Potential Sources of Frankliniella spp. (Thysanoptera: Thripidae) in Iowa 1

Potential Sources of Frankliniella spp. (Thysanoptera: Thripidae) in Iowa 1 Bethzayda Matos and John J. Obrycki 2 Department of Entomology, Iowa State University, Ames, Iowa 50011 USA J. Agric. Urban Entomol. 21(1): 1 8 (January 2004) ABSTRACT In Iowa, two possible sources of phytophagous Frankliniella spp. infesting strawberry fields in spring are individuals that overwinter in fields or migrate into fields. In April 2001 and March 2002, soil samples taken to a depth of 5 cm from three strawberry fields in central Iowa were dried in Berlese funnels to determine whether thrips overwintered in these strawberry fields. In 2001, one Frankliniella spp. second instar was collected from 39 soil samples; in 2002, five Frankliniella occidentalis (Pergande) adults were collected from 72 samples. To determine whether thrips were flying into fields, 13 yellow and 13 blue sticky cards (8 13 cm) were placed in each of three strawberry fields in central Iowa from April to June 2001 and from March to June 2002. Thrips were first captured on sticky cards during the third week of April 2001 and 2002. In 2001, yellow sticky cards caught significantly higher numbers of thrips in strawberry fields compared with blue sticky cards, whereas in 2002, more thrips were captured on blue sticky cards. On the basis of this field study, we conclude that F. occidentalis overwinters in relatively low numbers in the soil in Iowa strawberry fields. Frankliniella tritici (Fitch) was the most common thrips found on the sticky cards during both years. Pest managers may use sticky cards to monitor early colonization of strawberry fields by F. tritici before flowers start appearing. KEY WORDS Frankliniella tritici, Frankliniella occidentalis, overwintering, migration, strawberry, thrips, sticky cards The presumed annual migration of Frankliniella spp. (Thysanoptera: Thripidae) from southern latitudes has been examined by several researchers who sampled for overwintering thrips in northern latitudes (greater than 40 N; Post & Thomasson 1966, North & Shelton 1986b, Felland et al. 1993, Broadbent & Hunt 1991). A spring migration of Frankliniella tritici (Fitch) from southern states (Louisiana, Mississippi, and Arkansas) was proposed by Stannard (1968) because F. tritici had not been observed to overwinter in Illinois. The collection of F. tritici in aerial samples at altitudes of 3048 m over Louisiana supported the concept of long-distance movement of this species (Glick 1939). In New York, North & Shelton (1986b) collected thrips from November to April from selected vegetation and soil samples. Frankliniella tritici adults only were found in No- 1 Accepted for publication 2 June 2004. 2 Department of Entomology, University of Kentucky, Lexington, Kentucky 40546 USA. 1 Prod. #A01

2 J. Agric. Urban Entomol. Vol. 21, No. 1 (2004) vember and April. Thus, they concluded that F. tritici migrates to northern latitudes in the spring and does not overwinter in Ontario County, New York (42.85 N). In contrast, on the basis of 180 sod samples taken in both fall and spring, Post & Thomasson (1966) estimated that 20% of F. tritici survived in roadside sod in North Dakota (45.55 N). In Ontario, Canada, Frankliniella occidentalis (Pergande) is a major pest in greenhouse and vegetable crops (Broadbent el al. 1987); therefore, Broadbent & Hunt (1991) investigated the overwintering of F. occidentalis at this latitude (42 N). On the basis of collections from chrysanthemums grown outdoors, they reported that laboratory-reared and field-collected F. occidentalis did not overwinter in Ontario. Farther south, Felland et al. (1993) recovered fourteen adult F. occidentalis from soil emergence traps in Pennsylvania (34 N) in May. This was the first report of successful overwintering of F. occidentalis in the northeastern United States. In the southeastern United States, F. occidentalis overwinters in soil, whole plants, and shoots of several plant species (Chamberlin et al. 1992, Cho et al. 1995b). Frankliniella tritici has been found on 41 plant species in Georgia and Florida during the winter and spring (Chamberlin et al. 1992). Several sampling techniques have been used to quantify thrips occurrence and densities in fields and greenhouses, e.g., water traps (Felland et al. 1993, Williams et al. 1999), tapping of flowers (Gonzalez-Zamora & Garcia-Mari 2003), sticky cards (Gillespie & Vernon 1990, Felland et al. 1993, Williams et al. 1999), and plastic pipe