Body Size Variation of Diaphorina Citri (Hemiptera: Psyllidae) Through an Elevation Gradient

Annals of the Entomological Society of America Advance Access published July 24, 2015

ECOLOGY AND POPULATION BIOLOGY Body Size Variation of Diaphorina citri (Hemiptera: Psyllidae) Through an Elevation Gradient

1 L. I. PE´ REZ-VALENCIA AND G. MOYA-RAYGOZA

Departamento de Botańica y Zoologıá,CUCBA. Universidad de Guadalajara. Camino Ramoń Padilla Sańchez #2100, Nextipac, Zapopan, Jalisco, Me´xico.

Ann. Entomol. Soc. Am. 1–7 (2015); DOI: 10.1093/aesa/sav072 ABSTRACT The Asian citrus psyllid, Diaphorina citri Kuwayama, vectors the bacterium ‘Candidatus Liberibacter asiaticus’ responsible for the huanglongbing (HLB) disease. In Mexico, economic losses caused by HLB severely affect the citrus industry. Despite the threat that the presence of D. citri implies, due to its invasive characteristics, there are few ecological and biological studies addressing its adaptation to new and different environments in Mexico. Based on the temperature-size rule, stating smaller adult size at higher rearing temperatures, the aim of this study was to evaluate D. citri’s body size variation at different temperatures related to an elevation gradient. Adults were collected at four different elevations in the states of Jalisco and Colima, Mexico. Right forewing length and width as well as prothorax width and right antenna length were measured. Statistical differences between the sexes were analyzed by a multivariate analysis using Hotelling’s T2 and Kruskal–Wallis nonparametric test to evaluate body size variation between elevations followed by a Nemenyi’s pairwise comparison test. To evaluate relationships between size variation and elevation, a v2 independence test was performed. Females were shown to be statistically larger than males. All body structures except the prothorax were shown to be larger at location El Arenal (higher elevation) and smaller at location Tecoma´n (lower elevation). Forewing length and width best explained the differences observed between the sexes and at the four locations, showing that the temperature-size rule applies in this case.

KEY WORDS temperature, huanglongbing, invasive pest

The Asian citrus psyllid, Diaphorina citri Kuwayama, is on the behavior, abundance, and distribution of insects, the most important pest in citrus plantations because it with temperature being the most important variable is responsible for the transmission of the bacterium (Messenger 1959, Peacock 2006, Chown and Gaston ‘Candidatus Liberibecter asiaticus’ associated with 2010). Temperature changes significantly along eleva- huanglongbing disease (HLB) that causes severe eco- tion gradients and often has effects on life history traits nomic losses to the citrus industry worldwide (Bove´ like body size variation. In insects there is no consistent 2006). In Mexico, D. citri presence was detected for pattern for how geographic and climatic factors influ- first time in Campeche and Quintana Roo in 2002 ence body size variation (Smith et al. 2000; Chown and (Halbert and Nun˜ez2004) while HLB symptoms were Klok 2003; Moya-Raygoza et al. 2005; Bidau and Martı´ detected in citrus plantations and backyard trees in Yu- 2007, 2008). Some studies indicate that body size in- catań in 2009 (Servicio Nacional de Sanidad, Inocuidad creases at higher and decreases at lower elevations y Calidad Agroalimentaria [SENASICA] 2009). Since (Stalker and Carson 1948, Janzen et al. 1976, Atkinson then, D. citri has been found in all commercial or- 1994, Hawkins and DeVries 1996, Chown and Klok chards in the country (SENASICA 2013). 2003, de Oliveira et al. 2004, Rodrı´guez-Jimeńez and Mexican citrus plantations have a broad distribution Sarmiento 2008, Tantowijoyo and Hoffmann 2011), across Mexico; thus, D. citri’s individuals likely display others reveal the opposite (inverse) pattern (Sota 1996, phenotypic plasticity in response to different environ- Blanckenhorn 1997, Arnett and Gotelli 1999, Brehm ments in order to persist in habitats that vary in tem- and Fiedler 2004, Kanˇuch and Krisˇtıń 2009), while still perature, atmospheric pressure, precipitation, relative others show no variation at all (Smith et al. 2000, humidity, and other biotic and abiotic elements. Moya-Raygoza et al. 2005). Despite D. citri’s economic and ecological importance, The objective of this study was to evaluate body size there are few scientific studies evaluating how abiotic variation in different temperatures along an elevation elements are modifying life history traits in this invasive gradient. According to a temperature-size rule, animals species. Climate conditions are a dominant influence reared at low temperatures grow to a larger size (von Bertalanffy 1960; Berrigan and Charnov 1994; Atkinson 1994, 1996; Perrin 1995; Atkinson and Sibly 1997; Klok and Harrison 2013). Observations made by Lashkari 1 Corresponding author, e-mail: [email protected]. et al. (2013) revealed a pattern in which populations

