Abdominal Color of the Asian Citrus Psyllid (: Liviidae) is Associated with Flight Capabilities Author(s): Xavier Martini, Angelique Hoyte and Lukasz L. Stelinski Source: Annals of the Entomological Society of America, 107(4):842-847. Published By: Entomological Society of America URL: http://www.bioone.org/doi/full/10.1603/AN14028

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BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. BIOLOGY Abdominal Color of the Asian Citrus Psyllid (Hemiptera: Liviidae) Is Associated With Flight Capabilities

1 XAVIER MARTINI, ANGELIQUE HOYTE, AND LUKASZ L. STELINSKI

University of Florida, Entomology and Nematology Department, Citrus Research and Education Center, 700 Experiment Station Road, Lake Alfred, FL 33850

Ann. Entomol. Soc. Am. 107(4): 842Ð847 (2014); DOI: http://dx.doi.org/10.1603/AN14028 ABSTRACT We examined the propensity for ßight initiation and ßight capability of the Asian citrus psyllid ( citri Kuwayama, Hemiptera: Liviidae) with a ßight mill. We measured continuous ßight by D. citri for up to 3 h, which equated to a distance of Ϸ2.4 km. We compared the ßight capability of D. citri depending on their sex and morphotype (color of abdomen). Two general morphotypes exist within this species: greenÐblue and grayÐbrown. We observed that Ϸ32% of psyllids from the greenÐblue morphotype tested exhibited long durations of ßight (Ͼ60 s); whereas Ͻ5% of psyllids from the grayÐbrown morphotype performed such long duration ßights. There was no signiÞcant difference in ßight performance between the two sexes within both the grayÐbrown and greenÐblue morphotypes. Furthermore, psyllids from the grayÐbrown morphotype were characterized by smaller pronotums and shorter wings than psyllids from the greenÐblue morphotype. In addition, males, in general, were characterized by smaller pronotums and shorter wings than females. However, neither pronotum nor wing size were associated with ßight capability of D. citri. Our results may help explain dispersal behavior of D. citri with respect to practical management on an area-wide scale.

KEY WORDS color morph, ßight mill, , movement, insect coloration

In the context of a vector-borne pathogen system, the HLB reduced orange production by Ϸ24% in Florida spread of disease depends on movement of vectors in 2011 (Hodges and Spreen 2012). To date, all known across a landscape (Finke 2012). Indeed, vector dis- commercial citrus species are susceptible to HLB in- persal is essential for pathogens to encounter new fection regardless of rootstock (Bove´ 2006). The max- hosts to spread infection. The degree of vector dis- imum ßight distance of D. citri needs to be estimated persal is often associated with the level of spread of to identify safe isolation and quarantine boundaries, as plantÐpathogen mediated diseases (Bailey et al. 1995, well as to establish effective area-wide control proto- Christiansen-Weniger et al. 1998, Hodge and Powell cols (Halbert and Manjunath 2004). 2008). Consequently, an understanding of vector dis- It has been previously shown that D. citri migrates persal potential is useful for implementing efÞcient actively between citrus groves, notably from unman- control tactics for vector-transmitted pathogens. aged (abandoned) to managed groves (Boina et al. The Asian citrus psyllid, Kuwayama 2009, Tiwari et al. 2010). In addition, D. citri were (Hemiptera: Liviidae), is the vector of several bacte- found within a dense forest in Florida located 2 km rial pathogens including ÔCandidatus Liberibacter asi- away from the closest existing citrus grove (Martini et aticusÕ (Las). Las is the agent presumably causing the al. 2013). These Þeld data indicate that D. citri has the citrus disease huanglongbing (HLB), also known as ability to migrate long distances and through chal- citrus greening in the United States (Grafton- lenging environments. Migrations farther than 2 m Cardwell et al. 2013). HLB-infected trees have a short- from citrus trees by D. citri mostly occur during spring ened lifespan; fruit from infected trees are smaller and summer (Hall and Hentz 2011). Under laboratory than from healthy trees, remain green in color, often conditions, Arakawa and Miyamoto (2007) used a drop prematurely, and are characterized by undesir- ßight mill to investigate the ßight capability of D. citri. able organoleptic properties (Wang and Trivedi Flight capability was found to be equivalent between 2013). HLB is considered the most important threat to males and females, and maximal ßight capability oc- sustainable citrus production in the world (Bove´ curred at 4 d after adult emergence (Arakawa and 2006). In Florida, D. citri was initially observed in 1998 Miyamoto 2007). (Halbert 1998), and has since spread throughout all of There are three morphotypes of D. citri that have citrus production areas in the state. It is estimated that been characterized based on differences in abdominal color: grayÐbrown, greenÐblue, and orangeÐyellow 1 Corresponding author, e-mail: [email protected]. (Skelley and Hoy 2004, Wenninger and Hall 2008).

