Environmental Entomology, 49(4), 2020, 974–982 doi: 10.1093/ee/nvaa068 Advance Access Publication Date: 13 June 2020 Population Ecology Research

Seasonal Population Dynamics of Potato Psyllid

(: Triozidae) in the Columbia River Basin Downloaded from https://academic.oup.com/ee/article/49/4/974/5856891 by University of Missouri-Columbia user on 12 November 2020

1,7 2 3, 4 applyparastyle "fig//caption/p[1]" parastyle "FigCapt" Abigail L. Cohen, Carrie H. Wohleb, Silvia I. Rondon, Kylie D. Swisher Grimm, 5 5 1,6 1 applyparastyle "fig" parastyle "Figure" Isabel Cueva, Joseph E. Munyaneza, Vincent P. Jones, and David W. Crowder

1Department of Entomology, Washington State University, 166 FSHN Building, Pullman, WA 99164, 2Washington State University Extension, 1525 E. Wheeler Road, Moses Lake, WA 98837, 3Oregon State University, Hermiston Agricultural Research and Extension Center, 2121 South 1st Street, Hermiston, OR 97838, 4United States Department of Agriculture—Agricultural Research Service, Temperate Tree Fruit and Vegetable Research Unit, 24106 N. Bunn Road, Prosser, WA 99350, 5United States Department of Agriculture—Agricultural Research Service, Temperate Tree Fruit and Vegetable Research Unit, 5230 Konnowac Pass Road, Wapato, WA 98951, 6Tree Fruit Research & Extension Center, 1100 N Western Avenue, Wenatchee, WA 98801, and 7Corresponding author, e-mail: [email protected]

Subject Editor: Rodrigo Mercader

Received 23 January 2020; Editorial decision 7 May 2020

Abstract Understanding factors that affect the population dynamics of pest species is key for developing integrated pest management strategies in agroecosystems. Most insect pest populations are strongly regulated by abiotic factors such as temperature and precipitation, and assessing relationships between abiotic conditions and pest dynamics can aid decision-making. However, many pests are also managed with insecticides, which can confound relationships between abiotic factors and pest dynamics. Here we used data from a regional monitoring network in the Pacific Northwest United States to explore effects of abiotic factors on populations of an intensively managed potato pest, the potato psyllid ( cockerelli Šulc), which can vector Candidatus Liberibacter psyllaurus, a bacterial pathogen of potatoes. We assessed effects of temperature on psyllid populations, and show psyllid population growth followed predictable patterns within each year, but there was considerable variation across years in psyllid abundance. Examination of seasonal weather patterns suggested that in 2017, when psyllid populations were less abundant by several orders of magnitude than other years, a particularly long and cold period of winter weather may have harmed overwintering populations and limited population growth. The rate of degree-day accumulation over time, as well as total degree-day accumulation also affected trap catch abundance, likely by mediating the number of psyllid generations per season. Our findings indicate that growers can reliably infer the potential magnitude of risk from potato psyllids using monitoring data, date of first detection, seasonal weather patterns, and population size early in the growing season.

Key words: polyphagous pests, phenology, integrated pest management, decision support

Integrated pest management (IPM) strategies require knowledge of Temperature is a reliable predictor of insect development; key life how biotic and abiotic factors in agroecosystems affect pests (Pedigo stages and population dynamics can be estimated based on degree- and Rice 2015). All have physiological traits that are medi- day accumulation (Logan 1988, Nietschke et al. 2007, Jones et al. ated by environmental conditions (Pedigo and Rice 2015), and as- 2013, Sporleder et al. 2013). For many insects, development from sessing how abiotic factors affect pest phenology aids in predicting one life stage to another requires the environment to stay within the timing of insect life stages in the field, and the development of a certain temperature range. Decision-support systems that inte- populations across space and time (Angilletta 2009, Régnière et al. grate temperature data can predict when insect populations may 2012, Chuine and Jacques 2017). Moreover, relationships between reach economic thresholds, and assist growers in targeting insecti- environmental conditions and pest populations can form the foun- cide applications to specific life stages likely to be present (Jones dation of decision-support systems that aid growers in choosing et al. 2010). Such approaches can limit management intensity by management options (Logan 1988; Jones et al. 2009, 2010, 2013; ensuring that insecticide applications are effectively timed based on Sporleder et al. 2013). degree-day models and pest biology. However, insects are affected by

© The Author(s) 2020. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For permissions, please e-mail: [email protected]. 974 Environmental Entomology, 2020, Vol. 49, No. 4 975 factors other than temperature, and identifying additional sources of Pest Monitoring variation, like landscape context (Tscharntke and Brandl 2004) or We established a monitoring network for potato psyllid in com- available moisture (Chown et al. 2011) can improve the accuracy of mercial potato fields across the Columbia River Basin region of population models. Washington and Oregon (Fig. 1A). Data on potato psyllid abun- In this study, we explored how temperature and site-specific dance was collected weekly at each site for 4 yr (2014 to 2017), variation affected populations of potato psyllid (Bactericera cock- with 36 sites sampled per year in Oregon and 43–57 sites per year erelli Šulc), a pest of potato, Solanum tuberosum L. crops in the in Washington (Fig. 1A, Table 1). Each site was monitored using U.S. Pacific Northwest (PNW) (Crosslin et al. 2012, Murphy et al. four 15 × 10 cm yellow sticky cards (AlphaScents, Portland, OR).

