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Biological Control 47 (2008) 167–171

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Biological Control journal homepage: www.elsevier.com/locate/ybcon

Effect of host-plant genotypes on the performance of three candidate biological control agents of Schinus terebinthifolius in Florida Veronica Manrique a,*, J.P. Cuda b, W.A. Overholt a, D.A. Williams c, G.S. Wheeler d a

Biological Control Research and Containment Laboratory, University of Florida, 2199 South Rock Road, FL 34945, USA Department of Entomology & Nematology, University of Florida, Building 970 Natural Area Drive, Gainesville, FL 32611, USA c Department of Biology, Texas Christian University, 2800 S. University Drive, Fort Worth, TX 76129, USA d USDA-ARS Invasive Plant Research Laboratory, 3225 College Avenue, Fort Lauderdale, FL 33314, USA b

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Article history: Received 23 January 2008 Accepted 15 July 2008 Available online 24 July 2008 Keywords: Host-plant genotypes Biological control Local adaptation Schinus terebinthifolius Episimus utilis Pseudophilothrips ichini

a b s t r a c t Brazilian peppertree, Schinus terebinthifolius Raddi, native to South America, is an invasive weed in Florida, California, Texas, and Hawaii. Genetic studies have recognized two S. terebinthifolius haplotypes (A and B) in Florida, and extensive hybridization has occurred between these two populations. Three candidate biological control agents were identified from the native range (Brazil); a leaflet rolling moth Episimus utilis Zimmerman, a thrips Pseudophilothrips ichini Hood from Ouro Preto, and an unindentified thrips, referred to as Pseudophilothrips sp. near ichini, from Curitiba, Brazil. The objective of this study was to compare the performance of these three candidate agents on different S. terebinthifolius genotypes found in Florida and Brazil. Survival (54%), adult longevity (9 days), fecundity (84 eggs laid), and fertility (68% eggs hatched) of E. utilis were similar on all S. terebinthifolius genotypes tested from Florida. In contrast, the two thrips species differed in their ability to utilize different genotypes of their host plant. Pseudophilothrips sp. near ichini exhibited low survival (0–4%) and short adult longevity (0.90 in a respective cluster and as hybrids if they contained a maximum of q = 0.40 for either western or eastern ancestry. Hybrid individuals were further categorized as having either the A cpDNA haplotype or B haplotype. The cut ends of different S. terebinthifolius plants (10 plants per genotype) from Florida were coated in rooting hormone powder (Schultz TakeRootÒ Rooting Hormone) and planted in pots (18 cm height, 17 cm diameter) using sterilized soil mix (FafardÒ germination mix). Pots were placed in the shade and misted every 10 min. After three months, cuttings with attached roots were transplanted to new pots (18 cm height, 17 cm diameter) containing soil mixture (FafardÒ #3B mix), and all plants were placed in the greenhouse under ambient conditions and watered as needed. Schinus terebinthifolius seeds from Brazil (5 plants per genotype) were collected in Blumenau, Santa Catarina State (haplotype A) and in Curitiba (haplotype D), and grown inside a quarantine greenhouse at the BCRCL. Genetic analyses were conducted on all the plants to confirm their genotypes (Williams et al., 2002, 2005). Schinus molle seedlings were purchased from a Nursery in California, and grown inside a greenhouse at the BCRCL. All plants were fertilized once with 15 g of OsmocoteÒ (a slow release fertilizer 15–9–12, N–K–P), and 400 ml per pot of liquid fertilizer (Miracle GrowÒ 24–8–16) monthly. 2.1. Development of E. utilis on different S. terebinthifolius genotypes To determine the suitability of different S. terebinthifolius genotypes as hosts for E. utilis, groups were confined on the plants and the following life-history parameters were recorded: (1) pupal fresh weight (mg), (2) developmental time to adult (days), (3) percent survival to adult, (4) adult longevity (days), (5) fecundity (total eggs laid), and (6) fertility (percent eggs hatched). The experiments were conducted in an environmental growth chamber (25 ± 2 °C, 60–70% RH, 14 L:10 D photoperiod). Four different S. terebinthifolius genotypes were compared (6–8 replicates per treatment): (1) Florida haplotype B, (2) Florida haplotype A, (3) Florida hybrid A, and (4) Florida hybrid B. Ten neonates of E. utilis were caged on each potted plant inside a clear acrylic cylinder (45 cm height, 15 cm diameter) with six holes (6 cm diameter) and tops covered by a fine mesh to allow air circulation. After 20 days, the cylinders were removed and all plant foliage was removed. Last instars or pupae were placed individually inside plastic vials (29.5 ml Dixie PL1) containing moist filter paper and plant leaflets from the same genotype on which they were reared. Upon adult emergence, individual pairs from each treatment were placed inside wax paper oviposition cages made by stapling together six rectangles of wax paper (19  30 cm) to form a cube. Each cage containing a cotton wick with GatoradeÒ and one S. terebinthifolius leaflet (same plant genotype). The cages were placed inside ZiplocÒ freezer bags and kept in the environmental growth chamber. After all adults had died, the numbers of hatched and unhatched eggs were counted under a dissecting microscope (magnification 25). In a separate experiment, E. utilis larval development and survival to the adult stage were compared on two S. terebinthifolius genotypes: Florida hybrid B, and Brazil haplotype D. The E. utilis colony was originally collected from haplotypes Brazil haplotype D around Curitiba, Brazil. Since E. utilis survived equally well on all the Florida genotypes tested only one type was included in the experiment. Individual neonates were placed inside vials containing moist filter paper and plant leaflets (10 vials for each plant genotype), and a total of 5 replicates per treatment were conducted. Several insect parameters were recorded:

