vinifera. V. agnus-castus was more attractive to both male and female H. obsoletus than the other plants. H. obsoletus antennal response was stronger to volatiles collected from V. agnus-castus than from Cabernet Sauvignon variety of V. vinifera. To determine if V. agnus-castus would serve as a reservoir for the pathogen, H. obsoletus were collected from leaf and stem samples of native V. agnus-castus, and were tested by polymerase chain reaction (PCR) for the presence of phytoplasma DNA. While 14% and 25% (2003 and 2004, respectively) of the insects tested positive for phytoplasma DNA, none of the plant samples tested positive. To determine if V. agnus-castus could serve as a host plant for the development of the planthopper, we placed emergence cages beneath field shrubs and enclosed wild-caught H. obsoletus in a cage with a potted young shrub. We found adult H. obsoletus in the emergence cases and planthopper nymphs in the soil of the potted plant. We concluded that V. agnus-castus is attractive to H. obsoletus, which seems to be refractory to phytoplasma infections and warrants further testing as a trap plant near vineyards.

S. Daniel Wesley

Papers

The role of chemical cues in host and mate location in the pear psylla Cacopsylla bidens (Homoptera: Psyllidae)

Vitex agnus-castus is a preferred host plant for Hyalesthes obsoletus.