2013). Potato psyllids can transmit a bacterial pathogen, Candidatus Downloaded from https://academic.oup.com/ee/article/49/4/974/5856891 by University of Missouri-Columbia user on 12 November 2020 Yellow sticky cards were deployed during the potato vegetative Liberibacter psyllaurus (‘CLp,’ also known as Ca. Liberibacter sola- growth stage, prior to row closure and tuber initiation. Trapping nacearum), which causes the devastating zebra chip disease of potato continued throughout the season, which included tuber maturation. (Hansen et al. 2008, Liefting et al. 2009, Butler and Trumble 2012). Trapping was ceased either at the time of potato harvest, or during As potato psyllids can transmit CLp even at low abundance, many vine kill, which occurs when growers shut off the irrigation to pro- growers are risk-averse in their management programs. Currently, a mote tuber maturation. Traps were placed inside potato fields, about typical potato psyllid management strategy in the PNW is to apply 2–3 m from field edges, and were positioned at the canopy level. All a neonicotinoid at planting, followed by regular insecticide appli- potato psyllids collected were standardized as potato psyllids per site cations, after neonicotinoid residues diminish, until the preharvest per week for data analysis. interval (Goolsby et al. 2007, Schreiber et al. 2018). This is referred Potato psyllids collected in WA were tested for CLp using a to as a ‘no-gaps’ strategy because the pest is controlled throughout cetyl trimethyl ammonium bromide nucleic extraction procedure the season. Since the first outbreak of zebra chip in the Columbia followed by conventional polymerase chain reaction using primers River Basin of Washington and Oregon in 2011, applications target- OA2/OI2c (Crosslin et al. 2011). In 2014, 2015, and 2017, all us- ing potato psyllids have increased grower expenses for insecticides able psyllids were tested for CLp individually. However, in 2016, by over $11M per year (Greenway and Rondon 2018). This has due to the large number of psyllids, this was unfeasible. A subset of threatened the sustainability of potato production as PNW potato potato psyllids collected in 2016 were tested individually, and re- growers typically operate on thin profit margins due to high land, maining specimens were tested for CLp in groups, with up to 30 labor, and transportation costs. A better understanding of popula- psyllids per group (Crosslin et al. 2011). Overall in 2016, a total of tion dynamics should aid in moving away from this expensive, insec- 1,923 individual and grouped samples were tested for CLp, which ticide-heavy, ‘no-gaps’ approach to zebra chip management. included a total of 21,522 psyllids (Supp Table 1 [online only]). To To assess effects of abiotic factors on potato psyllid population date, four different potato psyllid haplotypes (or populations) have dynamics, we used data from a regional monitoring network in sites been identified in geographically distinct, but overlapping regions spread across the Columbia River Basin in Oregon and Washington. of the U.S., identified as the Central, Western, Northwestern, and Absent any temperature extremes that would increase mortality Southwestern haplotypes (Swisher et al. 2012, 2014a). The Western excessively, we hypothesized that there would be a strong positive and Northwestern haplotypes have routinely been identified in the correlation between degree-day accumulation in any given year and PNW, with the Northwestern haplotype overwintering on Solanum potato psyllid abundance, as well as the timing of movement into dulcamara and Lycium spp. and the Western haplotype predomin- potato crops. We also explored how various other weather factors antly overwintering on Lycium spp. (Swisher et al. 2012, 2013a,b; affected psyllid dynamics within and across years. Overall, our study Thinakaran et al. 2017). A subset of psyllids from this study from provides information that can guide potato psyllid management pro- WA (Supp Table 2 [online only]) were haplotyped using high reso- grams, which can aid in reducing the heavy reliance on insecticides lution melting (HRM) analysis of the cytochrome oxidase 1 (CO1) in potato agroecosystems. gene with primers CO1 F3/CO1meltR and CO1 meltF/CO1 meltR (Swisher et al. 2012, 2013a). Sequence analysis of a 500 basepair Materials and Methods amplicon of the CO1 gene generated with primers CO1 F3/CO1 R3 was performed on a subset of samples to verify HRM results Study System (Swisher et al. 2012). If the samples were of low quality and did not is a phloem-feeding hemipteran native have a conclusive high resolution melt or CO1 sequence, they were to western North America that primarily feeds on plants in the considered unknown. Solanaceae family (Butler and Trumble 2012; Munyaneza 2012). Potato psyllids are the vector of the CLp pathogen that causes zebra chip disease, which causes symptoms including necrosis in the tuber, Data Analysis aerial tubers, and leaf chlorosis; symptomatic potatoes are unsuit- We related potato psyllid cumulative trap catch to degree-days. To able for commercial use (Munyaneza et al. 2007, Buchman and calculate degree-days, maximum and minimum daily temperatures Fisher 2012, Crosslin et al. 2012). Potato psyllids acquire CLp in less (in °C) for each site were obtained from the DayMet database with than a day of feeding, and undergo a latent period of about 2 wk be- a 1 km2 resolution (https://daymet.ornl.gov/getdata) (Thornton et al. fore they become infectious (Munyaneza 2012, Sengoda et al. 2014). 2016). Degree-days were calculated using the single sine vertical The CLp pathogen can also spread quickly because infectious psyl- method, where a sine model changes from minimum to maximum lids are able to transmit the pathogen in less than 1 h, and infectious to minimum temperature over 24 h intervals (Baskerville and Emin psyllid populations can rapidly infect many plants even at low popu- 1968). Using the vertical sine method, degree-days do not accumu- lation densities (Buchman et al. 2011). When B. cockerelli reach late after upper or lower thresholds are crossed (Baskerville and relatively high densities, they may infect an entire field before the Emin 1968). pathogen is detected. It remains difficult to identify CLp in potato Data from potato psyllid development on potato was used to crops (Sengoda et al. 2010), and it is often not found until tubers determine the lower threshold for total development (from ovipos- have been tested at a processing plant. ition to adult emergence). We used the duration time in days for 976 Environmental Entomology, 2020, Vol. 49, No. 4 Downloaded from https://academic.oup.com/ee/article/49/4/974/5856891 by University of Missouri-Columbia user on 12 November 2020

