PLANT-INSECT INTERACTIONS Factors Influencing Aster Leafhopper (Hemiptera: Cicadellidae) Abundance and Aster Yellows Phytoplasma Infectivity in Wisconsin Carrot Fields 1 2 3 3 4 K. E. FROST, P. D. ESKER, R. VAN HAREN, L. KOTOLSKI, AND R. L. GROVES Environ. Entomol. 42(3): 477Ð490 (2013); DOI: http://dx.doi.org/10.1603/EN12239 ABSTRACT In Wisconsin, vegetable crops are threatened annually by infection of the aster yellows phytoplasma (AYp), the causal agent of aster yellows (AY) disease, vectored by the aster leafhopper, Macrosteles quadrilineatus Forbes. Aster leafhopper abundance and infectivity are inßuenced by processes operating across different temporal and spatial scales. We applied a multilevel modeling approach to partition variance in multiÞeld, multiyear, pest scouting data sets containing temporal and spatial covariates associated with aster leafhopper abundance and infectivity. Our intent was to evaluate the relative importance of temporal and spatial covariates to infer the relevant scale at which ecological processes are driving AY epidemics and identify periods of elevated risk for AYp spread. The relative amount of aster leafhopper variability among and within years (39%) exceeded estimates of variation among farm locations and Þelds (7%). Similarly, time covariates explained the largest amount of variation of aster leafhopper infectivity (50%). Leafhopper abundance has been decreasing since 2001 and reached its minimum in 2010. The average seasonal pattern indicated that periods of above average abundance occurred between 11 June and 1 August. Annual infectivity appears to oscillate around an average value of 2% and seasonal periods of above average infectivity occur between 19 May and 15 July. The coincidence of the expected periods of high leafhopper abundance and infectivity increases our knowledge of when the insect moves into susceptible crop Þelds and when it spreads the pathogen to susceptible crops, representing a seasonal interval during which management of the insect can be focused. KEY WORDS Macrosteles quadrilineatus, aster yellows phytoplasma, aster yellows, insect migration, variance component analysis Aster yellows (AY) is a widespread disease of plants species (Mahr 1989, Christensen et al. 2005). How- caused by the aster yellows phytoplasma (AYp), a ever, the aster leafhopper, Macrosteles quadrilineatus small, wall-less prokaryotic organism that is currently Forbes, is considered to be the most important vector placed in the provisional genus ÔCandidatus Phyto- of the AYp because of its prevalence in susceptible, plasmaÕ (Lee et al. 2000, IRPCM Phytoplasma/Spiro- midwestern crops (Drake and Chapman 1965, Hoy et plasma working team Ð Phytoplasma taxonomy group al. 1992). 2004). The AYp has an extensive and diverse host The AYp is persistently transmitted by the aster range infecting over 350 plant species including many leafhopper and both nymphs and adults can acquire common vegetable, ornamental, and agronomically the pathogen. Once infected, an individual aster leaf- important Þeld crops, and several noncrop plant spe- hopper can remain infective for the remainder of its cies (Kunkel 1926, Chiykowski 1965, Chiykowski and life. The aster leafhopper is a polyphagous insect spe- Chapman 1965, Chiykowski 1967, Westdal and Rich- cies that uses over 300 different plant species for food, ardson 1969, Peterson 1973, Lee et al. 1998, Lee et al. oviposition, and shelter (Wallis 1962, Peterson 1973), 2000, Lee et al. 2003, Hollingsworth et al. 2008). Plant- many of which are susceptible to AYp infection. Aster to-plant spread of AYp in the Þeld generally occurs as leafhopper host plant species can be classiÞed into two a result of transmission by more than 24 leafhopper primary groups based on utilization patterns to in- clude: 1) feeding hosts, or 2) feeding and reproductive hosts. Other factors such as plant community compo- 1 Department of Plant Pathology, University of Wisconsin-Madison, 1630 Linden Drive, Madison, WI 53706. sition (Lee and Robinson 1958, Wallis 1962, Schultz 2 Centro de Investigaciones en Proteccio´n de Cultivos, Universidad 1979), plant physiological state (Peterson 1973), sea- de Costa Rica, San Jose´, Costa Rica. son and geographic location (Lee and Robinson 1958, 3 Pest Pros, Inc., PlainÞeld, WI 54966. Wallis 1962, Peterson 1973) can also affect host pref- 4 Corresponding author: Russell L. Groves, Department of Ento- mology, University of Wisconsin-Madison, 1630 Linden Drive, Mad- erences of aster leafhopper in the Þeld. In Wisconsin, ison, WI 53706 (e-mail: [email protected]). cultivated grains are hosts for overwintering eggs and 0046-225X/13/0477Ð0490$04.00/0 ᭧ 2013 Entomological Society of America 478 ENVIRONMENTAL ENTOMOLOGY Vol. 42, no. 3 also serve as