The potato leafhopper, Empoasca fabae (Harris) (Hemiptera: Cicadellidae), overwinters in states along the Gulf of Mexico on evergreens (Pinaceae) and herbaceous vegetation (mostly Fabaceae), and then migrates north in spring (Medler 1957, Sidumo et al. 2005, Taylor et al. 1993, Taylor and Shields 1995). The first appearance of E. fabae in the midwestern United States occurs in late April or mid-May (Maredia et al. 1998, Medler 1957). Arrival of E. fabae in these areas coincides with low-pressure weather systems, suggesting transport is passive on warm low-level jet streams (Carlson et al. 1992). In Pennsylvania, early-spring migrant E. fabae populations were nearly 80% fertile females that began ovipositing upon arrival in alfalfa fields (Flinn et al. 1990).

Empoasca fabae is a key pest of alfalfa (Medicago sativa L.) (Fabaceae) in the midwestern United States and usually begins to arrive in Iowa in late April, but peak arrival is not until mid- to late May (Medler 1957; L.W.E., pers. obs.). Although E. fabae are found in alfalfa at this time, populations do not reach damaging levels in alfalfa fields until after the first cutting (mid-May to early June) (DeGooyer et al. 1998a, Giles et al. 1999, Steffey and Armbrust 1991). The life cycle of E. fabae requires approximately 350 degree days (°C) to complete development from egg to adult (Flinn et al. 1986). Consequently, the period from peak arrival in early to mid-May until harvest in late May is insufficient time for eggs laid by migrating E. fabae to complete development into adults in alfalfa. Because alfalfa is a disturbed habitat due to several harvests each year, E. fabae may be viewed as a cyclic colonizer (sensu Wissinger 1997). Each harvest of alfalfa creates a temporary unsuitable habitat for E. fabae, which then moves out of alfalfa to alternate hosts and may return once alfalfa has begun to regrow. Empoasca fabae feeds on over 200 host species in 100 genera and 26 families, all in the class Magnoliopsida (Hogg and Hoffman 1989, Lamp et al. 1994), thus many plant species could be used by E. fabae before returning to alfalfa. Sixty-two percent of these host plants belong to the family Fabaceae (Lamp et al. 1994). Recolonization of alfalfa after harvest by E. fabae initially occurs on the edges of the field with subsequent movement to the interior (Emmen et al. 2004, Flinn et al. 1990). In Illinois, E. fabae uses plant hosts in woodlands, orchards, and roadsides near alfalfa fields for feeding and reproduction in early spring (Lamp et al. 1989). Poos (1935) and Lamp et al. (1989) have suggested that E. fabae builds up populations on these hosts in early spring and then moves into alfalfa, but movement into alfalfa from these hosts has not been demonstrated. The objective of this study was to determine if E. fabae adults are colonizing Iowa alfalfa fields from adjacent nonagricultural habitat in early spring.

Materials and Methods

In 1998 and 1999, four Iowa State University alfalfa fields in Ames, IA (42°2′ N, 93°48′ W) (Ross farm [Field 1] and Applied Science Complex [ASC; Field 2]) in 1998, Beef Cattle Nutrition Management Research Center [Field 3] and ASC [Field 4] in 1999) were sampled from mid-April until late May (first alfalfa harvest). These fields were approximately 3.5 km from each other. In each of the fields, the trees and shrubs from 3 to 50 m from the edge of the field were surveyed as potential hosts of E. fabae (Table 1). Because several species of Empoasca are very similar morphologically and only distinguishable by genitalia (Chasen et al. 2014, DeLong 1931), Empoasca species were not determined outside of alfalfa because we used sticky cards, which can result in specimens that cannot be identified to species using genitalia. We did, however, identify Empoasca under a dissecting microscope using characteristics given by Fenton and Hartzell (1923). Leafhoppers in these edge plant habitats were monitored weekly by hanging one yellow sticky trap (Pherocon AM®, Adair, OK) from a branch approximately 2 m from the ground. Sticky traps were replaced weekly and the number of Empoasca spp. adults was counted. Tree and shrub species were monitored using sticky traps for Empoasca spp. activity until first alfalfa harvest in 1998 (20 May) and until the second harvest in 1999 (11 July and 18 July). To monitor the movement of E. fabae into alfalfa fields, sticky traps were placed within the alfalfa at the edge of the field (closest to tree/shrub line), 20 m from the edge, and 40 m from the edge. Sticky traps were placed horizontally at the top of the alfalfa canopy to maximize the number of E. fabae collected (DeGooyer et al. 1998b). There were four replicates at each distance and traps in each replicate were placed 25 m apart. Sticky traps were replaced weekly and the number of E. fabae adults recorded. Data were analyzed using repeated measures analysis of variance; factors examined were date and location within alfalfa field (SAS Institute 1998). Weather data were collected (www.wunderground.com) to determine degree-day accumulation during the study period. To calculate degree days, a minimum developmental threshold for E. fabae of 8.8°C was used (Simonet and Pienkowski 1980).