Fig. 1. (A) Map of all sampling network sites from 2014 to 2017 in Washington and Oregon. (B) The same sites, separated by year and weighted by total trap catch abundance for the entire year. development from egg to adult from Tran et al. (2012). Using the development duration. We then used linear regression to relate de- mean development duration at six temperatures: 8, 10, 15, 20, 23, velopment rates to temperature. The regression generated a y-inter- and 27°C, we calculated the rate of development, which is 1/mean cept and slope, which we used to calculate the x-intercept, which Environmental Entomology, 2020, Vol. 49, No. 4 977

Table 1. Sampling data from 2014 to 2017

Year State No. of Sampled Fields No. of Sites with >0 Trap Catch First sample Last sample Total abundance

2014 WA 43 40 29 May 25 Sept. OR 36 29 1 May 18 Sept. Combined 79 69 785 2015 WA 44 44 22 May 25 Sept. OR 36 33 1 May 11 Sept. Combined 80 77 4,939 2016 WA 54 53 20 May 23 Sept. Downloaded from https://academic.oup.com/ee/article/49/4/974/5856891 by University of Missouri-Columbia user on 12 November 2020 OR 36 30 25 May 25 Aug. Combined 90 83 23,055 2017 WA 57 22 12 May 13 Oct. OR 36 13 27 Apr. 7 Sept. Combined 93 35 463 is the temperature at which the rate of development crosses zero. Western haplotype (95.3%), with 3.1% Northwestern haplotype We found the lower developmental threshold to be 2.86°C using and 0.2% Central haplotype; 1.3% of psyllids were unknown. These this method. We also used life history data from Lewis et al. (2015) results were consistent across years (Supp Table 2 [online only]). to calculate a threshold 2.15°C; given similarity of these thresholds The magnitude of average trap catches in a year was positively we used the higher value. The upper threshold for reduced devel- associated with the date potato psyllids were first detected, as popu- opment is at 31°C and above, as developmental duration increases lations increased relatively linearly (on a log scale) after the first at that temperature (Tran et al. 2012, Lewis et al. 2015). We chose potato psyllids were captured (Fig. 2A). This may be explained by the vertical sine method, which is used when temperatures above a degree-day accumulation within each year, as the higher abundance threshold arrest development (Baskerville and Emin 1968), because years (2015 and 2016) had higher average daily degree-days in the models of potato psyllid development at all life stages show a steep winter and spring compared to the lower abundance years (2014 drop off after 31°C (Tran et al. 2012). and 2017) (Fig. 2B). By May 1, the year with the highest accumu- We used psyllid trap catch data from 1 May to 25 September in lated degree-days was 2016, and the lowest was 2017 (Fig. 3A; the analyses, reflecting the full range of sampling regimens across the Supp Table 3 [online only]). By the end of the season, 2016 still has years analyzed. We calculated the total average trap catch over time the highest accumulated degree-days while 2017 has the least. This and average daily degree-day accumulation for each year, and plotted means that the year with the highest abundance also had the largest the seasonal dynamics of trap catch across time. We also created his- amount of accumulated degree-days, and the lowest psyllid abun- tograms of average accumulated degree-days for the first instance of dance year had the least degree-days (Fig. 3B; Supp Fig. 1B and Table potato psyllid detection and the total accumulated degree-days at 3 [online only]). The order of most to least degree-days is the same as each site between when first detection occurred and the latest sam- the order of total trap catch: 2016, 2015, 2014, and 2017. pling date of September 25. The weighted average trap catch are cal- culated by dividing the trap catch for each site on a given date by the Psyllid Population Development and Generations total trap catch for that year. We then bin these weighted averages by Per Year 100 degree-days to track population density through the sampling A greater number of degree-days in a season would be expected to season. A bin of 100 is equivalent to the average amount of degree- promote increased development rate of psyllids and an increased days that accumulate in a week in the sampling region. The degree- number of generations of potato psyllids. Potato psyllids are multi- days at the first and last sampling date are binned by 50 degree-days voltine, and the time for a generation to complete development can because they occur over a smaller temporal range. To contextualize be estimated to be approximately 612 degree-days, based on our the degree-days information with seasonal weather data, we plot the regression of the Tran et al. 2012 data. The dotted lines in Fig. 4 daily average minimum and maximum temperature across all sites, indicate these generation intervals. In 2014 through 2016 there are as well as the daily average snowpack. Fig. 1 was generated with two complete generations and a partial third, with the second gen- ArcMap10.4.1 (ESRI 2016) and all other figures were generated eration of 2016 increasing more steeply. Interestingly, the 2017 trap using the ggplot2 package in R (Wickham 2017). catch began earlier than any other year, but the abundance did not increase to the same extent observed in the other years. This is likely a result of three factors: 1) a lag in degree-day accumulation in the Results early season, 2) lower total degree-day accumulation over the course Seasonal Dynamics of the season, and 3) lower initial population densities in that year. The total number of potato psyllids caught increased each year from 2014 to 2016, before decreasing by several orders of magnitude in Effects of Weather on Psyllid Populations 2017 (Fig. 2A; Table 1). In 2014, only 1 out of 706 psyllids tested When looking at seasonal weather patterns, the winter between 2016 positive for CLp, and 0 psyllids tested positive in 2015 (out of 4,760 and 2017 had the lowest daily minimums of any period (Fig. 5A), tested) and 2017 (out of 170 tested) (Supp Table 1 [online only]). and is the only time where daily minimums reached −20°C. These In 2016, two of the bulk groups of psyllids tested positive for CLp; cold snaps also appeared to extend over a considerable number of these groups had 23 and 30 psyllids and thus the total psyllids that days, suggesting a prolonged freeze that may have negatively af- tested positive was between 2 and 53 (0.0093 to 0.25%) (Supp Table fected psyllids in 2017, which had both the lowest total psyllid abun- 1 [online only]). The vast majority of psyllids collected were of the dance and the fewest sites with psyllids (Table 1). 2017 was also the 978 Environmental Entomology, 2020, Vol. 49, No. 4 Downloaded from https://academic.oup.com/ee/article/49/4/974/5856891 by University of Missouri-Columbia user on 12 November 2020