0013-8746/14/0842Ð0847$04.00/0 ᭧ 2014 Entomological Society of America July 2014 MARTINI ET AL.: FLIGHT CAPABILITY OF D. citri 843

Fig. 1. Schematic diagram of the ßight mill apparatus. The measurement in the diagram is presented in millime- ters.

Only older (Ͼ30 d after adult emergence) males, and Materials and Methods females with eggs may have orangeÐyellow abdomens Insect Rearing. Adult D. citri used in behavioral (Wenninger and Hall 2008). Therefore, the orangeÐ bioassays were obtained from a laboratory culture yellow morphotype is sometimes excluded from ex- maintained at the University of Florida, Citrus Re- periments investigating biological differences in D. search and Education Center (Lake Alfred, FL). The citri based on abdominal color, given its apparent culture was established in 2000 from Þeld populations plasticity (example: Wenninger et al. 2009). Overall, collected in Polk Co., FL (28.0Ј N, 81.9Ј W) before the greenÐblue morphs are characterized by greater Þt- discovery of HLB in Florida. The culture was main- ness, greater body mass, and higher fecundity than tained without exposure to insecticides on curry grayÐbrown morphs (Wenninger and Hall 2008, Wen- leaves (Bergera koenigii L.) in an air-conditioned ninger et al. 2009). Also, greenÐblue D. citri females greenhouse at 27Ð28ЊC, 60Ð65% relative humidity are more attractive to males of either morph than (RH), and a photoperiod of 14:10 (L:D) h. Illumina- grayÐbrown females (Wenninger et al. 2009). Differ- tion in the greenhouse was supplemented with linear ences in insecticide susceptibility between color ßuorescent 54 W lights (F54W/T5/865/ECO, GE morphs of D. citri have also been noted with the lighting, Nela Park, OH). Monthly testing of randomly orangeÐyellow morph exhibiting highest susceptibil- sampled nymphs, and adults by quantitative PCR as- ity (Tiwari et al. 2013). It has not yet been fully says was conducted to conÞrm that psyllids and plants conÞrmed whether color polymorphism in D. citri is in this culture were free of Las. It is known that D. citri completely plastic or in some way genetically prede- reach their maximal ßight capability at 4 d after emer- termined; however, it has been suggested that biotic gence (Arakawa and Miyamoto 2007). Given that D. factors such as host plant quality or intraspeciÞc com- citri have a lifespan of Ϸ40dat25ЊC after adult emer- petition may play roles in determination of morpho- gence (Tsai and Liu 2000), we elected to perform type (Wenninger and Hall 2008). behavioral assays using psyllids aged between 5 and The objective of this investigation was to explore 15 d after adult emergence. To obtain psyllid between the ßight capability of D. citri among psyllid color 5 and 15 d old, four B. koenigii were infested with Ϸ100 morphotypes. We conducted a study using a ßight mill unsexed D. citri adults. After 1 wk, all of these adults modiÞed from Arakawa and Miyamoto (2007). We were removed. Thereafter, the cage was inspected compared ßight capability of D. citri depending of daily and the adults that emerged were transferred to their abdominal color and sex. We also measured wing a separate plant free of D. citri. The day of the transfer length and pronotum width to test for a possible cor- was noted and these psyllids were used 5Ð15 d after relation between these morphometric data and ßight their transfer. The experiments were performed be- capability of D. citri. tween the 5 September 2013 and 27 November 2013. 844 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 107, no. 4