early season feeding and reproductive not known. In turn, many producers avoid risk of hosts for the aster leafhopper (Drake and Chapman pathogen spread by using inexpensive, prophylactic 1965). In addition to grain crops, the aster leafhopper applications of pyrethroid insecticides, a management feeds upon and is moderately abundant in mixed broa- practice that circumvents the utility of the AYI. An dleaf weeds and grasses that border crop Þelds improved understanding the factors that inßuence (Schultz 1979). variation in aster leafhopper abundance and infectiv- Each spring, the aster leafhopper migrates from the ity will further improve aster yellows management. Gulf Coast states to the upper midwest (Chiykowski Environmental processes that drive plant disease and Chapman 1965). The aster leafhopper generally epidemics occur at multiple temporal and spatial migrates in a south to north direction but, in ßight, scales. For example, large (temporal and spatial) scale leafhopper movement is greatly inßuenced by synop- climate patterns may inßuence the risk for fusarium tic weather systems, making it difÞcult to predict when head blight (FHB) development in the midwestern and where the aster leafhopper will arrive. The mi- United States (Kriss et al. 2012). However, smaller gratory behavior together with the mode of pathogen scale weather ßuctuations such as a short-term dry transmission by the aster leafhopper enables the insect period around wheat at anthesis can counteract the to acquire and transmit the pathogen over great dis- overall impact of a generally wet year by reducing the tances. Large numbers of migrating aster leafhoppers number of primary fungal infections leading to re- have been reported to inßuence the potential for AY duced FHB severity (De Wolf et al. 2003, Kriss et al. epidemics in vegetable crops grown in Wisconsin and 2012). Investigating the patterns of aster leafhopper in other midwestern states (Chiykowski 1965, Chi- abundance or infectivity variation across different ykowski and Chapman 1965, Drake and Chapman temporal and spatial scales will provide insight into the 1965, Chapman 1973, Hoy et al. 1992). The severity of processes that drive the variation in annual AY epi- AY outbreaks is thought to be directly related to the demics. For example, if aster leafhopper migration was infectivity and the abundance of aster leafhoppers important for producing variation in the aster leaf- immigrating into a susceptible crop (Chapman 1971). hopper infectivity, then it might be expected that In Wisconsin, AY management has focused primar- interannual variation of aster leafhopper infectivity ily on controlling the insect vector, the aster leafhop- would be high relative to intra-annual variation. In per. The aster yellows index (AYI), was developed as addition, an improved understanding of variation a risk assessment tool to enumerate the maximum across different temporal and spatial scales can also allowable numbers of infectious leafhoppers and de- inform future sampling strategies (Wheatley and Þne periods in the growing season when protection of Johnson 2009). For instance, if interannual variation of a susceptible crop was most needed (Chapman 1971, aster leafhopper infectivity was comparatively large 1973). Simply, the AYI metric is the product of aster relative to intra-annual variation, then repeated sam- leafhopper (relative) abundance and infectivity. In- pling within a season would explain very little about secticide sprays are then recommended if the AYI aster leafhopper infectivity. Unfortunately, experi- exceeds an allowable threshold that is based on the ments that manipulate environmental processes relative susceptibility of the crop to infection by AYp. across multiple spatial and temporal scales (simulta- Originally, the AYI was calculated using an infectivity neously) are difÞcult to perform. Yet, compiled data estimate determined from a series of early season from observational studies that include spatial and (migratory) leafhopper collections and bioassays on temporal information at multiple scales offer an op- susceptible Chinese aster, Callistephus chinensis (L.) portunity to obtain information about the scale at Nees. This infectivity estimate was used for the entire which ecological factors, contributing to abundance growing season, whereas aster leafhopper abundance and infectivity variation, occur (Magnuson 1990, Sa- was determined weekly, or more frequently, for each garin and Pauchard 2010). Þeld throughout the summer (Mahr et al. 1993). Here we present an approach for parsing sources of Following observations that aster leafhopper abun- variation in Poisson-distributed count data, similar to dance and infectivity in and around carrot (Daucus the method described