Fig. 2. (A) Log average B. cockerelli trap catch across all locations at weekly intervals (Mean ± SE). The data are presented on a log10 scale to better reflect the difference in magnitude of trap catches between years. (B) The average number of degree-days in a single day, averaged across month, for January–September (Mean ± SE).

Fig. 3. Histograms of the degree-days accumulated at the first (A) and last (B) possible sampling date, for each year. The dotted lines represent the mean degree- days accumulated in each year. The degree-days are binned by 50. Environmental Entomology, 2020, Vol. 49, No. 4 979 Downloaded from https://academic.oup.com/ee/article/49/4/974/5856891 by University of Missouri-Columbia user on 12 November 2020

Fig. 4. The sum of potato psyllid trap catch across all sites by cumulative degree-day. The dotted lines represent 612 degree-days, the estimated number of degree-days needed for the development of a potato psyllid generation. The degree-days are binned by 100.

Munyaneza et al. 2009, Wenninger et al. 2017). This suggests that established populations in potato have at least two distinct gener- ations in the growing season. However, the cumulative abundance of potato psyllids differed considerably across years, and the date of first detection was highly variable across years. Our data suggest that the 2014 and 2015 trap catch may be reflecting two and a partial third generations of growth in the population. The greatest psyllid abundance likely occurred in 2016, which likely reflects both the higher initial population level early in the season and higher tem- peratures that supported a nearly complete third generation (Fig. 4). Overall, our results suggest higher degree-day accumulation before and within the growing season (Figs. 2B and 4), and the date of first detection (Supp Fig. 1A [online only]) are reliable indicators of po- tato psyllid population size later in the season. These results are similar to those for other agricultural pests where early season sampling has strong predictive power. For ex- ample, preseason monitoring is a strong predictor of summer in- festation in the olive fruit fly, Bactrocera oleae (Rossi) (Diptera: Fig. 5. Average minimum temperature for all sampling sites across each year. Tephritidae) (Petacchi et al. 2015) because in warmer regions the in- The dotted line represents the lower temperature development threshold. sect does not enter dormancy, and has an overwintering generation. This principle is also relevant to pests with longer life cycles like only year that had 0 Northwestern haplotype psyllids (Supp Table 2 Asian longhorn beetles, Anoplophora glabripennis (Motschulsky) [online only]), suggesting that the particularly harsh conditions may (Coleoptrea: Cerambicidae), where the number of emergence holes have limited psyllid overwintering survival. in a tree from previous years is an effective predictor of future popu- lation dynamics (Smith et al. 2004). Similarly, our results suggest that by monitoring early season trap catch and winter conditions, Discussion growers may reliably infer the risk of potato psyllids, and potentially Our results indicate there are thresholds to potato psyllid popula- CLp, during peak months. tion development dictated by heat accumulation, which may allow Correlations between decreased degree-day accumulation in the for targeted insecticide sprays and higher potato psyllid mortality spring and low psyllid abundance may be caused by fewer psyllid before the populations can build up. Our data support historical generations in low abundance years. We hypothesize that more data and recent studies, which show potato psyllid populations degree-day accumulation before 1 May increases rates of psyllid have a similar pattern of population growth within seasons, with population growth, allowing potato psyllids to undergo an extra abundance spiking in late June, and again in late July (Wallis 1955, generation before planting of potatoes, leading to a larger overall 980 Environmental Entomology, 2020, Vol. 49, No. 4 population size. For example, 2016 had the highest daily average tied to management, it is difficult to determine how each contribute degree-days in April, the highest average amount of degree-days’ ac- to this variation. cumulated as sampling began, and the largest average trap catch in The make-up and intensity of the management program at a site the first sampling week. In contrast, 2017 had the fewest degree-days depends on the grower and seasonal trends. Conventional growers in the early season, and the lowest average trap catch in the first have the option of treating potato fields with systemic insecticides sampling week (Figs. 2 and 3A; Supp Fig. 1B and Table 3 [online as seed or soil (in-furrow) treatments for early insect pest manage- only]). We thus suggest there may be a direct relationship between ment (Schreiber et al. 2018), but not all choose to do so. Many dif- the date of first detection and the total psyllid trap catch due to extra ferent insecticide products can be applied to the foliage throughout