Table 1. Percentage of D. citri adults tested in the flight mill that did not fly (“nonflyer”); that flew for a short period of time (“short flyer,” < 60 s); or that flew for a long period of time (“long flyer,” > 60 s)

Abdominal Sex Nonßyer (%) Short ßyer (%) Long ßyer (%) Na Avg. ßight (s)b Max ßight (s) color GreenÐblue Male 27.27ac 36.36a 36.36a 22 195.4 Ϯ 91 1,313 GreenÐblue Female 18.18a 54.55a 27.27a 22 864.5 Ϯ 602 10,800 GrayÐbrown Male 52.63a 47.37a 0.00b 19 19.00 Ϯ 547 GrayÐbrown Female 28.57a 66.67a 4.76b 21 17.06 Ϯ 565

D. citri ßight capability was compared depending on their abdominal color and sex. Average (ϮSE) and max ßight duration recorded for each category is also provided. a Number of psyllids tested on the ßight mill for each category. b Average time that the psyllids ßew for each category; nonßyers were excluded here. c Percentages followed by different letters indicate signiÞcant differences (␣ Ͻ 0.05) between cells within the same column.

Flight Mill Apparatus. A schematic diagram of the analyses were conducted with the statistical software ßight mill is provided in Fig. 1. The ßight mill was R v3.02 (The R Foundation for Statistical Computing, composed of a 13-cm optic Þber horizontal axis, Þxed Vienna, Austria). We Þrst compared the proportion of to a pivot consisting of a metal Þber. The pivot was nonßyers, short ßyers, and long ßyers as a function of positioned vertically under a magnet. To prevent the sex and abdominal color with a generalized linear Þber from ßipping horizontally, the metal Þber was model with binomial distribution. Sex and abdominal inserted through a pierced acrylic glass sheet. In ad- color were used as Þxed variables. We subsequently dition, to maintain the metal Þber in a vertical orien- assessed the effect of psyllid age on the proportion of tation, a second magnet was positioned 1 cm below. At long ßyers with a different generalized linear model, each extremity of the horizontal optic Þber, two where only age of the psyllids was used as a Þxed smaller pieces of optic Þber were glued in a vertical variable. GrayÐbrown psyllids were excluded from orientation. The psyllids were afÞxed to the tip of this analysis because only a single grayÐbrown mor- one of these small optic Þber pieces. The other piece photype psyllid ßew Ͼ60 s (see the result section). We of optic Þber was present to maintain effective bal- also compared the duration of ßight and ßight speed ance of the ßight mill. All the experiments were by long ßyers as function of sex using a MannÐWhitney performed in an air-conditioned room between 0900 rank sum test. Finally, we compared effects of psyllid and 1400 hours at 27 Ϯ 1ЊC and 40 Ϯ 10% RH. age on ßight duration and ßight speed with linear Flight Mill Procedure. Five- to 15-d-old D. citri regressions. GrayÐbrown psyllids were again excluded adults were placed onto an ice-pack covered with from these analyses. Pronotum width and wing length Þlter paper. While immobilized on the ice pack, psyl- data were analyzed using a two-way analysis of vari- lids were attached to the tip of a 10-mm-length optic ance (ANOVA) with sex and abdominal color as Þxed Þber with a minute amount of