Am. J. Pot Res (2009) 86:513–518 DOI 10.1007/s12230-009-9108-9

Seasonal Occurrence and Abundance of the Potato Psyllid, cockerelli, in South Central Washington

Joseph E. Munyaneza & James M. Crosslin & Jeremy L. Buchman

Published online: 14 August 2009 # Potato Association of America 2009

Abstract The potato psyllid, Bactericera cockerelli Sulc, psyllids migrating to Washington has not yet been deter- has recently been identified as a vector of Candidatus mined. Information from this study will help potato growers in solanacearum, the putative causal agent of Washington manage the potato psyllid to better prevent zebra chip potato disease. Zebra chip is causing millions of potential zebra chip outbreaks. dollars in losses to the potato industry in the United States, Mexico, Central America, and New Zealand. Currently, the Resumen El psílido de la papa, Bactericera cockerelli most effective strategy to manage this potato disease is to Sulc, se ha identificado recientemente como un vector de target the potato psyllid with insecticides. Effective man- Candidatus Liberibacter solanacearum, el presunto agente agement of this pest requires knowledge of its causal de la enfermedad de la papa Zebra chip. Esta biology, ecology, geographic distribution, and population enfermedad esta causando millones de dólares en pérdidas dynamics. Although it is well documented that the potato en la industria de la papa en Estados Unidos, México, psyllid is common throughout the western United States, Centroamérica y Nueva Zelanda. Actualmente, la estrategia several reports have indicated that this insect pest does not más efectiva para manejar esta enfermedad de la papa es occur in Washington and Oregon. However, this insect has enfocarse al psílido de la papa con insecticidas. El manejo recently been observed and collected in this region. Studies efectivo de este insecto plaga requiere del conocimiento de were conducted from 2005 to 2008 to document and su biología, ecología, distribución geográfica y dinámica determine the seasonal occurrence of the potato psyllid in poblacional. Aún cuando está bien documentado que el this important potato growing region of the United States. psílido de la papa es común a lo largo del oeste de los The potato psyllid was monitored in untreated experi- Estados Unidos, varios reportes indican que este insecto no mental potato plots at Moxee and Prosser in south central se presenta en Washington y Oregon. No obstante, se le ha Washington. Contrary to previous reports, the potato observado y colectado a este insecto en esta región. Se han psyllid was found to occur in Washington and appears to hecho estudios de 2005 a 2008 para documentar y migrate into the region late in the growing season. Upon determinar la ocurrencia estacional del psílido de la papa arrival in south central Washington in late July, this en esta región tan importante de cultivo de papa en los insect readily reproduces in potatoes and appears to have Estados Unidos. El psílido de la papa se ha monitoreado en at least one generation a year. The origin of potato lotes experimentales de papa no tratados en Moxee y Prosser en la parte centro-sur de Washington. Contrario a reportes previos, se ha visto que el psílido de la papa se * : J. E. Munyaneza ( ) J. L. Buchman presenta en Washington y parece migrar al interior de la USDA-ARS, Yakima Agricultural Research Laboratory, 5230 Konnowac Pass Road, región al final del ciclo de cultivo. Al llegar al centro sur de Wapato, WA 98951, USA Washington a finales de julio, el insecto se reproduce e-mail: [email protected] rápidamente en papa y parece tener por lo menos una generación al año. Aun no ha sido determinado el origen de J. M. Crosslin USDA-ARS, Vegetable and Forage Crops Research Unit, los psílidos de papa que emigran a Washington. La Prosser, WA 99350, USA información de este estudio ayudará a los productores de 514 Am. J. Pot Res (2009) 86:513–518 papa en Washington a manejar el psílido para una mejor Idaho, Montana, Alberta and Saskatchewan (Pletsch 1947; prevención de establecimientos potenciales de zebra chip. Wallis 1955). This insect pest is common in western Texas and has also been documented in Oklahoma, Kansas, Nebraska, Keywords Potato psyllid . Bactericera cockerelli . Potato . South Dakota, North Dakota, Minnesota and as far west as Zebra chip . Candidatus Liberibacter . Population dynamics California and British Columbia (Richards and Blood 1933; Pletsch 1947; Wallis 1955; Abernathy 1991; Ferro and Boiteau 1993; Cranshaw 1994, 2001; Capinera 2001). The potato Introduction psyllid also occurs in Mexico (Pletsch 1947; Wallis 1955; Rubio-Covarrubias et al. 2006). Several reports indicate that Zebra chip, an important and emerging disease of potato, this