reproduction in potato fields, although detailed phenology models the growing season (Schreiber et al. 2018), but some growers make Downloaded from https://academic.oup.com/ee/article/49/4/974/5856891 by University of Missouri-Columbia user on 12 November 2020 are needed to assess this hypothesis. fewer applications than others, particularly when pest levels are Our results may also reflect effects of climate on psyllid migra- deemed to be low. As a polyphagous pest, potato psyllid movement tion and development. Prior studies show cold temperatures are as- may be affected by the distribution (Thinakaran et al. 2015, 2017; sociated with decreased psyllid abundance and increased mortality Wenninger et al. 2019) and quality of noncrop hosts in the land- (Henne et al. 2010; Workneh et al. 2013). This was in line with scape (Huot and Tamborindeguy 2017), and it is likely that these our sampling data, as years with the coldest winters were associ- landscape factors also affect the variation of trap catch across sites. ated with the lowest psyllid trap catch (Fig. 5; Table 1). Moreover, Potato psyllids have long adult longevity and several generations as most psyllids in our study were of the migratory Western haplo- a year (Munyaneza 2012), meaning there can be multiple waves type (Swisher et al. 2012; Swisher et al. 2014b), colder winters may of entry into crop fields. However, as yellow sticky cards capture have delayed the date at which they began to migrate into the Pacific adults but not eggs and nymphs, we were unable to classify potato Northwest. Cold winters also limit the development and abundance psyllids into generations. Thus, we cannot know if differences in of weedy alternative hosts such as bittersweet nightshade (S. dulca- potato psyllid abundance between years are due to more gener- mara) and matrimony vine (L. barbarum) that provide early season ations, or higher populations with the same number of generations. resources for psyllids and serve as sources of dispersal into potato The timing of planting may also affect the level of pest pressure in crop fields (Murphy et al. 2013; Nelson et al. 2014; Thinakaran a field (Munyaneza et al. 2012), as could the level of disturbance et al. 2015, 2017) within a colonized field (Nelson et al. 2014). The trap catch in a We hypothesized that temperature would drive potato psyllid given week will be affected by the timing of insecticide applica- populations, but differences in temperature correlate to other en- tions, survival of potato psyllids at all life stages, and their dis- vironmental factors, which may affect variation in potato psyllid persal between fields. abundance across years. Cold snaps can kill host plants and psyl- Our results will be incorporated into existing predictive tools lids, but high amounts of snow may increase available meltwater. for potato producers. There is currently a pest alert newsletter and Warm spring temperatures might decrease die-off of wild hosts or website for Washington growers that includes density maps cre- increase the amount of meltwater available, providing additional ated using an inverse-distance model. In the future, the phenology host resources to overwintering potato psyllid populations. Rainfall data provided in this study, as well as models of other potato pests could affect the availability of alternative hosts in the landscape that and models of disease spread and potato development, could form are not irrigated and depend solely on rainfall and waterways for the backbone of a decision support tool for potato growers that is moisture. Several solanaceous weed species exhibit increased ger- similar to the tree fruit ‘decision aid system’ in Washington State mination with increasing soil osmotic potential (Zhou et al. 2005, (Jones et al. 2010). Continuing to refine these predictive tools will Waggy 2009, Stanton et al. 2012). In the Columbia River Valley, provide more accurate pest forecasts and management suggestions the summer months are usually without rain; precipitation is most that allow for targeted management and increased production likely to occur in late September or October as the potato harvest efficiency. begins and potato psyllids no longer have access to crop hosts. The matrimony vine is an overwintering host of potato psyllids and can have a flush period of vegetative growth triggered by even small Supplementary Data amounts of rain (Thinakaran et al. 2017). Another host is bitter- Supplementary data are available at Environmental Entomology sweet nightshade, found in damp areas like streams and drainage online. ditches (Whitson et al. 2004, Murphy et al. 2013, Castillo Carrillo et al. 2016). Higher degree-day accumulations may have a causal re- lationship with increased potato psyllid because it causes an increase Acknowledgments in population development, or it may be correlated to favorable en- The authors were supported by USDA NIFA awards 2014-51106-22096, vironmental conditions, like increased host plant or water resources. 2015-51181-24292, and 2019-67011-29603 and USDA Hatch award There are some similarities in potato psyllid trap catch across 1014754. In addition, trapping programs in Washington and Oregon were latitude and longitude (Fig. 1B) that may be driven by larger popula- funded by the Washington State Potato Commission and Oregon Potato tion trends and geography. The higher trap catch in 2015 and 2016 Commissions, respectively. Potato psyllid testing was supported by USDA- seen around 46° N may be explained by proximity to the Columbia ARS and US Department of Agriculture Foreign Agricultural Service, River in the southern edge of the range, and the Potholes Reservoir Technical Assistance for Specialty Crops (TASC) program project 2092- 22000-021-17-R. The use of trade, firm, or corporation names in this publi- at the northern edge. There is also a large concentration of potato cation is to provide information for the reader. Such use does not constitute fields in that area. It also appears that the sites with the highest trap an official endorsement or approval by the United States Department of catch in those years were on the eastern edge of the sampling region. Agriculture or the Agricultural Research Service. We thank J. Ilan and S.R. That region is the Central Basin, which has the lowest elevation in Puerh for assistance with data analysis, and employees of WSU Extension Eastern Washington and annual average precipitation that ranges and the Hermiston Agricultural Research and Extension Center who helped from 15 to 35 cm. However, because difference in sampling site is to collect sampling data. Environmental Entomology, 2020, Vol. 49, No. 4 981