Table 1 List of tree species samples for Empoasca spp. in spring 1998 and 1999 adjacent to alfalfa fields in Ames, IA.

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Results

Empoasca spp. were primarily observed on sticky traps placed in field-margin trees and shrubs in Ames, IA, during the last week of April in 1998 and 1999. Leafhoppers were first found on sticky traps on Celtis occidentalis L. and Prunus sp. on 19 April 1998 and on Gleditsia triacanthos L. and Quercus rubra L. on 30 April 1999 (Tables 1, 2). However, in alfalfa fields peak numbers of adults were observed on the sticky traps during the second (1998) or third (1999) week of May (Figs. 1, 2). In 1998 at Field 1 there were similar numbers of E. fabae at the three locations within the alfalfa field on each sampling date (F = 2.88; df = 2, 9; P = 0.08; F = 1.32; df = 2, 9; P = 0.29; F = 0.29; df = 2, 9; P = 0.75; F = 0.60; df = 2, 9; P = 0.56) (Fig. 1A). However, there were significant differences in the distribution of E. fabae in the alfalfa field at Field 2 on all dates (F = 5.56; df = 2, 9; P = 0.02; F = 3.29; df = 2, 9; P = 0.08 [t = 2.26; df = 2, 9; P < 0.05]; F = 10.33; df = 2, 9; P = 0.005) except 28 April (F = 1.40; df = 2, 9; P = 0.30). The number of E. fabae sampled closest to the edge of Field 2 near the tree line was higher than at 40 m inside the field (Fig. 1B).

Table 2 Mean ± SEM number of Empoasca spp. on sticky traps hung on tree and shrub species adjacent to alfalfa field in 1998 at Sites 1 and 2.

* Number of sticky traps.

† No samples taken from Site 1 on 19 April.

‡ Tree not present at site.

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In 1999 at Field 3, higher numbers of E. fabae were found at the edge than at 40 m inside the alfalfa field on 7 May (F = 10.92; df = 2, 9; P = 0.004); there were no significant differences in numbers at any of the other dates sampled (Fig. 2A). Similarly, there were significantly fewer E. fabae observed at 40 m compared with the edge and 20 m inside of Field 4 on 7 May (F = 4.25; df = 2, 9; P = 0.046) (Fig. 2B).

The number of Empoasca spp. found on the sticky traps placed in the trees and shrubs was not statistically different among tree and shrub species in either 1998 or 1999 at any of the locations (P > 0.05) (Tables 2, 3). The number of Empoasca spp. found on the sticky traps hanging from these plant species indicated that peak activity in these natural border areas occurred during the second week of May. In 1998, we sampled 10 times more Empoasca spp. on sticky traps hung in trees and shrubs at Site 1 than from Site 2 (Table 2). Similar numbers of Empoasca spp. were collected from sticky traps hung among trees and shrubs in Sites 3 and 4. In 1999, the numbers of Empoasca spp. collected on sticky traps in the adjacent trees and shrubs increased when the alfalfa field was harvested (Table 3).

Table 3 Mean ± SEM number of Empoasca spp. on sticky traps hung on tree and shrub species adjacent to alfalfa field 1999 at Sites 3 and 4.

* Number of sticky traps.

† Tree not present at site.

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Table 3 Extended.

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Discussion

In this study, we sampled Empoasca spp. adults from vegetation bordering alfalfa fields and E. fabae within the alfalfa fields to determine if E. fabae adults colonize alfalfa by movement out of adjacent nonagricultural habitat in early spring. We assume that the adult Empoasca collected from sticky traps placed in alfalfa fields are E. fabae based on previous studies (DeGooyer et al. 1998b, Lamp et al. 1989). We did not identify the adult Empoasca spp. collected in the surrounding habitats to species due to the use of weekly sampling of sticky traps. During early spring, more E. fabae were present on sticky traps in the edges of alfalfa fields closest to the trees and shrubs in Fields 2, 3, and 4 during the first week of May (1998 and 1999). Additionally, there were more E. fabae collected from alfalfa near the edge of Field 2 during the second and third weeks of May (1998). These results are consistent with previous studies that examined edge colonization of E. fabae in alfalfa (Emmen et al. 2004, Flinn et al. 1990). Bentz and Townsend (2004) also found that potato leafhoppers tended to aggregate on habitat edges in early spring. In addition, edge colonization behavior of E. fabae has been demonstrated in soybean fields after an alfalfa harvest (Poston and Pedigo 1975). Given these dispersion patterns, it seems unlikely that E. fabae colonization of alfalfa fields in early spring happens by random deposition from their northerly migration. It appears as though E. fabae are moving into alfalfa from another source. Our study indicates that these leafhoppers are aggregating on the edge of alfalfa after depositing eggs in alternate hosts within adjacent woody habitats.