nontoxic, washable glue variables. After excluding grayÐbrown morphotypes, (ElmerÕs products, Columbus, OH) via the pronotum we performed a two-way ANOVA with sex and ßyer (Fig. 1). Thereafter, the optic Þber was glued to the categories as Þxed variables. To obtain a normalized horizontal axis of the ßight mill and the behavioral distribution, we removed one outlier and log trans- assay was initiated. If a psyllid did not ßy during the formed the pronotum width data set. Þrst 10 min after attachment, it was removed and discarded. Preliminary tests showed that a psyllid that Results did not ßy during the Þrst 10 min would not ßy for at least the next hour. Assays were terminated 5 min after The proportion of greenÐblue morph D. citri adults psyllids ceased ßight activity. For psyllids that initiated that performed a long ßight (Ͼ60 s) was signiÞcantly ßight, duration of ßight and the number of rotations on greater than of grayÐbrown morphs (Table 1; ␹2 ϭ the ßight mill were recorded. The distance (in cm) 14.39; df ϭ 1; P Ͻ 0.001). The proportion of long ßyers ßown by each psyllid was calculated by multiplying was not different as a function of sex (Table 1; ␹2 ϭ the number of rotations by 13␲. After each assay, the 0.15; df ϭ 1; P ϭ 0.700), or age (␹2 ϭ 0.53; df ϭ 1; P ϭ sex and abdominal color of each psyllid tested were 0.466). The average duration of ßight for long ßyers determined. In addition, we measured pronotum was 1,300 Ϯ 752 s, with an average distance of 320.5 Ϯ width and wing length of a subsample of D. citri tested 209.5 m and a speed of 0.630 Ϯ 0.06 km/h. The maximal on the ßight mill. These were measured with a mi- ßight obtained was with a 10-d-old greenÐblue female croruler inserted into the lens of a dissecting micro- that ßew for 3 h, which equated to Ϸ2.4 km. There was scope (Wild M3C, Leica, Wetzlar, Germany). no difference in ßight speed (MannÐWhitney rank Statistical Analysis. The psyllids used on the ßight sum test: U ϭ 18; n ϭ 14; P ϭ 0.491) and ßight duration mill were classiÞed into three categories: 1) psyllids (MannÐWhitney rank sum test: U ϭ 11; n ϭ 14; P ϭ that did not ßy during the experiment were catego- 0.108) for long ßyers with respect to sex. Also, psyllid rized as “nonßyers;” 2) psyllids that ßew Ͻ60 s were age was not correlated with either ßight speed (n ϭ 14; categorized as “short ßyers;” and 3) psyllids that ßew F ϭ 1.470; P ϭ 0.249) or ßight duration (n ϭ 14; F ϭ Ն60 s were categorized as “long ßyers.” All statistical 0.009; P ϭ 0.923). July 2014 MARTINI ET AL.: FLIGHT CAPABILITY OF D. citri 845

Fig. 2. Average (ϮSE) wing length (A) and pronotum width (B) of D. citri depending of the abdominal color and the sex. Average (ϮSE) wing length (C) and pronotum width (D) of D. citri depending of the ßight performance on the ßight mill. For (C) and (D), grayÐbrown morphotypes were excluded because of the low number of long ßyers within this morphotype. Bars labeled by different capital letters within sex are signiÞcantly different at the ␣ Ͻ 0.05 level. Bars labeled by different lower case letters within abdominal color (A and B) or within ßight performance (C and D) are signiÞcantly different at the ␣ Ͻ 0.05 level.