References Cited Logan, J. A. 1988. Toward an expert system for development of pest simula- tion models. Environ. Entomol. 17: 359–376. Angilletta, M. J. 2009. Thermal sensitivity, pp. 1–89. In Thermal adaptation: Munyaneza, J. E. 2012. Zebra chip disease of potato: biology, epidemiology, a theoretical and empirical synthesis. Oxford Univeristy Press, Oxford, and management. Am. J. Potato Res. 89: 329–350. United Kingdom. Munyaneza, J. E., J. M. Crosslin, and J. E. Upton. 2007. Association of Baskerville, G. L., and P. Emin. 1968. Rapid estimation of heat accumulation Bactericera cockerelli (Homoptera: ) with ‘zebra chip,’ a new po- from maximum and minimum temperatures. Ecology. 50: 514–516. tato disease in southwestern United States and Mexico. J. Econ. Entomol. Buchman, J. L., and T. W. Fisher. 2012. Zebra chip progression: from inocu- 100: 656–663. lation of potato plants with Liberibacter to development of disease symp- Munyaneza, J. E., J. M. Crosslin, and J. L. Buchman. 2009. Seasonal occur-

toms in tubers. Am. Jo. Pot. Res. 89:159–168. rence and abundance of the potato psyllid, Bactericera cockerelli, in south Downloaded from https://academic.oup.com/ee/article/49/4/974/5856891 by University of Missouri-Columbia user on 12 November 2020 Buchman, J. L., V. G. Sengoda, and J. E. Munyaneza. 2011. Vector trans- central Washington. Am. J. Potato Res. 86: 513–518. mission efficiency of liberibacter by Bactericera cockerelli (Hemiptera: Munyaneza, J. E., J. L. Buchman, V. G. Sengoda, J. A. Goolsby, A. P. Ochoa, Triozidae) in zebra chip potato disease: effects of psyllid life stage and J. Trevino, and G. Schuster. 2012. Impact of potato planting time on in- inoculation access period. J. Econ. Entomol. 104: 1486–1495. cidence of potato zebra chip disease in the lower Rio Grande Valley of Butler, C. D., and J. T. Trumble. 2012. The potato psyllid, Bactericera cock- Texas. Southwest. Entomol. 37: 253–262. erelli (Sulc) (Hemiptera: Triozidae): life history, relationship to plant dis- Murphy, A. F., S. I. Rondon, and A. S. Jensen. 2013. First report of potato psyl- eases, and management strategies. Terr. Rev. 5: 87–111. lids, Bactericera cockerelli, overwintering in the Pacific Northwest. Am. Castillo Carrillo, C. I., Z. Fu, A. S. Jensen, and W. E. Snyder. 2016. Arthropod pests and J. Potato Res. 90: 294–296. predators associated with bittersweet nightshade, a noncrop host of the potato Nelson, W. R., K. D. Swisher, J. M. Crosslin, and J. E. Munyaneza. 2014. psyllid (Hemiptera: Triozidae). Environ. Entomol. 45: 873–882. Seasonal dispersal of the potato psyllid, Bactericera cockerelli, into potato Chown, S. L., J. G. Sørensen, and J. S. Terblanche. 2011. Water loss in insects: crops. Southwest Entomol. Perspect. 39: 177–187. an environmental change perspective. J. Insect Physiol. 57: 1070–1084. Nietschke, B. S., R. D. Magarey, D. M. Borchert, D. D. Calvin, and E. Jones. Chuine, I., and R. Jacques. 2017. Process-based models of phenology for 2007. A developmental database to support insect phenology models. plants and . Annu. Rev. Ecol. Evol. Syst. 48: 159–182. Crop Prot. 26: 1444–1448. Crosslin, J. M., H. Lin, and J. E. Munyaneza. 2011. Detection of ‘Candidatus Pedigo, L. P., and M. E. Rice. 2015. Insect ecology, pp. 177–212. In Entomology Liberibacter solanacearum’ in the potato psyllid, Bactericera cockerelli and pest management. Waveland Press, Long Grove, IL. (Sulc), by conventional and real-time PCR. Southwest Entomol. Perspect. Petacchi, R., S. Marchi, S. Federici, and G. Ragaglini. 2015. Large-scale simu- 36: 125–136. lation of temperature-dependent phenology in wintering populations of Crosslin, J. M., P. B. Hamm, J. E. Eggers, S. I. Rondon, V. G. Sengoda, and Bactrocera oleae (Rossi). J. Appl. Entomol. 139: 496–509. J. E. Munyaneza. 2012. First report of zebra chip disease and ‘Candidatus Régnière, J., J. Powell, B. Bentz, and V. Nealis. 2012. Effects of temperature on Liberibacter solanacearum’ on potatoes in Oregon and Washington State. development, survival and reproduction of insects: experimental design, Plant Dis. 96: 452. data analysis and modeling. J. Insect Physiol. 58: 634–647. Goolsby, J. A., J. Adamczyk, B. Bextine, D. Lin, J. E. Munyaneza, and Schreiber, A., K. Pike, A. Jensen, S. Rondon, E. J. Wenninger, and S. Reitz. G. Bester. 