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1 June 2017 Feeding and Oviposition of Diaphorina citri (Hemiptera: Liviidae) on Helietta apiculata (Sapindales: Rutaceae): a Potential Host?
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This study evaluated the survival and fertility of the huanglongbing vector Diaphorina citri Kuwayama (Hemiptera: Liviidae) on 2 species of the family Rutaceae, Murraya exotica L. (Sapindales: Rutaceae) and Helietta apiculata Bentham (Sapindales: Rutaceae). Females of D. citri oviposited on both hosts. The survival of D. citri was similar on both hosts until day 7 of confinement on the plants. Helietta apiculata can support D. citri in regions where the vector's main host (M. exotica) or citrus groves are absent, a potential factor in the dispersal and epidemiology of huanglongbing.

The Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Liviidae), is the main vector of the bacteria associated with huanglongbing or HLB. This disease currently is considered the most harmful for the citrus industry worldwide (Bové 2006; Grafton-Cardwell et al. 2014). HLB is thought to be caused by the bacteria ‘Candidatus Liberibacter asiaticus’ (Las), ‘Candidatus Liberibacter americanus’ (Lam), and ‘Candidatus Liberibacter africanus’ (Laf) (Rhizobiales: Rhizobiaceae) (Machado 2010).

Lopes et al. (2009) suggested that the bacteria may lack host specificity, i.e., that they may be capable of infecting several alternative hosts. If this is so, then plant species in certain regions may be acting as a source of bacteria, which the insect vector can acquire and transmit to citrus plants.

The Asian citrus psyllid can exploit a large number of host plants, especially species of the family Rutaceae (Aubert 1987). Among the main hosts are orange jasmine Murraya exotica L. (a synonym for Murraya paniculata [L.] Jacquin) (Sapindales: Rutaceae) and species and varieties of the genus Citrus (Sapindales: Rutaceae) (Halbert & Manjunath 2004; Teck et al. 2011; Alves et al. 2014; Sétamou et al. 2015). Although adults can feed on a wide assortment of Rutaceae, the insects cannot complete their development on all of them (Burckhardt et al. 2014). Alternative hosts for adults are important because they allow the psyllid to survive on these plants in the absence of more suitable hosts.

This study evaluated the survival and fertility of D. citri on 2 plant species, M. exotica and Helietta apiculata Bentham (Sapindales: Rutaceae). For the survival test, groups of 10 D. citri adults (10 d old) were confined in mesh sleeve cages on M. exotica or H. apiculata saplings. The experimental design was fully randomized, with 10 repetitions (insect groups) per treatment (host). Survival was evaluated 1, 3, 5, 7, 10, 17, 24, and 31 d after the confinement.

The fertility of D. citri on the 2 host species was estimated from the number of eggs laid on each plant in a confinement test (no-choice test). With mesh sleeve cages, 2 D. citri couples (12 d old) were confined for 72 h on the plants (which were approx. 25 cm in height). After this period, the insects were removed and the eggs counted with the aid of a stereoscopic microscope. The experimental design was fully randomized, with 10 repetitions (each consisting of 2 couples) per treatment (host). Both experiments were conducted under controlled conditions, with a temperature of 25 ± 2 °C, relative humidity of 60 ± 10%, and a photoperiod of 14:10 h L:D.

The data for survivorship and number of eggs were analyzed by generalized linear models (GLM) (Nelder & Wedderburn 1972) through a quasi-binomial and quasi-Poisson distribution, respectively; the F value was calculated by ANOVA with the model. The quality of fit was determined with a half-normal graph of probabilities with simulation envelope (Demétrio & Hinde 1997). All analyses were carried out with R software (R Core Team 2015).

The survival of D. citri was similar between the 2 hosts until day 7 of confinement (Fig. 1). By day 10 and afterwards, the survivorship differed between the hosts (F = 5.126; df = 1,19; P = 0.036), with increasingly reduced survival on H. apiculata, although an average of 50% of the insects survived on H. apiculata for 17 d after confinement (Fig. 1). The results obtained indicate that H. apiculata can serve as a food host for D. citri, thus helping the psyllid to survive during periods of food shortages. In general, on M. exotica about 85% of the insects survived to the end of the assessments (31 d), whereas only 20% of the insects on H. apiculata survived after 31 d (Fig. 1). El-Shesheny et al. (2016) also obtained 80% mean survival of D. citri on M. exotica.

Oviposition was higher (F = 14.723; df = 1,19; P = 0.012) on M. exotica, with a mean of 24.5 eggs per plant, than on H. apiculata, with a mean of 5.5 eggs per plant (Fig. 2), indicating that M. exotica was more suitable than H. apiculata for oviposition.

Fig. 1.

Survivorship of adults of Diaphorina citri on 2 rutaceous species. Means followed by the same letter did not differ in the glm test by quasi-binomial distribution (F = 5.126; df = 1,19; P = 0.036).


Fig. 2.

Mean number of eggs laid on 2 rutaceous species by Diaphorina citri during 72 h. Means followed by the same letter did not differ in the glm test by quasi-Poisson distribution (F = 14.723, df = 1,19; P = 0.012).