VC The Authors 2015. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For Permissions, please email: [email protected] 2ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA with smaller wings are more consistently present in To compare body size differences between sexes, all arid regions, while populations with larger wings tend female and male measurements (WL, WW, PT, and to be present in semiarid climates. Therefore, we hy- AN) were analyzed with a Hotelling’s T2 (Johnson pothesized that at a high elevation site (El Arenal), 2002). The statistical significance of body size variation which has a moderately warm climate, mean annual through an elevation gradient considering both females temperature of 21.0C, and mean annual precipitation and males was tested using a nonparametric Kruskal– of 998.0 mm (Instituto Nacional de Estadı´stica y Geo- Wallis test, followed by a post hoc Nemenyi’s pairwise grafıá [INEGI] 2009a), we expect to find D. citri adults comparison test using R software (R Core Develop- with larger bodies compared to adults observed at a ment Team 2013). Finally, a v2 independence test was low elevation site (Tecomań) characterized by a semi- used to evaluate independence between body size and arid climate, a 26.3C mean annual temperature, and elevation (Zar 1999). 484.9 mm mean annual precipitation (INEGI 2009b). This study will improve our understanding of rapid phenotypic adaptation in an invasive insect occupying Results environments of different elevation. Hotelling’s T2 analysis indicated significant differences of body size between females and males 2 (T ¼ 208.47; F0.05, 4,180 ¼ 2.42). WL and WW means showed females from all locations were larger com- Materials and Methods pared to males, and that both females and males from Orchards where collections took place were located El Arenal were larger and wider than females and in the states of Jalisco and Colima, Mexico. They were males from Tecomań (Figs. 1 and 2). PT and AN selected by elevation gradient and the presence of D. showed no clear tendencies (Figs. 3 and 4). citri adults in Citrus x latifolia (Yu Tanaka) Tanaka and Kruskal–Wallis tests revealed significant differences Citrus aurantifolia (Christm) Swingle; we considered between sites in all body structures except for PT only these two species to avoid variation associated (H ¼ 3.39; df ¼ 3; P ¼ 0.33). Results from Nemenyi’s with host plants, although it is well documented that comparison test indicated that, for all body structures, the subfamily Diaphorininae has adapted to members El Arenal had significant differences compared to one of the genus Citrus generally (Liu and Tsai 2000, Tsai or both of the lower locations (Colima and Tecomań), and Liu 2000, Nakata 2006, Hodkinson 2009; Table 1). suggesting body size variation through an elevation gra- D. citri adults were collected with a mouth aspirator dient (Table 2). Chi-square for independence test and preserved at 95% ethanol in a 1.5-ml microcentri- showed significant difference for WL (v2 ¼ 19.18; fuge tube for later analysis at the laboratory. Adult df ¼ 6; P ¼ 0.004), WW (v2 ¼ 15.38; df ¼ 6; P ¼ 0.02), identification was conducted using the dichotomous and AN (v2 ¼ 41.27; df ¼ 6; P ¼ 0.001), suggesting that keys for Psylloidea developed by Yang (1984) and the observed variation in body structures is related to Burckhardt (2007). All samples were collected in Janu- elevation. ary 2014, to avoid seasonal variation. In the laboratory 30 females and 30 males from each Discussion site were randomly selected and dissected under a Zeiss stereoscope to separate and measure right fore- In insects, it is not unusual to find that males are wing (length and width), prothorax width, and right an- smaller than females (Fairbairn 1997, Blanckenhorn tenna length. Forewing length was measured from the et al. 2007). Our study showed significant differences base to the distal part of the wing (WL) and width at in body size between the sexes, where female WL and the broadest part of the wing (WW). Right antenna was WW were larger or wider than males. These results are measured from the base of the scape to the distal part consistent with previous reports where D. citri mean of the flagellum (AN) and the prothorax was measured body length for females and males, respectively, were along its width (PT). All these measurements are useful 3.3 mm and 2.7 mm (Tsai et al. 2002), 3.1 mm and to determine the presence of variation among adults 2.5 mm (Fonseca et al. 2007), and 2.81 mm and (Hollis 1987). 2.46 mm (Garcıá-Pe´rez et al. 2013). Our results clearly