insect appears to migrate annually with wind and high Solanum tuberosum L., has been documented in commer- temperatures in late spring to northerly regions from its cial potato fields throughout the southwestern United overwintering and breeding areas in western Texas, southern States, Mexico, Central America, and most recently New New Mexico, Arizona, California, and northern Mexico Zealand (Munyaneza et al. 2007a; Liefting et al. 2008). (Pletsch 1947; Wallis 1955;Abernathy1991; Ferro and This disease is causing millions of dollars in losses to the Boiteau 1993; Cranshaw 1994, 2001; Capinera 2001). potato industry in affected areas, often leading to the Despite abundant documentation of its distribution throughout abandonment of entire potato fields (Munyaneza et al. the western United States, several reports indicate that the 2007a, b; 2008). Zebra chip is characterized by symptoms potato psyllid does not occur in the Pacific Northwest, that develop in tubers from infected potato plants and that particularly in the states of Washington and Oregon (Pletsch consist of a striped pattern of necrosis in tubers (Munyaneza 1947; Wallis 1955; Ferro and Boiteau 1993;Cranshaw1994, et al. 2007a, b; 2008). Potato chips and fries processed from 2001). However, this insect has recently been observed and infected tubers are commercially unacceptable. Zebra chip- collected in Washington (Munyaneza et al. 2008;Munyaneza infected potato plants exhibit a range of foliar symptoms that and Crosslin, unpublished data), although no formal report resemble those caused by potato purple top and psyllid on its occurrence in this region has been published. yellows diseases (Wallis 1955;Cranshaw1994;Crosslinet The Pacific Northwest, and the Columbia Basin of al. 2005; Munyaneza et al. 2006, 2007a, b; 2008). The Washington and Oregon in particular, is an important potato disease was first identified in potato fields near Saltillo, growing region of the United States. Although no zebra chip Coahuila, Mexico, in 1994, and it was first documented in has so far been documented in potato fields in the Columbia the United States in 2000 in commercial potato fields near Basin, insect transmission experiments conducted in south Pearsall and lower Rio Grande Valley in Texas (Secor and central Washington under controlled field cage conditions Rivera-Varas 2004). In addition to Texas, zebra chip has early in the growing season indicated that the potato psyllid been documented in Nebraska, Colorado, Kansas, Wyoming, can induce typical zebra chip symptoms in potato plants and New Mexico, Arizona, Nevada, and California (Munyaneza tubers for potato crops grown in this geographic region et al. 2007a; Crosslin and Bester 2009; Lin et al. 2009). (Munyaneza et al. 2007a; Munyaneza, unpublished data). The causal agent(s) and vectors of zebra chip were Additional transmission studies conducted under controlled unknown. However, recent studies conducted in US, field conditions in Texas showed that potato psyllids Mexico, and New Zealand have shown that zebra chip is collected from Washington readily produced zebra chip associated with a previously undescribed species of the (Munyaneza et al. 2008). These observations suggest that bacterium Candidatus Liberibacter vectored by the potato this insect could potentially cause serious damage to potatoes psyllid, Bactericera cockerelli Sulc (Munyaneza et al. 2007a, with zebra chip in the Columbia Basin, especially if it were b;Hansenetal.2008;Lieftingetal.2008; Munyaneza et al. to migrate into the region early in the season. There is a need 2008;Abadetal.2009;CrosslinandBester2009;Crosslin for information on the population dynamics of this insect and Munyaneza 2009;Lieftingetal.2009a, b; Lin et al. pest in this important potato growing region to better prevent 2009; Munyaneza et al. 2009; Secor et al. 2009). Effective potential zebra chip outbreaks. The objective of the present monitoring and control of the potato psyllid are essential in study was to document and determine the seasonal occur- order to better manage zebra chip in potatoes (Goolsby et al. rence and abundance of the potato psyllid at two sites in 2007; Gharalari et al. 2009; Munyaneza, unpublished data). south central Washington. Thus, increasing the understanding of the distribution, movement, and population dynamics of this insect pest is important to reduce incidence of zebra chip in potatoes. Materials and Methods The potato psyllid is native to North America and occurs mainly in the Rocky Mountain region, from Colorado, New From 2005 to 2008, the potato psyllid was monitored in Mexico, Arizona, and Nevada, north to Utah, Wyoming, experimental potato plots at the USDA-ARS Research Am. J. Pot Res (2009) 86:513–518 515