soil emergence traps (Felland et al. 1993). In rye fields, yellow sticky cards were more attractive to F. tritici compared with red, black, and white sticky cards (Walker 1974). In a greenhouse study, the numbers of F. occidentalis collected by blue, violet, yellow, and white sticky cards were similar (Gillespie & Vernon 1990). The objectives of this study were to determine whether thrips overwinter in soil in central Iowa strawberry fields and/or immigrate into fields in the spring. In addition, we compared the numbers of thrips captured by blue and yellow sticky cards in strawberry fields. Materials and Methods Soils samples. In 2001, six soil samples were taken within 1mofthefields edges, and six samples were taken from the central area (10 to 15 m from the edge) from each of three fields on 10 April (Table 1). After removing the straw mulch covering the area, soil was collected using a hand trowel. Soil was removed to a depth of 5 cm from a 20 cm diameter area for each sample (Deligeorgidis & Ipsilandis 2004). Wet weight of soil samples averaged 742 ± 140 g (mean ± SD; n 36). Soil samples were dried for 7dinBerlese funnels (Southwood 1978) and thrips were collected in 70% alcohol. Although there might be additional overwintering sites for thrips (Chamberlin et al. 1992, Cho et al. 1995b), we chose to focus on soil because of the protective layer of straw mulch present in Iowa strawberry fields. On 18 March 2002, we collected 72 soil samples from the same strawberry fields using the same methodology as in 2001. Wet weight of soil samples averaged 563.4 ± 52.4 g (mean ± SD; n 72). Thrips on sticky cards. We placed 13 yellow and 13 blue (#100SSB35, Great Lakes IPM, Inc., Vestaburg, Michigan) sticky cards (8 13 cm), oriented

MATOS and OBRYCKI: Sources of Thrips 3 Table 1. Locations, sizes, and characteristics of three strawberry farms where thrips were collected in central Iowa, 2001 and 2002. Site/location Size No. of rows Cultivar Age of planting Horticultural farm (No. 1) Gilbert Turtle farm (No. 2) Granger Berry patch (No. 3) Nevada 48 34 m 10 a /25 rows Honeoye Third year 60 30 m 30 rows Jewel, Northeaster, Delmarvel, Winona 60 33 m 30 rows Honeoye, Jewel, Northeaster, Winona Third year Fifth year a Ten rows were sampled the first year. In the second year, 25 rows were sampled. vertically at a height of 20 cm, at the three farms on 10 April 2001. Individual yellow and blue sticky cards were placed back to back at each location. The orientation (N, S, E, and W) of blue and yellow sticky cards was randomly determined. Six to eight paired sticky cards were placed within 1 m of the edge of the field. Five to seven pairs were placed in the central portion of the fields (10 and 20 m from the edge). The vertically oriented sticky cards were changed weekly, except for cards placed in the field on 26 April, which remained in the field until 7 May. The straw mulch was removed from the strawberry fields between 9 and 19 April. The last sticky cards were removed on 18 June, because the strawberry harvest in all fields was nearly completed. To determine whether thrips were present in the fields later in the season, we placed six sticky cards (four on the edges of the field and two in the center of the field) at Farm 1 on 8 and 14 August 2001. Sticky cards were examined using a stereomicroscope at 30X magnification for Frankliniella species. Frankliniella tritici was identified from the sticky cards using a dichotomous key (Mound & Kibby 1998). On several occasions, thrips with different morphological characteristics appeared on the sticky cards, but these were not counted as Frankliniella spp. The same methodology was used with sticky cards at the same three strawberry fields in 2002, except we sampled for two additional weeks. Each year, thrips collected from the soil samples were sent to Steve Nakahara, at the USDA-Agricultural Research Service Systematics Entomology Laboratory (USDA-ARS-SEL) for identification. In addition, in 2002, 62 specimens from sticky cards, randomly chosen to represent individuals collected on each sampling date and farm, were mounted in Hoyer s medium and submitted for identification. Voucher specimens have been deposited in the Iowa State University Insect Collection, Ames, Iowa. Data analysis. We used a paired t test to determine whether the number of thrips caught on the sticky cards (yellow and blue) were different from each other for each farm for the whole season (PROC UNIVARIATE, SAS Institute 1998). Data from each year were analyzed separately.