Table 1. D. citri collecting data at four localities in Jalisco and Colima

Estate County-Locality N W Elevation Temp C Precipitation mm Date Citrus sp. m (MAT–Min–Max) (MAP–Min–Max) Jan. 2014

Jalisco El Arenal, Potrero 20 44055.6100 103 38039.5200 1,400 20.1–18–24 1,043–800–1,100 10 Citrus x latifolia Tempsique (Yu Tanaka) Tanaka Jalisco Autla´n de Navarro 19 45052.79400 104 19055.16100 894 23.2–14–24 816–700–1,300 16 Citrus x latifolia Potrero La Lima (Yu Tanaka) Tanaka Colima Colima, Col. 19 14019.3200 103 46021.43200 413 25.2–22–28 970–600–1,300 14 Citrus aurantifolia Tabachines (Christm) Swingle Colima Tecoma´n, Potrero 18 46034.700 103 49015.900 5 26.4–22–28 750–600–1,100 13 Citrus aurantifolia El Destierro (Christm) Swingle MAT, mean annual temperature; MAP, mean annual precipitation. 2015 PE´ REZ-VALENCIA AND MOYA-RAYGOZA: D. citri BODY SIZE VARIATION 3

4.4 Females 4.3 Males

4.2

4.1

3.9

Mean (±SEM) Wing lenght (mm) 3.8 El Arenal Autlán de Colima Tecomán (1400 m) Navarro (414 m) (5 m) (894 m)

Locations Fig. 1. D. citri mean wing length 6 SE (SE) at four different locations.

1.85 Females 1.8 Males

1.75

1.7

1.65

1.6 Mean (±SEM) Wing Width (mm) 1.55 El Arenal Autlán de Colima Tecomán (1400 m) Navarro (414 m) (5 m) (894 m) Locations Fig. 2. D. citri mean wing width 6 SE at four different locations. indicate WL and WW as body structures that best ex- Harrison 2013), showing in this case larger sizes at plained differences between sexes and among locations. higher elevation (i.e., lower temperature) and smaller The unclear pattern of PT and AN may require an ex- sizes at lower elevation (higher temperature). Studies tended evaluation. have shown that other abiotic elements such as nutri- D. citri forewings (length and width, respectively) tional resources (availability and quality), relative hu- showed significant differences between sites midity, and atmospheric pressure, among others, lead (H ¼ 15.78, df ¼ 3, P ¼ 0.001; H ¼ 17.6, df ¼ 3, to intra- and interspecific size variation, but tempera- P ¼ 0.001). Both females and males from El Arenal ture appears to be the most important (Hodkinson (1,400 m) have larger and wider wings compared to fe- 2005, Kingsolver and Huey 2008, Chown and Gaston males and males from Tecoma´n (5 m), indicating that 2010, Shelomi 2012). Hall et al. (2011) gave direct evi- D. citri forewings change through an elevation gradi- dence supporting the importance of temperature for ent. Because geographic factors such as elevation are oviposition in D. citri,whileGarcı´a- Pe´rez et al. (2013) directly correlated with climatic factors such as temper- discussed possible explanations for the morphological ature (Bidau and Martı´2007, 2008), results are consis- variation in their study, including host plant and the in- tent with the temperature-size rule (von Bertalanffy fluence of other abiotic factors such as temperature, as 1960; Berrigan and Charnov 1994; Atkinson 1994, D. citri had to adapt to a geographical change. A recent 1996; Perrin 1995; Atkinson and Sibly 1997; Klok and survey of populations of D. citri from Iran and Pakistan 4ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA

1.1 Females 1.09 Males 1.08 1.07 1.06 1.05 1.04 width (mm) 1.03

Mean ( ± SEM) Protorax 1.02 1.01 1 El Arenal Autlán de Colima Tecomán (1400 m) Navarro (414 m) (5 m) (894 m)

Locations

Fig. 3. D. citri mean prothorax width 6 SE at four different locations.

0.84 Female 0.82 Male 0.8 0.78 0.76 0.74 Length (mm) 0.72 Mean (±SEM) Antenna 0.7 0.68 El Arenal Autlán de Colima Tecomán (1400 m) Navarro (414 m) (5 m) (894 m) Locations Fig. 4. D. citri mean antenna length 6 SE at four different locations.

Table 2. Nemenyi’s comparison test (post hoc) on forewing showed that most populations with smaller wings were length (WL), forewing width (WW), and antenna length (AN) at D. found at lower elevations (Lashkari et al. 2013). Lash- citri locations kari et al. (2013) suggest that body size variation may be due to climate elements, especially temperature, Location Elevation Mean 6 SEM where populations with smaller wings are more consis- (m) tently found in arid regions with moderate winters and WL WW AN warm summers while larger wings tend to be found in El Arenal 1,400 4.24 6 0.02a 1.75 6 0.01a 0.80 6 0.01a semiarid climates with cool winters and very warm Autlań de 894 4.20 6 0.03b 1.74 6 0.02ab 0.78 6 0.01ab summers. Our data agree with this study in that D. citri Navarro adults from high elevation site (El Arenal), where the Colima 413 4.15.8 6 0.02bc 1.69 6 0.01b 0.76 6 0.01ab Tecomań 5 3.86 6 0.02c 1.70 6 0.01b 0.78 6 0.01b mean annual temperature is 20.6 C, showed larger H ¼ 18.95 H ¼ 19.17 H ¼ 11.44 forewings, while D. citri adults from the low elevation Means within a column followed by the same letter are not signifi- site Tecomań where the mean annual temperature is cantly different (P ¼ 0.05). Kruskal–Wallis (H) test was significantly 26.4 C showed smaller forewings. Today the tempera- different for WL, WW, and AN (P ¼ 0.001, df ¼ 3). ture-size rule still generates controversy, but many have 2015 PE´ REZ-VALENCIA AND MOYA-RAYGOZA: D. citri BODY SIZE VARIATION 5 tried to give an explanation for this positive correlation, et al. 2007, Symonds 2011), but how antennal length as it is commonly observed in ectotherms (von Berta- affects D. citri behavior remains to be examined. lanffy 1960; Berrigan and Charnov 1994; Atkinson D. citri is an invasive insect that arrived to Mexico 1994, 1996; Perrin 1995; Atkinson and Sibly 1997; Klok about 13 yr ago. Since then, its populations have spread and Harrison 2013). Atkinson (1996) proposed that throughout the country, facing different geographic fac- early maturity at a small body size in warm environ- tors and adapting to different habitats with different cli- ments could be caused by constraints on growth that matic conditions. Rapid range expansion suggests that arise during late ontogeny. This proposal could be the species are highly dispersive (Sakai et al. 2001), and closest to a general explanation for the temperature- dispersal capacity is related to flight (Lee 2002). Our size rule, although the fact that it can be applied to the study suggests that larger wings at higher elevations en- majority of surveys related to ectotherms does not guar- hance dispersal ability, such that populations at high el- antee a simple and general explanation for the relation- evations could be considered a major threat. Hill et al. ship between environmental temperature and life (1999) found similar results for the butterfly Pararge history (Angilleta and Dunham 2003). aegeria (L.) and concluded that evolutionary changes in Lashkari et al. (2013) suggested that other possible flight morphology and dispersal rate may be important explanations for wing size variation could include geo- determinants of range expansion, and may affect re- graphic and