Farm at Moxee, Yakima County, WA. Additional psyllid compared by converting collected data to number of monitoring was conducted in a potato plot at USDA-ARS psyllids per 100 sweeps or potato leaves on each sampling in Prosser, Benton County, WA, in the 2008 growing date and performing a Chi-Square test (PROC FREQ; SAS season. At both locations, the experimental plots consisted Institute 2003). Repeated measures analysis of variance was of large blocks (ca. 8 rows × 100 m long each) of potatoes performed following transformation of count data using

(cv. Atlantic). Atlantic potatoes were selected because log10(x+1) and the level of significance was set at P=0.05. previous observations (Munyaneza et al. 2007a, b; 2008) have shown that this chipping cultivar is very susceptible to zebra chip and is commonly grown in the regions that are Results and Discussion severely affected by the disease. During each season and at each location, potatoes were planted in mid-May and Contrary to previous reports, results of the present study harvested in mid-October. A pre-plant herbicide (Eptam® clearly showed that the potato psyllid occurs in Washing- 7-E, Gowan, Yuma, AZ) was used to control weeds. Also, ton. For four growing seasons (2005–2008), this insect was Triple-16 fertilizer (J. R. Simplot Inc., Boise, ID) was observed and readily collected in potatoes at Moxee and in applied before potato planting at the rate of 285 kg/ha. Prosser (Figs. 1 and 2) in south central Washington. It is Irrigation of the potatoes was accomplished by sprinklers. also probable that this insect occurs in Oregon since At all sampling locations, the potatoes were not treated with potatoes grown on the south side of the Columbia River insecticides (except Bacillus thuringiensis for Colorado in Oregon are within 80 km of the Prosser site. potato beetle control) to allow the psyllids to colonize the Data collected during the present study suggests that the experimental plots. No fungicide was applied to the potato psyllid does not overwinter in south central potatoes. During each season, psyllid monitoring and sampling were initiated at both study sites in early June, shortly after plant emergence. Psyllid adults in the plots a 400 were collected using heavy duty sweep nets (BioQuip 2005 2006 Products, Inc., Gardena, CA), with a 30 cm net hoop. Four 2007 2008 100-sweep samples were randomly taken in the plot weekly 300 at each sampling site. Psyllid nymphs were sampled weekly at each study site by randomly hand picking four samples of 100 mature and fully expanded potato leaves each; the 200 leaves were collected from the middle portion of the plant canopy (Wallis 1955). All sweep and leaf samples were transferred to plastic bags, placed in coolers, and brought to 100 the laboratory at the USDA-ARS in Wapato, WA, for processing. The samples were checked for potato psyllid Number of psyllid adults/100 sweeps 0 nymphs and adults, and the numbers of both stages were 8/5 9/2 9/9 7/15 7/22 7/29 8/12 8/19 8/26 9/16 9/23 9/30 10/7 recorded. b Samples of psyllids collected from Moxee and Prosser, 400 were submitted for identification. The psyllids were 2006 2007 identified by Ethan C. Kane at the Systematic Entomology 2008 Laboratory, USDA-ARS, Beltsville, MD. The psyllid 300 samples were determined to be potato psyllids, B. cock- erelli. Voucher specimens are deposited at the USDA-ARS 200 Yakima Agricultural Research Laboratory Insect Collec- tion, Wapato, WA.