4 J. Agric. Urban Entomol. Vol. 21, No. 1 (2004) Results Soil samples. One second instar Frankliniella spp. was found in the 39 soil samples collected in 2001. In 2002, 5 adult F. occidentalis were collected from the 72 soil samples. Thrips on sticky cards. In 2001, the most abundant thrips species observed on sticky cards was F. tritici. From 10 to 19 April, an average of 0.01 F. tritici adults and larvae per trap per day was captured at Farm 2, on both yellow and blue sticky cards. On 7 May, the number of Frankliniella spp. on both yellow and blue cards increased at each farm (Table 2). On 21 May, Frankliniella spp. larvae were observed on yellow and blue sticky cards in Farm 2, indicating some wind dispersal of wingless larval stages. However, fewer than 10 immature Frankliniella spp. were found on sticky cards on all other sampling dates; thus, 99% of the 11,427 Frankliniella spp. found on sticky cards were adults. The highest number of thrips captured (mean 17.01 thrips per trap per day) in 2001 was observed on 13 June at Farm 1 on yellow sticky cards (Table 2). The number of Frankliniella spp. was significantly different between yellow and blue sticky cards for the three farms (P<0.0001). In samples after 14 May, the number of thrips on yellow cards was 2 to 11 times higher than captures on blue sticky cards (Table 2). During August, 13 thrips were caught on yellow sticky cards and 2 thrips were caught on blue sticky cards (Table 2). In 2002, 53 of the 62 specimens sent to the USDA-ARS-SEL for identification were F. tritici; none of the thrips were F. occidentalis. Thrips started to appear on the sticky cards at Farm 2 on 15 April (Table 3). The remaining nine individuals were Frankliniella tenuicornis (Uzel) (n 1), Frankliniella fusca (Hinds) (n 4), Frankliniella exigua (Hood) (n 1), Thrips trehernei (Priesner) (n 1), and Thrips tabaci Lindenman (n 2). Throughout the 2002 season, numbers of thrips on blue sticky cards were higher than on yellow sticky cards at two of the three farms (P 0.0005). Collection of immature thrips was sporadic; only one or two immature stages were captured on any given sampling date. Discussion More thrips were collected in 2001 (11,427) compared with 2002 (4,173), even though we sampled for an additional 2 weeks in 2002. Peak populations were observed at the end of May and early June in both years. Precipitation in May and June during both years was similar. Strawberry flowers were present at all farms during this period. Even though F. occidentalis overwintered in strawberry fields, it was not collected from sticky cards in 2001 and 2002. In a related study conducted in the same fields from 2000 to 2002, F. tritici accounted for 99% of thrips species collected from strawberry flowers and fruits (Matos 2001). The source or sources of F. tritici that migrate into strawberry fields from April to June are known. One of the first crops to flower in Iowa in early May is June-bearing strawberries, which may be highly attractive to thrips flying from their overwintering sites. Previously, North & Shelton (1986a) reported movement of F. tritici from forage fields to cabbage fields when the forage crops were harvested.