2007. Development of an IPM program for management of 2018. Integrated pest management guidelines for insects and mites in the potato psyllid to reduce incidence of zebra chip disorder in potatoes. Idaho, Oregon and Washington potatoes. Northwest Potato Research Subtrop. Plant Sci. 59: 85–94. Consortium, Lakeview, OR. Greenway, G. A., and S. Rondon. 2018. Economic impacts of zebra chip in Sengoda, V. G., J. E. Munyaneza, J. M. Crosslin, J. L. Buchman, and Idaho, Oregon, and Washington. Am. J. Potato Res. 95: 362–367. H. R. Pappu. 2010. Phenotypic and etiological differences between psyllid Hansen, A. K., J. T. Trumble, R. Stouthamer, and T. D. Paine. 2008. A new yellows and zebra chip diseases of potato. Am. J. Potato Res. 87: 41–49. Huanglongbing Species, ‘Candidatus Liberibacter psyllaurous,’ found to Sengoda, V. G., W. R. Cooper, K. D. Swisher, D. C. Henne, and J. E. Munyaneza. infect tomato and potato, is vectored by the psyllid Bactericera cockerelli 2014. Latent period and transmission of ‘Candidatus Liberibacter sola- (Sulc). Appl. Environ. Microbiol. 74: 5862–5865. nacearum’ by the potato psyllid Bactericera cockerelli (Hemiptera: Henne, D., L. Paetzold, F. Workneh, and C. M. Rush. 2010. Evaluation of Triozidae). PLoS One. 9: 1–10. potato psyllid cold tolerance, overwintering survival, sticky trap sampling, Smith, M. T., P. C. Tobin, J. Bancroft, G. Li, and R. Gao. 2004. Dispersal and effects of Liberibacter on potato psyllid alternative host plants, pp. and spatiotemporal dynamics of Asian Longhorned Beetle (Coleoptera: 149–153. In Proc. 10th Annu. 2010 Zebra Chip Report. Sess. Specialty Cerambycidae) in China. Environ. Entomol. 33: 435–442. Crop Research Initiative (SCRI), Dallas, TX. Sporleder, M., H. E. Z. Tonnang, P. Carhuapoma, J. C. Gonzales, H. Juarez, Huot, O. B., and C. Tamborindeguy. 2017. Drought stress affects Solanum and J. Kroschel. 2013. Insect life cycle modelling (ILCYM) software—a lycopersicum susceptibility to Bactericera cockerelli colonization. new tool for regional and global insect pest risk assessments under cur- Entomol. Exp. Appl. 165: 70–82. rent and future climate change scenarios, pp. 412–428. In J. E. Pena (ed.), Jones, V. P., T. R. Unruh, D. R. Horton, N. J. Mills, J. F. Brunner, E. H. Beers, Potential invasive pests of agricultural crops: trees for society and the en- and P. W. Shearer. 2009. Tree fruit IPM programs in the western United vironment. CABI, Boston, MA. States: the challenge of enhancing biological control through intensive Stanton, R., H. Wu, and D. Lemerle. 2012. Factors affecting silverleaf night- management. Pest Manag. Sci. 65: 1305–1310. shade (Solanum elaeagnifolium) germination. Weed Sci. 60: 42–47. Jones, V. P., J. F. Brunner, G. G. Grove, B. Petit, G. V. Tangren, and W. E. Jones. Swisher, K. D., J. E. Munyaneza, and J. M. Crosslin. 2012. High resolution 2010. A web-based decision support system to enhance IPM programs in melting analysis of the cytochrome oxidase I gene identifies three haplo- Washington tree fruit. Pest Manag. Sci. 66: 587–595. types of the potato psyllid in the United States. Environ. Entomol. 41: Jones, V. P., R. Hilton, J. F. Brunner, W. J. Bentley, D. G. Alston, B. Barrett, 1019–1028. R. A. Van Steenwyk, L. A. Hull, J. F. Walgenbach, W. W. Coates, et al. Swisher, K. D., J. E. Munyaneza, and J. M. Crosslin. 2013a. Temporal and 2013. Predicting the emergence of the codling moth, Cydia pomonella spatial analysis of potato psyllid haplotypes in the United States. Environ. (Lepidoptera: Tortricidae), on a degree-day scale in North America. Pest Entomol. 42: 381–393. Manag. Sci. 69: 1393–1398. Swisher, K. D., V. G. Sengoda, J. Dixon, E. Echegaray, A. F. Murphy, Lewis, O. M., G. J. Michels, E. A. Pierson, and K. M. Heinz. 2015. A pre- S. I. Rondon, J. E. Munyaneza, and J. M. Crosslin. 2013b. Haplotypes of dictive degree day model for the development of Bactericera cockerelli the potato psyllid, Bactericera cockerelli, on the wild host plant, solanum (Hemiptera: Triozidae) Infesting Solanum tuberosum. Environ. Entomol. dulcamara, in the Pacific northwestern United States. Am. J. Potato Res. 44: 1201–1209. 90: 570–577. Liefting, L. W., P. W. Sutherland, L. I. Ward, K. L. Paice, B. S. Weir, and Swisher, K. D., D. C. Henne, and J. M. Crosslin. 2014a. Identification of a G. R. G. Clover. 2009. A New ‘Candidatus liberibacter’ species associated fourth haplotype of Bactericera cockerelli (Hemiptera: Triozidae) in the with diseases of solanaceous crops. Plant Dis. 93: 208–214. United States. J. Insect Sci. 14: 1–7. 982 Environmental Entomology, 2020, Vol. 49, No. 4

