Behavioral responses of Diaphorina citri to host plant volatiles in multiple-choice olfactometers are affected in interpretable ways by effects of background colors and airflows.

Haroldo Xavier Linhares Volpe,Marcelo Pedreira De Miranda,Renato De Freitas,Jennifer Yslaine Delfino,Rômulo Igor De Carvalho,Leandro Peña,Victoria Esperança,Nelson Arno Wulff,Odimar Zanuzo Zanardi,Rodrigo Facchini Magnani,Tatiana Aparecida Mulinari,Rejane Angélica Grigio Luvizotto,Richard Mankin

doi:10.1371/journal.pone.0235630

Haroldo Xavier Linhares Volpe, Marcelo Pedreira De Miranda + Show 11 more

Open Access

https://doi.org/10.1371/journal.pone.0235630

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Abstract

In several phytophagous hemipterans, behavior appears to be mediated by both visual and chemical cues. For the Asian citrus psyllid (ACP) Diaphorina citri (Hemiptera: Liviidae), olfactometric assays are generally difficult to interpret owing to the low proportion of individuals responding to odors (~30–40%), which compromises the efficiency and reliability of the results of behavioral tests. In the present study, the ACP behavioral response to emitted odors from sweet orange (Citrus sinensis L. Osbeck) flushes in a 4-arm olfactometer using different colors (four white-, two white- and two yellow- on opposite sides, or four yellow-colored fields), and the role of the airflow in the concentration of volatile organic compounds (VOCs) were assessed at two airflows [0.4 and 0.1 L/min (LPM)]. Exposure to ‘Pera’ sweet orange or clean air in treatments with four yellow-colored-fields increased the response rate of ACP females to the odor sources compared with exposure to ‘Pera’ sweet orange or clean air in treatments with four white-colored-fields, independently of the odor source and airflow tested. For the assays using two white- and two yellow-colored fields on opposite sides and 0.4 or 0.1 LPM airflow, the residence time of ACP females to odors (‘Pera’ sweet orange or clean air) was similar or higher in treatments using yellow- than those using white-colored fields. For both assays (VOCs and olfactometric behavioral parameters), the reduction in airflow from 0.4 to 0.1 LPM greatly changed the airborne concentration and ACP behavior. Quantitative chemical analyses revelead that the concentration of most compounds emitted by ‘Pera’ sweet orange flushes for the headspace using 0.1 LPM airflow were greater than the concentrations measured using 0.4 LPM airflow. Therefore, this treatment design provides an useful tool to assess the ACP behavioral response to the odors from citrus plants, and it can also help in the discrimination of dose-response screenings for VOCs or conspecific insects.

Highlights

The Asian citrus psyllid (ACP) Diaphorina citri Kuwayama (Hemiptera: Liviidae) is one of the main citrus pests worldwide because it is a vector of the bacteria Candidatus Liberibacter spp., which are associated with Huanglongbing, the most devastating disease of citrus worldwide [1]
The four-yellow-colored-field device resulted in a significant increase in the proportion of responding ACP females in relation to the four-white-colored-field device for clean air × clean air (0.4 LPM) (χ2 = 6.8102; d.f. = 1; P = 0.0091), ‘Pera’ sweet orange × clean air (0.4 LPM) (χ2 = 14.805; d.f. = 1; P = 0.0001), ‘Pera’ sweet orange × ‘Pera’ sweet orange (0.4 LPM) (χ2 = 17.143; d.f. = 1; P < 0.0001), ‘Pera’ sweet orange × clean air (0.1 LPM) (χ2 = 42.140; d.f. = 1; P < 0.0001), and ‘Pera’ sweet orange × ‘Pera’ sweet orange (0.1 LPM) (χ2 = 15.619; d.f. = 1; P < 0.0001) treatments (Table 1)
Our results showed that the four-yellow-colored-field device increased the proportion of ACP females responding to odors compared with the four-white-colored-field device, regardless of the odor source and airflow used in treatments

Summary

Introduction

The Asian citrus psyllid (ACP) Diaphorina citri Kuwayama (Hemiptera: Liviidae) is one of the main citrus pests worldwide because it is a vector of the bacteria Candidatus Liberibacter spp., which are associated with Huanglongbing, the most devastating disease of citrus worldwide [1]. Doring and Chittka [10] revealed that some species positively responded to colors from the green domain of the spectrum with negative input from the blue and/or UV range. These same authors suggested that the aphid preference for yellow in field assays was not related to the true color but that additional brightness effects were involved. In terms of long-distance flight for ACP involving only visual cues, Hall et al [15] demonstrated that yellow stick cards were the most attractive to adults. Chemical volatile cues from Rutaceae are important for ACP hostplant location [20,21,22]

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