MATOS and OBRYCKI: Sources of Thrips 5 Table 2. Number of thrips (adults and larvae) attracted to yellow (Y) and blue (B) sticky cards placed in three strawberry farms in central Iowa, 2001 (thrips per trap per day, mean ± SE). Collection date a Card color b Farm 1 Farm 2 Farm 3 10-Apr Y 0 B 19-Apr Y 0 0.01 ± 0.01 0 B 0 0.01 ± 0.01 0 26-Apr Y 0 0 0 7-May Y 0.27 ± 0.08 0.65 ± 0.14 0.99 ± 0.16 B 0.04 ± 0.02 0.23 ± 0.07 0.33 ± 0.11 14-May Y 3.15 ± 0.67 1.49 ± 0.46 4.48 ± 1.15 B 0.41 ± 0.12 0.67 ± 0.12 1.48 ± 0.25 21-May Y 11.0 ± 1.75 5.52 ± 1.34 7.09 ± 1.88 B 0.87 ± 0.19 0.80 ± 0.26 1.59 ± 0.40 29-May Y 2.53 ± 0.44 3.64 ± 0.62 1.30 ± 0.34 B 0.89 ± 0.26 2.15 ± 0.49 0.55 ± 0.19 4-Jun Y 3.84 ± 0.77 5.95 ± 1.09 1.37 ± 0.38 B 1.64 ± 0.36 2.70 ± 0.63 0.52 ± 0.13 13-Jun Y 17.0 ± 3.90 7.89 ± 1.45 6.26 ± 1.22 B 4.91 ± 1.14 3.73 ± 0.73 1.56 ± 0.42 18-Jun Y 10.29 ± 3.12 2.66 ± 0.83 2.86 ± 1.00 B 1.55 ± 0.43 0.25 ± 0.11 0.79 ± 0.42 14-Aug c Y 0.31 ± 0.18 B 0.05 ± 0.03 21-Aug Y 0.31 ± 0.09 B 0 a On each sample date, 13 sticky cards of each color were placed at each farm. b Y, yellow; B, blue. c Six cards of each color were placed at Farm 1 only. Understanding the overwintering biology of insect pests is important for predictions of their occurrence and abundance the next season (Tauber et al. 1986). The size of a pest population that enters the overwintering stage may be used to predict the size of the spring population (Leather et al. 1993). In our study, F. occidentalis overwintered in the strawberry fields, but only F. tritici was collected from strawberry flowers and fruits (Matos 2001) and sticky cards. The recovery of five adult F. occidentalis from the soil samples in Iowa strawberry fields is the first record of F. occidentalis overwintering in the midwestern United States. No greenhouses were located within 2 km of our field sites, reducing the possibility that these individuals were from greenhouse populations that colonized the fields in early spring. The single, second instar Frankliniella spp. and five adult F. occidentalis recovered from the soil samples indicates a rela-

6 J. Agric. Urban Entomol. Vol. 21, No. 1 (2004) Table 3. Number of thrips (adults and larvae) attracted to yellow (Y) and blue (B) sticky cards placed in three strawberry farms in central Iowa, 2002 (thrips per trap per day, mean ± SE). Collection date a Card color b Farm 1 Farm 2 Farm 3 25-Mar Y 0 0 0 1-Apr Y 0 0 0 8-Apr Y 0 0 0 15-Apr Y 0 0.01 ± 0.01 0 22-Apr Y 0.01 ± 0.01 0 0.01 ± 0.01 29-Apr Y 0 0.07 ± 0.03 0.01 ± 0.01 B 0.01 ± 0.01 0 0 6-May Y 0.04 ± 0.02 0.05 ± 0.03 0.05 ± 0.03 B 0.08 ± 0.03 0.10 ± 0.04 0.09 ± 0.02 13-May Y 0.07 ± 0.03 0.04 ± 0.02 0.08 ± 0.03 B 0.15 ± 0.07 0.01 ± 0.01 0.18 ± 0.07 20-May Y 0.19 ± 0.05 0.27 ± 0.12 0.10 ± 0.04 B 0.21 ± 0.06 0.11 ± 0.03 0.05 ± 0.02 27-May Y 0.97 ± 0.25 0.37 ± 0.08 0.25 ± 0.09 B 1.24 ± 0.20 0.91 ± 0.33 0.44 ± 0.10 3-Jun Y 1.45 ± 0.25 2.70 ± 0.64 0.89 ± 0.18 B 1.29 ± 0.27 2.82 ± 0.63 1.32 ± 0.24 10-Jun Y 3.85 ± 1.02 2.23 ± 0.63 1.30 ± 0.22 B 4.19 ± 0.89 3.55 ± 0.67 1.37 ± 0.27 17-Jun Y 6.64 ± 0.98 3.90 ± 0.82 3.07 ± 1.19 B 6.62 ± 0.91 4.44 ± 0.76 3.48 ± 0.75 24-Jun Y 3.98 ± 0.44 0.89 ± 0.22 1.37 ± 0.46 B 5.92 ± 1.00 1.05 ± 0.35 4.62 ± 1.18 1-Jul Y 4.07 ± 0.54 1.01 ± 0.24 5.13 ± 1.61 B 7.36 ± 1.57 2.05 ± 0.44 14.87 ± 7.04 a On each sample date, 13 sticky cards of each color were placed at each farm. b Y, yellow; B, blue. tively low occurrence of thrips overwintering in Iowa strawberry fields. However, sampling over multiple dates and from several substrates (crowns, plant tissues, straw mulch) may provide additional information about the overwintering biology of F. occidentalis. Sampling from a soil depth of 5 cm was appropriate. Deligeorgidis & Ipsilandis (2004) found thrips more often in the first 2 cm of soil, whereas no thrips were found below 8 cm. Gerdes (1982) found overwintering Frankliniella spp. within the top 5 cm of soil from northeast Illinois prairies.