Swisher, K. D., V. G. Sengoda, J. Dixon, J. E. Munyaneza, A. F. Murphy, Wallis, R. L. 1955. Ecological studies on the potato psyllid as a pest of pota- S. I. Rondon, B. Thompson, A. V. Karasev, E. J. Wenninger, N. Olsen, et al. toes, pp. 1–25. In USDA Tech. Bull. 1107. Washington, DC. 2014b. Assessing potato psyllid haplotypes in potato crops in the Pacific Wenninger, E. J., A. Carroll, J. Dahan, A. V. Karasev, M. Thornton, J. Miller, northwestern United States. Am. J. Potato Res. 91: 485–491. P. Nolte, N. Olsen, and W. Price. 2017. Phenology of the potato Thinakaran, J., E. Pierson, M. Kunta, J. E. Munyaneza, C. M. Rush, and psyllid, Bactericera cockerelli (Hemiptera: Triozidae), and ‘Candidatus D. C. Henne. 2015. Silverleaf Nightshade (Solanum elaeagnifolium), a Liberibacter solanacearum’ in commercial potato fields in Idaho. Environ. reservoir host for ‘Candidatus Liberibacter solanacearum’, the putative Entomol. 46: 1179–1188. causal agent of zebra chip disease of potato. Plant Dis. 99: 910–915. Wenninger, E. J., J. Dahan, M. Thornton, and A. V. Karasev. 2019. Thinakaran, J., D. R. Horton, W. Rodney Cooper, A. S. Jensen, C. H. Wohleb, Associations of the potato psyllid and ‘Candidatus Liberibacter

J. Dahan, T. Mustafa, A. V. Karasev, and J. E. Munyaneza. 2017. solanacearum’ in Idaho with the noncrop host plants bitter- Downloaded from https://academic.oup.com/ee/article/49/4/974/5856891 by University of Missouri-Columbia user on 12 November 2020 Association of potato psyllid (Bactericera cockerelli; Hemiptera: Triozidae) sweet nightshade and field bindweed. Environ. Entomol. 28: with Lycium spp. (Solanaceae) in potato growing regions of Washington, 470–476. Idaho, and Oregon. Am. J. Potato Res. 94: 490–499. Whitson, T. D., L. C. Burrill, S. A. Dewey, D. W. Cudney, B. E. Nelson, Thornton, P. E., M. M. Thornton, B. W. Mayer, Y. Wei, R. Devarakonda, R. D. Lee, R. Parker, D. A. Ball, C. L. Elmore, R. G. Lym, et al. R. S. Vose, R. B. Cook. 2016. Daymet: daily surface weather data on a 2004. Weeds of the west, 9th ed. Western Society of Weed Science, 1-km grid for North America, version 3. ORNL DAAC, Oak Ridge, TN. Jackson, WY. doi:10.3334/ORNLDAAC/1328 Wickham, H. 2017. ggplot2—elegant graphics for data analysis. J. Stat. Softw. Tran, L. T., S. P. Worner, R. J. Hale, and D. A. Teulon. 2012. Estimating 77: 317–320. development rate and thermal requirements of Bactericera cockerelli Workneh, F., D. C. Henne, J. A. Goolsby, J. M. Crosslin, S. D. Whipple, (Hemiptera: Triozidae) reared on potato and tomato by using linear and J. D. Bradshaw, A. Rashed, L. Paetzold, R. M. Harveson, and C. M. Rush. nonlinear models. Environ. Entomol. 41: 1190–1198. 2013. Characterization of management and environmental factors as- Tscharntke, T., and R. Brandl. 2004. Plant-insect interactions in fragmented sociated with regional variations in potato zebra chip occurrence. landscapes. Annu. Rev. Entomol. 49: 405–430. Phytopathology. 103: 1235–1242. Waggy, M A. 2009. Solanum dulcamara. In Fire effects information system Zhou, J., E. L. Deckard, and W. H. Ahrens. 2005. Factors affecting germin- [Online]. U.S. Department of Agriculture, Forest Service, Rocky Mountain ation of hairy nightshade (Solanum sarrachoides) seeds. Weed Sci. 53: Research Station, Fire Sciences Laboratory, Missoula, MT. 41–45.