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Field survey of Asian citrus psyllid (Hemiptera: Liviidae) infestations associated with six cultivars of Poncirus trifoliata (Rutaceae).

The Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Liviidae), is an important pest because it transmits a bacterium 'Candidatus Liberibacter asiaticus' putatively responsible for a serious citrus disease known as Asiatic huanglongbing or citrus greening disease (Bove 2006; Gottwald 2010). Classic recommendations to growers confronted with the disease are to plant disease-free nursery stock, routinely identify and remove infected trees to reduce inoculum loads, and aggressively manage populations of the psyllid (Hall et al. 2013). Insecticidal control is the key tactic used to manage the psyllid, but host plant resistance may hold some promise in the search for alternative tactics. Whereas no resistance to the psyllid has been observed within the Citrus genus (Rutaceae), relatively strong levels of antixenotic resistance to the psyllid have been reported in Poncirus trifoliata (L.) Raf. (Rutaceae), a species in the same Rutaceae subfamily as Citrus. Aubert (1987) noted reduced infestations of the psyllid on P. trifoliata. Westbrook et al. (2011) conducted a field survey of 87 genotypes in the plant family Rutaceae and concluded P. trifoliata was one of the most resistant to psyllid colonization. Recent laboratory and greenhouse investigations confirmed that P. trifoliata cultivars usually are colonized less by the psyllid than are Citrus cultivars (Richardson & Hall 2013; Hall et al. 2015).

The purpose of the research presented here was to assess infestations of the psyllid associated with 5-yr-old P. trifoliata trees underfield conditions. Infestation densities of eggs and nymphs on flush shoots were monitored over the summer of 2016 on 6 pure P. trifoliata cultivars, 4 citrange cultivars, and 2 conventional Citrus cultivars--a sweet orange (Citrus sinensis [L] Osbeck) cultivar (Hamlin) and a sweet orange hybrid (Temple) (Table 1). Citranges are hybrids between P. trifoliata and sweet orange. Six to 8 trees of each of the 12 cultivars were available for monitoring in a large planting of many experimental citranges (0.8 ha area, 8 rows with about 100 trees per row, 1.5 m spacing between trees, 1 cultivar per row). The trees were subjected to regular irrigation, fertilization, and weed control but without any insecticides or horticultural oils. On each sample date, 2 flush shoots (each with at least some leaves appropriate for oviposition) were randomly collected from each tree, transported to a laboratory, and examined under a microscope to count numbers of eggs and nymphs of D. citri. Additionally on each sample date, each tree was examined to estimate the percentage of branches with flush shoots appropriate for oviposition. Data on log-transformed numbers of psyllids per flush shoot and on arcsine-transformed percentages of flush shoots with 5th instar nymphs were subjected to analyses of variance (PROC GLM; SAS Institute 2010), mean comparisons among cultivars were investigated with the Ryan-Einot-Gabriel-Welsch multiple range test, and results were reported with untransformed means.

Poncirus trifoliata is a deciduous genotype, and trees in the field are thus usually completely void of foliage throughout the winter, whereas citranges may be semi-deciduous. During early Mar of this survey, ample quantities of flush shoots were present in trees of the Citrus and citrange cultivars, and psyllid eggs and nymphs were present on this flush. However, none of the P. trifoliata trees at this time had yet broken winter dormancy and thus all of them were barren of foliage. The P. trifoliata cultivars began to flush toward the end of Mar. Thereafter during the summer, at least some flush was consistently available on the P. trifoliata cultivars, and flushing patterns were similar in Citrus, citranges, and P. trifoliata (Fig. la). Among 9 sample dates during late Marto Sep, relatively large infestation densities of eggs and nymphs were observed on the Citrus and citrange cultivars whereas significantly fewer were consistently observed on the pure P. trifoliata cultivars (Table 1; Fig. 1b). Over all sample dates, means [+ or -] SE of 13.3 [+ or -] 1.9, 23.7 [+ or -] 2.4, and 1.1 [+ or -] 0.2 eggs per flush shoot were observed on the Citrus, citrange, and P. trifoliata cultivars, respectively. Although fewer eggs were deposited on P. trifoliata, at least some of these hatched: means of 22.0 [+ or -] 2.3, 20.8 [+ or -] 1.9, and 1.0 [+ or -] 0.2 nymphs per flush shoot were observed on the Citrus, citrange, and P. trifoliata cultivars, respectively. Few nymphs were observed on the pure P. trifoliata shoots but at least some developed to the 5th instar (Table 1), and general observations indicated these older nymphs were healthy enough that they would have successfully molted to the adult stage.

Reduced colonization by Asian citrus psyllid on P. trifoliata was largely a result of reduced rates of oviposition. Because P. trifoliata readily hybridizes with Citrus species, if the specific traits responsible for reduced oviposition can be identified, then it might be possible to transfer these traits to conventional Citrus cultivars. However, we found no reduced oviposition on the 4 citrange cultivars tested in this study. The resistance in P. trifoliata to psyllid oviposition may be either a recessive or a multi-genic trait, or there may be genetically controlled traits in Citrus that promote oviposition.

We thank Kathy Moulton and Patrick Legler for their contributions tothis research project. This article reportsthe results of research only. Mention of a trademark or proprietary product is solely for the purpose of providing specific information and does not constitute a guarantee or warranty of the product by the United States Department of Agriculture (USDA) and does not imply its approval to the exclusion of other products that also may be suitable. USDA is an equal opportunity provider and employer. The research was partially funded by a grant (#853) from the Citrus Research & Development Foundation.