Oviposition on H. apiculata was significantly lower than that obtained on M. exotica; however, this does not eliminate the possibility that H. apiculata can serve as a potential host for D. citri, because a low oviposition rate is not directly associated with impaired development of the offspring (Thompson 1988; Mayhew 2001; Wise et al. 2008). In areas that lack its main host (M. exotica) or citrus groves, H. apiculata could help D. citri survive and may be important for insect dispersal and the epidemiology of HLB.

The results of this study indicate that H. apiculata can be considered an important host plant for the survival of the psyllid, especially in locations where H. apiculata is abundant, such as along the edges of citrus groves and in urban areas. The next step is to determine if this species can support the complete development of the psyllid (egg to adult) and to compare its attractiveness with that of other hosts. In addition to Citrus species and M. exotica, more than 30 species of the family Rutaceae are reported in the state of São Paulo, Brazil (REFLORA 2016), and all are potential candidates for future studies of the vector.

The ability of H. apiculata to serve as a host for the Candidatus Liberibacter species also should be investigated. Similarly, if D. citri can colonize H. apiculata, it should be determined whether transmission of the bacteria to the next generation of insects via the feeding site occurs in this host.

We extend our thanks to Janet W. Reid (JWR Associates) for English revision.

References Cited


Alves GR, Diniz AJF, Parra JRP. 2014. Biology of the huanglongbing vector Diaphorina citri (Hemiptera: Liviidae) on different host plants. Journal of Economic Entomology 107: 691–696. Google Scholar


Aubert B. 1987. Trioza erytreae Del Guercio and Diaphorina citri Kuwayama (Homoptera: Psylloidea), the two vectors of citrus greening disease: biological aspects and possible control strategies. Fruits 42: 149–162. Google Scholar


Bové JM. 2006. Huanglongbing: a destructive, newly-emerging, century-old disease of citrus. Journal of Plant Pathology 88: 7–37. Google Scholar


Burckhardt D, Queiroz DL, Malenovský I. 2014. First record of the Australian genus Platyobria Taylor, 1987 from Europe and P. biemani sp. nov. as a potential pest of Eucalyptus (Myrtaceae) (Hemiptera: Psylloidea). Entomologische Zeitschrift, Schwanfeld 124: 109–112. Google Scholar


Demétrio CGB, Hinde J. 1997. Half-normal plots and overdispersion. Glim Newsletter 27: 19–26. Google Scholar


El-Shesheny I, Hijaz F, El-Hawary I, Mesbah I, Killiny N. 2016. Impact of different temperatures on survival and energy metabolism in the Asian citrus psyllid, Diaphorina citri Kuwayama. Comparative Biochemistry and Physiology Part A 192: 28–37. Google Scholar


Grafton-Cardwell EE. 2014. The status of citrus IPM in California. Acta Horticulturae 1065: 1083–1090. Google Scholar


Halbert SE, Manjunath KL. 2004. Asian citrus psyllids (Sternorrhyncha: Psyllidae) and greening disease of citrus: a literature review and assessment of risk in Florida. Florida Entomologist 87: 330–353. Google Scholar


Lopes SA, Frare GF, Bertolini E, Cambra M, Fernandes NG, Ayres AJ, Marin DR, Bové JM. 2009. Liberibacters associated with citrus huanglongbing in Brazil: ‘Candidatus Liberibacter asiaticus’ is heat tolerant, ‘Ca. L. americanus’ is heat sensitive. Plant Disease 3: 257–262. Google Scholar


Machado AM, Locali-Fabris EC, Coletta-Filho HD. 2010. Candidatus Liberibacter spp., citrus huanglongbing agents. Citrus Research and Technology 31: 25–35. Google Scholar


Mayhew PJ. 2001. Herbivore host choice and optimal bad motherhood. Trends in Ecology and Evolution 16: 165–167. Google Scholar


Nelder JA, Wedderburn RWM. 1972. Generalized linear models. Journal of the Royal Statistical Society 135: 370–384. Google Scholar


R Core Team. 2015. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, (last accessed 27 Oct 2016). Google Scholar


REFLORA. 2016. Brazilian plants: historic rescue and virtual herbarium for knowledge and conservation of the Brazilian flora, (last accessed 28 Oct 2016). Google Scholar


Sétamou M, Graça JV, Sandoval II JL. 2015. Suitability of native North American Rutaceae to serve as host plants for the Asian citrus psyllid (Hemiptera: Liviidae). Journal of Applied Entomology 140: 645–654. Google Scholar


Teck SLC, Fatimah A, Beattie A, Heng RKJ, King WS. 2011. Influence of host plant species and flush growth stage on the Asian citrus psyllid, Diaphorina citri Kuwayama. American Journal of Agricultural and Biological Sciences 6: 536–543. Google Scholar


Thompson JN. 1988. Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects. Entomologia Experimentalis et Applicata 47: 3–14. Google Scholar


Wise MJ, Partelow JM, Everson KJ, Anselmo MK, Abrahamson WG. 2008. Good mothers, bad mothers, and the nature of resistance to herbivory in Solidago altíssima. Oecologia 155: 257–266. Google Scholar
Higor Augusto Seraphim Pimpinato, Gustavo Rodrigues Alves, and Pedro Takao Yamamoto "Feeding and Oviposition of Diaphorina citri (Hemiptera: Liviidae) on Helietta apiculata (Sapindales: Rutaceae): a Potential Host?," Florida Entomologist 100(2), 476-477, (1 June 2017).
Published: 1 June 2017

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