Seasonal occurrence and abundance of the potato psyllid 100 adults at Moxee was compared within and between growing seasons (2005–2008) by converting collected Number of psyllid nymphs/100 leaves sweep count data to the number of psyllids per 100 sweeps 0 8/5 9/2 9/9 7/15 7/22 7/29 on each sampling date and then statistically analyzing the 8/12 8/19 8/26 9/16 9/23 9/30 10/7 converted data using a repeated measures analysis of Sampling date variance (PROC GLM; SAS Institute 2003). Similarly, Fig. 1 Average number of potato psyllid adults (a) and nymphs (b) occurrence of nymphal and adult populations of potato per 100 sweeps or potato leaves on each sampling date at Moxee, WA. psyllid at Moxee and Prosser in each growing season was Data show psyllid nymphs collected only in 2006, 2007, and 2008 516 Am. J. Pot Res (2009) 86:513–518

Washington but migrates into the region late in the growing 2006 (χ2=96.0; P=0.0309), 2007 (χ2=112.0; P=0.0106), season. During the four years of the study, the potato and 2008 (χ2=102.0; P=0.0246), and in Prosser in 2008 psyllid consistently arrived at Moxee in late July, with (χ2=120.0; P=0.0392), indicating that the two values were peaks of psyllid adults in late August to early September in not independent during each growing season. Peaks of 2005 and 2006 and mid- to late September in 2007 and nymphal populations were observed at Moxee in mid- to 2008 (Fig. 1a). Similar observations were made in Prosser late August in 2006, and early to mid-September in 2007 in 2008, with a peak of psyllid adults occurring in early to and 2008 (Fig. 1b). A peak of nymphs was observed early late September (Fig. 2). No psyllids were observed in the to mid-August to early in 2008 at Prosser (Fig. 2). These plots before late July, despite presence of potato plants at observations also suggest that there is at least one the study sites beginning early June. Comparison between generation produced in local potatoes by this insect in the occurrence of the potato psyllid adults in potatoes at south central Washington. In general, numbers of collected Moxee over the four years (Fig. 1a) indicated that there nymphs were lower than those of adults. Differences were significant differences in the timing of colonization of between nymph and adult numbers may be due to sampling the potatoes by this insect pest among the different years methods used during the study and mobility of these two (F=30.20; df= 3, 12; P<0.0001). There were also signif- insect stages. Sweep samples are more effective in icant differences in abundance of psyllid adults between the capturing adults which are very active and jump quickly sampling dates (F=60.28; df= 13, 156; P<0.0001). In into the air when disturbed whereas picking leaves allows addition, there was a significant interaction between the to effectively collect nymphs that are usually found on the different years and sampling dates (F=9.45; df= 39, 156; underside sides of leaves and rarely move far from the leaf P<0.0001), suggesting that the psyllid abundance varied on which they hatched and feed (Wallis 1955). with the growing season and date of sampling (Fig. 1a). It is well documented that the potato psyllid overwinters However, specific factors behind this variation in psyllid in desert areas along the border between United States and abundance are not known. Mexico on several native shrubs, primarily Lycium spp. The results of the present study also indicated that the (Pletsch 1947; Wallis 1955;Abernathy1991; Ferro and potato psyllid readily reproduced in potatoes upon arrival in Boiteau 1993;Cranshaw1994, 2001; Capinera 2001). It has the surveyed region and that nymphs were collected in high also been reported that breeding on winter hosts by the numbers within 2–3 weeks of adult arrival always prior to potato psyllid occurs from January through May (Pletsch adult peaks (Figs. 1 and 2). This suggests that the increase 1947; Wallis 1955;Abernathy1991;Cranshaw1994, 2001). in numbers of collected psyllid adults is the result of local During this time, psyllids may also migrate to winter- breeding of the insect. Numbers of potato psyllid adults and grown solanaceous crops in the overwintering region. With nymphs collected at Moxee and in Prosser were compared the arrival of warmer weather and desiccation of winter for each growing season from 2006 to 2008 (Figs. 1 and 2). hosts, the potato psyllid migrates to northern areas. Statistical analysis showed that there was a strong correla- Cranshaw (2001) reported that psyllids often begin to tion between adult and nymphal populations at Moxee in arrive at their summer areas, primarily Colorado, Wyoming, Utah, and western Nebraska, by mid- to late June, and

200 that early-season solanaceous weeds and potatoes are Adults common hosts. Although the origin of psyllids migrating Nymphs to Washington is not known, these observations could 160 explain the timing of the arrival of the potato psyllid in this northerly region of south central Washington in late 120 July, about 7–8 weeks later compared to these summer breeding locations (Figs. 1 and 2).