From first arrival of leafhoppers in Iowa until first harvest in 1998 and 1999 we determined that 233 and 148 degree days accumulated above the developmental threshold of 8.8°C, respectively. Because the life cycle of E. fabae requires approximately 350 degree days (°C) to complete development from the egg to adult (Flinn et al. 1986), it would not be possible for E. fabae to reproductively increase population numbers in the alfalfa before first harvest. Eggs laid inside alfalfa stems are removed from the field when the alfalfa is harvested. Due to low vagility of the nymphs, they would not find suitable hosts and, therefore, up to 95% of nymphs are killed when the field is harvested (Simonet and Pienkowski 1979). It appears that reproduction in alfalfa fields during early spring is, for the most part, a waste of reproductive effort because only the few eggs that were laid in late April will develop into adults. Typically, E. fabae may occur in damaging numbers during the second growth of alfalfa (Giles et al. 1999). Because E. fabae cannot complete a generation in alfalfa before the first harvest, E. fabae infesting second-growth alfalfa must be from other sources.

Empoasca fabae feeds and oviposits on the new growth of woody species, such as Quercus, Acer, and Carya (Bentz and Townsend 1999, Lamp et al. 1994, Poos 1935). Although we found leafhoppers on the sticky traps hanging on several of these woody species (Tables 2, 3), we did not confirm that the leafhoppers were laying eggs in these hosts during this time. In early May during alfalfa harvest in Illinois, Lamp et al. (1989) found more E. fabae in adjacent Quercus and Acer trees than in alfalfa fields. In contrast, we did not find a higher number of Empoasca spp. per sticky trap in the trees than in the alfalfa fields during this study. This difference may be due to the method of collection; Lamp et al. (1989) swept tree foliage to obtain E. fabae, whereas we used hanging sticky traps. However, the numbers of Empoasca spp. in our late-April and early-May samples from trees were comparable with the numbers of E. fabae collected on sticky traps on Acer rubrum L. clones in Maryland during the same time of year (Bentz and Townsend 1997). In addition, we found increased activity of Empoasca spp. on sticky traps in the adjacent tree and shrub species when an adjacent alfalfa field was harvested. This increased activity remained elevated for at least 2 weeks (Table 3) suggesting that E. fabae may be using the adjacent woodland as a refuge habitat. This is consistent with the hypothesis of Poos (1935), who collected E. fabae from light traps from North Carolina to New York and suggested that E. fabae used Quercus and Carya trees when alfalfa is unavailable.

Sources of E. fabae infestation of the second alfalfa growth require further investigation. It is possible that E. fabae may still be arriving from overwintering sites in early June as the length of the spring migration has not been determined. Although there are no distinguishable morphological characteristics between migrant versus resident E. fabae, molecular analyses could be used to determine the host plants of E. fabae and, therefore, determine status (resident versus migrant) of E. fabae adults in second-growth alfalfa (Taylor et al. 1993, Wassenaar and Hobson 1998). For example, Wassenaar and Hobson (1998) traced the origins of migratory Danaus plexippus L. (Lepidoptera: Danaidae) using the composition of stable-hydrogen and carbon isotopes found in its food source, which varies along a north–south continuum.

This study does not exclude the possibility of two distinct populations of E. fabae, one on woody species (i.e., trees and shrubs) and a second on herbaceous species (i.e., alfalfa and other legumes). This type of host segregation is found in pea aphids (Acyrthosiphon pisum [Harris]) (Hemiptera: Aphididae), where specialization occurs on alfalfa and red clover (Trifolium pratense L.) (Fabaceae) (Via 1991). Lamp et al. (1989) found E. fabae within grass, clover, and roadside weeds early in the season and suggested that these may serve as a source or sink for dispersing E. fabae. In Iowa, E. fabae may be using unharvested alfalfa or other herbaceous plants to feed and reproduce in early spring. These plants are not cut and E. fabae would have sufficient time to produce a new generation. Further studies examining E. fabae eggs deposited in these habitats in addition to woody trees adjacent to alfalfa fields in early spring may shed light on the source of E. fabae population buildup and subsequent infestation of second-growth alfalfa.