The Asian citrus psyllid (Hemiptera: Liviidae) transmits a bacterium responsible for huanglongbing, a serious citrus disease. Insecticidal control of the psyllid is a key tactic used to manage the disease, but host plant resistance may hold some promise and clues in the search for alternative tactics. Results of a field survey revealed that relatively large infestation densities of the psyllid developed on conventional Citrus (Rutaceae) and citrange (Rutaceae) cultivars but not on any of 6 Poncirus trifoliata (L.) Raf. (Rutaceae) cultivars. Poncirus trifoliata is a species closely related to Citrus, and citranges are hybrids of sweet orange and P. trifoliata. Reduced colonization by the psyllid on P. trifoliata was largely a result of reduced rates of oviposition. Poncirus trifoliata resistance to oviposition was not observed in 4 citrange cultivars.

Key Words: citrus greening; huanglongbing; Diaphorina citri; Liberbacter


El psilido asiatico de los citricos (Hemiptera: Liviidae) transmite la bacteria responsable del huanglongbing, una enfermedad seria de los citricos. El control quimico del psilido es una tactica clave utilizada para manejar la enfermedad, pero la resistencia de la planta hospedera puede ser prometedora y dar una pista en la busqueda de tacticas alternativas. Los resultados de un sondeo del campo revelaron densidades de infestacion relativamente grandes del psilido desarrollandose en cultivares convencionales de Citrus (Rutaceae) y citrange (Rutaceae), pero no sobre ninguno de los 6 cultivares de Poncirus trifoliata (L.) Raf. (Rutaceae). Poncirus trifoliata es una especie estrechamente relacionada con Citrus y las citranges son hibridos de naranja dulce y P trifoliata. La reduccion de la colonizacion por el psilido sobre P trifoliata fue en gran parte resultado de una tasa de oviposicion reducida. No se observo resistencia a la oviposicion en Poncirus trifoliata en los 4 cultivares de citrange.

Palabras Clave: enverdecimiento de los citricos; huanglongbing; Diaphorina citri; Liberibacter

References Cited

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.

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

Gottwald TR. 2010. Current epidemiological understanding of citrus huanglongbing. Annual Review of Phytopathology 48:119-139.

Hall DG, Richardson ML, Ammar ED, Halbert SE. 2013. Asian citrus psyllid, Diaphorina citri (Hemiptera: Psyllidae), vector of citrus huanglongbing disease. Entomologia Experimentalis et Applicata 146: 207-223.

Hall DG, George J, Lapointe SL. 2015. Further investigations on colonization of Poncirus trifoliata by the Asian citrus psyllid. Crop Protection 72:112-118.

Richardson ML, Hall DG. 2013. Resistance of Poncirus and Citrus x Poncirus germplasm to the Asian citrus psyllid. Crop Science 53:183-188.

SAS Institute, Inc. 2010. SAS[R] Procedures Guide Version 9.3. SAS Institute, Cary North Carolina.

Westbrook CJ, Hall DG, Stover EW, Duan YP, Lee RF. 2011. Colonization of Citrus and Citrus-related germplasm by Diaphorina citri (Hemiptera: Psyllidae). HortScience 46: 997-1005.

David G. Hall (1,*), Matthew G. Hentz (1), and Ed Stover (1)

(1) United States Department of Agriculture (USDA) Agricultural Research Service (ARS), U.S. Horticultural Research Laboratory, 2001 S. Rock Road, Ft. Pierce, FL 34945, USA; E-mail: (D. G. H.), (M. G. H.), (E. S.)

(*) Corresponding author; E-mail: (D. G. H.)

Caption: Fig. 1. Comparisons among cultivars of Citrus, citranges, and pure Poncirus trifoliata with respect to infestations of Asian citrus psyllid (ACP) in 5-yr-old trees at a grove in east-central Florida during 2016. a) Percentage of branches with flush suitable for oviposition by Asian citrus psyllid. b) Average infestation densities of immature Asian citrus psyllids (counts of eggs and nymphs combined) per flush shoot. Error bars are standard errors of the mean.
Table 1. Mean number of immature Asian citrus psyllids per flush shoot
in a 5-yr-old field planting of Citrus, citrange, and P. trifoliata
trees sampled during Mar to Sep 2016.

                               Mean number per flush shoot (a)
                                               Mean percentage of
                                               infested samples with
Genotype group  Cultivar       Eggs    Nymphs  fifth instar nymphs (a)

Citrus          Hamlin         16.0ab  21.6a   37.2ab
Citrus          Temple         10.6b   22.5a   47.7ab
Citrange        C-35           25.0a   20.4a   18.5ab
Citrange        Carrizo        18.6ab  16.1a   23.3ab
Citrange        Norton         21.4ab  20.2a   34.0ab
Citrange        Uvalde         28.7ab  24.4a   35.3ab
Poncirus        Argentina       0.8c    1.5b   13.3b
Poncirus        Flying Dragon   2.0c    1.1b    7.7b
Poncirus        Large Flower    0.8c    0.8b   57.1a
Poncirus        Pomeroy         0.8c    1.6b   27.3ab
Poncirus        Rich 16-6       0.9c    0.4b   20.0ab
Poncirus        Rubidoux        1.7c    1.0b    9.1b

(a) Means in the same column followed by the same letter are not
significantly different (P > 0.05), Ryan-Einot-Gabriel-Welsch multiple
range test.

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Title Annotation:Scientific Notes
Author:Hall, David G.; Hentz, Matthew G.; Stover, Ed
Publication:Florida Entomologist
Article Type:Report
Date:Sep 1, 2017
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