Regarding biometric data, the length of male wings that lasted Ͼ20 min in duration. The maximum dura- (Fig. 2A; F ϭ 12.00; df ϭ 1, 60; P Ͻ 0.001) was shorter tion of ßight by D. citri reported by Arakawa and than that of females. Also, wings of grayÐbrown Miyamoto (2007) was 50 min. However, in our inves- morphs (Fig. 2A; F ϭ 12.15; df ϭ 1, 60; P Ͻ 0.001) were tigation, we observed a blueÐgreen, female morph D. shorter than that of greenÐblue morphs. We found no citri ßy continuously for Ϸ3 h. This 3 h ßight in the interaction between sex and abdominal color regard- laboratory equated to an approximate distance of 2.4 ing wing length (Fig. 2A; F ϭ 0.17; df ϭ 1, 60; P ϭ km of continuous ßight. These data corroborate pre- 0.680). We also found that the pronotum of males was vious Þeld observations (Boina et al. 2009, Tiwari et al. smaller than that of females (Fig. 2B and F ϭ 5.80; df ϭ 2010, Martini et al. 2013), indicating that D. citri are 1, 59; P ϭ 0.019). Also, pronotum size of grayÐbrown able to disperse multiple kilometers and this capability morphs (Fig. 2B; F ϭ 11.11; df ϭ 1, 59; P ϭ 0.001) was appears not to require assistance from wind. smaller than that of greenÐblue morphs. We found no Our morphometric analyses also revealed physical interaction between sex and abdominal color regard- differences between D. citri color morphs. Pronotum ing pronotum width (Fig. 2B; F ϭ 1.84; df ϭ 1, 59; P ϭ width and wing length were both shorter in grayÐ 0.180). Finally, after excluding grayÐbrown morphs, brown than greenÐblue D. citri. These data are con- neither wing length (Fig. 2C; F ϭ 1.10; df ϭ 2, 28; P ϭ gruent with Wenninger and Hall (2008), who found 0.346) nor pronotum width (Fig. 2D; F ϭ 2.08; df ϭ 2, that grayÐbrown D. citri morphs were of lower mass 27; P ϭ 0.145) was signiÞcantly different between than greenÐblue morphs. Wenninger et al. (2008) nonßyers, short ßyers, and long ßyers. suggested, based on observational data, that a propor- tion of D. citri may switch from the grayÐbrown to the blueÐgreen morphotype (and vice versa). However, Discussion differences in Þxed biometric characteristics such as In the current investigation, we found that variation wing length or pronotum width may indicate genet- in abdominal color of D. citri morphotypes is related ically predetermined morphotypes or morphotypes to ßight capability of both male and female psyllids. that are determined during nymphal development. For both sexes, grayÐbrown individuals were charac- We did not Þnd differences in wing length and pro- terized by lower ßight capability than greenÐblue notum width between the various ßyer categories (as psyllids. Predominantly greenÐblue morph D. citri deÞned by our experiments), suggesting that these performed long distance (Ͼ60 s) ßights; however, morphometric characteristics did not impact ßight there was no difference in ßight capacity between the capability of D. citri in the range of variability ob- sexes within this morphotype. Our results were con- served. The smaller size and mass, lower ßight capa- gruent with those reported by Arakawa and Miyamoto bility, and lower reproductive potential of grayÐ (2007), who observed individual ßights by psyllids brown than greenÐblue morphs imply that the 846 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 107, no. 4 occurrence of this morphotype should be selected insecticide application protocols following detection against within populations of D. citri. Therefore, why of D. citri in a quarantined area. Another possible this polymorphism is maintained in Þeld populations application of these results is that the proportion of of D. citri is an intriguing question. greenÐblue versus grayÐbrown morphs within a pop- The relationship between variation in body pigmen- ulation may indicate the risk of D. citri dispersal. Al- tation and ßight performance of hemipteran is ternatively, given that the greenÐblue morphotype not fully understood. Ahsaei et al. (2013) found dif- occurs within Þeld populations of D. citri in large ferences between the red and green morphs of the pea proportions and is also selected for given higher fe- aphid, Acyrthosiphon pisum Harris, with respect to cundity (Wenninger and Hall 2008), determining the their energetic reserves. The red morphs maintained color of D. citri morphotypes within populations of a higher percentage content of water-soluble carbo- cultivated citrus may have no practical implication hydrates and lipids than green morphs; whereas green with respect