80 Several authors (Richards and Blood 1933; Pletsch 1947; Wallis 1955; Abernathy 1991;Cranshaw1994, 2001; Capinera 2001) reported that the principal factors 40 affecting psyllid outbreaks are largely related to conditions that affect late-spring and early-summer migrations from Number of psyllids/100 sweeps or leaves 0 overwintering areas. These include the size of the spring population developing on winter hosts, wind patterns and Sampling date temperature during migration, and the suitability of host plants along the migratory path. The potato psyllid seems to Fig. 2 Average number of potato psyllid adults per 100 sweeps and nymphs per 100 potato leaves on each sampling date in Prosser, WA. be adapted for warm, but not hot weather. Cool weather Psyllid sampling was conducted only in 2008 during migrations, or at least the absence of elevated Am. J. Pot Res (2009) 86:513–518 517 temperatures, has been associated with several outbreaks biotype including populations from eastern Mexico and (Wallis 1955; Capinera 2001; Cranshaw 2001). Optimum central United States (including Texas, Colorado, and psyllid development occurs at approximately 27°C, where- Nebraska). The group to which the psyllids migrating to as oviposition, hatching, and survival are reduced at 32°C Washington belong to has not yet been identified, making it and cease at 35°C, and a single generation may be impossible to accurately determine the origin of these completed in 3 to 5 weeks (List 1939; Wallis 1955; psyllids and better predict potential zebra chip outbreaks. Cranshaw 1994, 2001; Capinera 2001; Abdullah 2008). In summary, contrary to previous reports, results of the Temperatures begin to cool down in south central Wash- present study clearly show that the potato psyllid does ington by the time potato psyllid arrives in the region, occur in Washington and appears to migrate into the region favoring reproduction of this insect before freezing temper- late in the growing season. Upon arrival in south central atures in early to mid-October, decreasing day length, and Washington, the potato psyllid reproduces in potatoes and the scarcity of alternative host plants (due to arid conditions appears to have at least one generation a year. The reasons in the area) negatively affect the insect reproduction and behind this recent distribution and the origin of potato survival, thereby limiting the number of generations that psyllids migrating to Washington have not yet been this insect can produce in south central Washington. determined. Although some of the potato psyllid popula- To date, no zebra chip has been observed in Washington tions arriving in south central Washington carry Ca. commercial potato fields (Andy Jensen, Washington State Liberibacter solanacearum (Liefting et al. 2009b), the Potato Commission, personal communication), in addition putative causal agent of zebra chip, to date the disease has to the experimental potato plots in the study (Munyaneza, not been observed in Washington potatoes. Effective personal observations). However, zebra chip-inducing monitoring and control of the potato psyllid are crucial for potato psyllid populations have been identified and collect- prevention and management of potential zebra chip out- ed in this region (Munyaneza et al. 2008) and transmission breaks in this important potato growing region of the experiments conducted under controlled cage conditions in Pacific Northwest. Additional studies are needed to gain Texas (Munyaneza et al. 2008) and Washington in early more information on the seasonal occurrence of the potato summer (Munyaneza, unpublished data) using from psyllid throughout the Columbia Basin of Washington and these populations demonstrated that psyllids which have Oregon and factors that may influence the migration of this migrated to Washington can cause typical zebra chip insect pest and potential development of zebra chip symptoms in both potato plants and tubers. Moreover, Ca. outbreaks into the region. Information from the present Liberibacter solanacearum has been detected in some of study provides an update to previously existing literature on these populations (Liefting et al. 2009b; Lin et al. 2009; the distribution of the potato psyllid in North America. Munyaneza, unpublished data). It is not clear why zebra chip does not occur in this important potato growing Acknowledgments We thank Jeff Upton, Millie Heidt, Dan Hallauer, region, despite the occurrence of zebra chip-inducing potato Blaine Heilman, and Launa Hamlin for their invaluable technical assistance. We also thank Ethan C. Kane at the Systematic Entomology psyllids in the area. It is suspected that cool temperatures Laboratory, USDA-ARS, Beltsville, MD, for his assistance in the prevailing at the time the potato psyllid migrates into the identification of collected psyllids. We are also grateful to anonymous region may not be conducive to or delay zebra chip reviewers who made suggestions to an earlier draft of this manuscript. symptom expression, or that mature potato plants may Financial support for this work was partially provided by Frito Lay, Inc. and the USDA-ARS State Cooperative Potato Research Program. show some resistance or tolerance to the disease. 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