MATOS and OBRYCKI: Sources of Thrips 7 High overwintering mortality rates would influence the collection of individuals in the samples in this study (Felland et al. 1995, Kirk 1997). In North Dakota, 80% mortality of F. tritici overwintering in turf was estimated from 180 sod samples taken in the fall and spring (Post & Thomasson 1966). In New York, North & Shelton (1986b) collected thrips species from vegetation and soil samples from November to April, but no F. tritici were recovered from December to March. After mid-may in 2001, we observed 2 to 11 times more thrips on yellow sticky cards than on blue cards. These results are similar to those of Walker (1974), who reported that F. tritici was attracted to yellow sticky cards in rye fields. However, in 2002, numbers observed on blue and yellow sticky cards were similar on all sampling dates, except on 24 June at Farms 1 and 3, when thrips numbers were from two to four times higher on blue sticky cards. Blue sticky cards were most attractive to F. occidentalis in greenhouses (Gillespie & Vernon 1990) but we observed no F. occidentalis on sticky cards in our strawberry fields. More F. tritici were captured on yellow and white sticky cards compared with blue sticky cards when traps were placed near tomato flowers (Cho et al. 1995a). The observed yearly variation in captures of F. tritici by yellow and blue sticky cards may be related to the densities of thrips in the strawberry fields. Even though F. occidentalis overwintered in soils collected in strawberry fields it was not collected in Iowa strawberry flowers (Matos 2001) or on sticky cards. The sticky card samples indicate early season colonization of strawberry fields by F. tritici. Pest managers may use this sampling tool to determine whether thrips are present. Despite the presumed relationship between thrips infestations and bronzing of strawberry fruits, high densities of thrips (up to 48 thrips per flower) caused less than 1% damage of strawberries in the fields (Matos 2001). Acknowledgments The authors thank Angela Tedesco, owner of the Turtlefarm, Granger, Iowa, and Dean Henry, owner of the Berry Patch, Nevada, Iowa, for their collaboration during this 2-year study. Steve Nakahara, U.S. Department of Agriculture, Beltsville, Maryland, identified the thrips specimens. Thanks to Dr. Royce Bitzer, Karini Encarnacion, and Wilma I. Pillot for their technical assistance and Justin Recknor and Rhonda DeCook for statistical assistance. Research was partially supported by a grant from the Leopold Center for Sustainable Agriculture. The Iowa State University Graduate College Minority Assistantship Program and College of Agriculture provided a graduate research assistantship for the senior author. References Cited Broadbent, A. B., W. R. Allen & R. G. Foottit. 1987. The association of Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) with greenhouse crops and the tomato spotted wilt virus in Ontario. Can. Entomol. 119: 501 503. Broadbent, A. B. & D. W. A. Hunt. 1991. Inability of western flower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), to overwinter in Southern Ontario. Proc. Ent. Soc. Ont. 122: 47 49. Chamberlin, J. R., J. W. Todd, R. J. Beshear, A. K. Culbreath & J. W. Demski. 1992. Overwintering hosts and wingform of thrips, Frankliniella spp., in Georgia (Thysanoptera: Thripidae): implications for management of spotted wilt disease. Environ. Entomol. 21: 121 128. Cho, K., C. S. Eckel, J. F. Walgenbach & G. G. Kennedy. 1995a. Comparison of colored sticky cards for monitoring thrips populations (Thysanoptera: Thripidae) in staked tomato fields. J. Entomol. Sci. 30: 176 190.

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