genetic isolation. Supporting this hypothe- sponses to future climate change. sis, Arnett and Gotelli’s (2003) survey indicates that Although D. citri is of recent origin in Mexico, our Myrmeleon immaculatus (DeGeer) larvae are geneti- study identified phenotypic changes in traits related to cally well differentiated as a result of geographic isola- body size across an elevation gradient. The positive re- tion. Moreover, Euphilotes enoptes (Boisduval), which lationship of size with elevation for at least WL, WW, is closely associated with plant phenology, shows ge- and AN suggests that clines are an adaptive response to netic differentiation along an elevation gradient, sug- elevation and thus to temperature, favoring large size gesting stepwise gene transfer (Peterson 1995). at lower temperatures. Huey et al. (2000) and Gilchrist Consistent with those results, we may be observing ge- et al. (2001) found the same consistently positive corre- netic variation due to geographic conditions, genetic lation of size with latitude in Drosophila subobscura in isolation, and host plant phenology. Future investiga- less than two decades and concluded that North Amer- tions could evaluate those ideas. ican females have rapidly evolved a cline in wing size Larger females usually have high potential fecundity statistically indistinguishable from the European cline. due to the opportunity to lay more eggs than smaller Consequently, high phenotypic plasticity found in the females; however, in ectotherms, physiology is strongly natural populations of D. citri might precede evolution- correlated with temperature (Berger et al. 2008)and ary changes, genetic adaptation to environmental stress, egg laying could be affected by this climatic factor. and a high tolerance for environmental heterogeneity. Because females from El Arenal are bigger, they could Such phenotypic and genetic responses to different have an egg-laying advantage, but what effects geo- temperatures in this introduced pest at low and high el- graphic and climatic factor promote has yet to be deter- evations in Mexico should be the subject of more de- mined. Hall et al. (2011) conducted a study in Florida tailed study in future surveys. to evaluate cold hardiness and temperature thresholds for oviposition in D. citri where they found that mild to moderate freeze events (5to6C for several hours) were nonlethal to D. citri and that lower and upper Acknowledgments thresholds for oviposition were 16.0 and 41.6C, respectively. These extreme temperatures are uncommon We thank Victor Hugo Gomez Flores, Rau´l GarcıáGalvań at our locations, suggesting oviposition is not affected from the Comite´ de Sanidad Vegetal de Jalisco, and Renato at all in lower or higher elevations. Jenkins et al. (2015) Flores Virgen from the Comite´de Sanidad Vegetal de Colima for their help in accessing commercial plantations and collect- argue that abundance of D. citri declines at higher ele- ing D. citri adults. We also thank Pablo Torres Moran and vations, suggesting slow egg development to adult, Alejandro Munõz Urias for their statistical advice and Andrew influenced directly by the temperature. This survey Michel for his comments on this manuscript. was conducted in Puerto Rico and the highest elevation considered was 600 m; a similar study will be helpful at our locations to provide a better understanding of how References Cited temperatures across different elevations can affect Angilleta, M. J., and A. E. Dunham. 2003. The temperature- abundance in D. citri populations. size rule in ectotherms: Simple evolutionary explanations may In this study also AN showed size variation, espe- not be general. Am. 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