to optimizing insecticide sprays. How- morphs were characterized by a higher percentage of ever, it is clear that adult D. citri are capable of long- protein content than red morphs. Interestingly, the distance migration, which must be considered when authors associated these differences with the fact that determining area-wide management and quarantine red morphs produce more winged offspring than protocols. Other factors impacting dispersal of D. citri, green morphs and therefore higher levels of carbo- such as pathogen infection, are currently under in- hydrates and lipids may improve the ßight potential of vestigation and will also contribute to the manage- this morphotype (Ahsaei et al. 2013). ment of this pathosystem. In the case of D. citri, it has been hypothesized that abdominal color variation may be associated with the quantity or quality of acquired food resources (Wen- Acknowledgments ninger and Hall 2008). Alternatively, differing color We thank the Citrus Research and Development Foun- morphs within a population may partially result from dation for funding. We thank two anonymous reviewers for competition between conspeciÞcs during nymph de- their valuable comments on an earlier version of the manu- velopment (Wenninger et al. 2009). In both cases, script. such biotic factors may affect energetic reserves of emerging adult D. citri and consequently their ßight capability. Future work should address the energetic References Cited contents of greenÐblue versus brownÐgray morpho- Ahsaei, S. M., S. M. Tabadkani, V. Hosseininaveh, H. Allah- types, and determine if this energetic content is af- yari, and M. Bigham. 2013. Differential accumulation of fected by plant host quality or intraspeciÞc competi- energy by the colour morphs of the pea aphid Acyrtho- tion during nymph development. siphon pisum (Hemiptera: Aphididae) mirrors their eco- Our results indicate that on average, D. citri per- logical adaptations. Eur. J. Entomol. 110: 241Ð245. forming long-distance ßights dispersed 320 m (great- Arakawa, K., and K. Miyamoto. 2007. Flight ability of Asiatic est distance observed was 2.4 km) without wind as- citrus psyllid, Diaphorina citri Kuwayama (Homoptera; sistance. These data indicate that adult D. citri are Psyllidae), measured by a ßight mill. Res. B. Plant Prot. capable of signiÞcant long-range dispersal. It is prob- Serv. Japan 43: 23Ð26. able; however; that wind may signiÞcantly increase Bailey, S. M., M. E. Irwin, G. E. Kampmeier, C. E. Eastman, and A. D. Hewings. 1995. Physical and biological per- the dispersal capability of D. citri. Obviously, our ex- turbations: their effect on the movement of apterous periments did not take into account how wind may Rhopalosiphum padi (Homoptera: Aphididae) and local- alter ßight capability of D. citri. It is possible that there ized spread of barley yellow dwarf virus. Environ. Ento- is an optimal wind speed at which D. citri preferen- mol. 24: 24Ð33. tially initiate ßight, and a maximal speed above which Boina, D. R., W. L. Meyer, E. O. Onagbola, and L. L. Stelinski. they will not ßy. Also, our experiments did not deter- 2009. Quantifying dispersal of Diaphorina citri mine whether upwind ßight is preferred by D. citri in (Hemiptera: Psyllidae) by immunomarking and potential response to odor cues (speciÞcally citrus odors). impact of unmanaged groves on commercial citrus man- Overall, impact of wind on dispersal of D. citri requires agement. Environ. Entomol. 38: 1250Ð1258. Bove´, J. M. 2006. Huanglongbing: A destructive, newly- further investigation beyond the ßight mill investiga- emerging, century-old disease of citrus. J. Plant Pathol. 88: tions conducted here that indented to test physiolog- 7Ð37. ical limits of ßight potential. Christiansen-Weniger, P., G. Powell, and J. Hardie. 1998. Nevertheless, our study demonstrated that D. citri Plant virus and parasitoid interactions in a shared insect has signiÞcant ßight capability and is able to ßy long vector/host. Entomol. Exp. Appl. 86: 205Ð213. distances without wind assistance. Furthermore, the Finke, D. L. 2012. Contrasting the consumptive and non- ability of D. citri to survive short durations on nonhost consumptive cascading effects of natural enemies on vec- plants (Martini et al. 2013) may further increase their tor-borne pathogens. Entomol. Exp. Appl. 144: 44Ð55. potential for long-range dispersal. The current results Grafton-Cardwell, E. E., L. L. Stelinski, and P. A. Stansly. 2013. 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