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V. Manrique et al. / Biological Control 47 (2008) 167–171 Table 1 Life-history parameters (means ± SE) of E. utilis on different genotypes of S. terebinthifolius from Florida Host genotype

Survival to adult (%)

Developmental time to adult (days)

Adult longevity (days)

Fecundity (eggs per female)

Fertility (% egg hatched)

Haplotype A Haplotype B Hybrid A Hybrid B F P

55.0 ± 8.8 55.0 ± 9.4 56.2 ± 8.2 48.3 ± 11.9 F3,29 = 0.11 0.93

31.9 ± 0.6 32.0 ± 0.5 31.5 ± 0.3 31.9 ± 0.6 F3,29 = 0.12 0.94

8.4 ± 0.8 8.2 ± 0.7 9.6 ± 1.1 9.5 ± 0.2 F3,23 = 0.89 0.46

53.2 ± 3.6 91.2 ± 30.8 95.0 ± 21.4 98.9 ± 17.0 F3,17 = 0.87 0.47

74.1 ± 9.1 81.1 ± 5.3 81.2 ± 4.9 78.8 ± 5.8 F3,17 = 0.11 0.95

(1) developmental time to adult (days), (2) percent survival to adult, and (3) adult longevity (days). 2.2. Development of two thrips species on different S. terebinthifolius genotypes and on S. molle

formed prior to analysis (Zar, 1999). Means were separated using the Student–Neuman–Keuls (SNK) test (SAS Institute, 1999). A significance level of a = 0.05 was used for all statistical analyses. 3. Results

The experiments described below were conducted separately for the two thrips species inside an environmental growth chamber (28 ± 2 °C, 60–70% RH, 14 L:10 D photoperiod). Seven treatments were established (8 replicates per treatment): (1) Florida haplotype B, (2) Florida haplotype A, (3) Florida hybrid B, (4) Florida hybrid A, (5) Brazil haplotype A, (6) Brazil haplotype D, and (7) S. molle. Ten neonate thrips were placed inside a plastic vial (11 cm height, 5 cm diameter) contained a plant shoot and moist filter paper. Vials were checked every other day, and moisture and food were added as needed. The life-history parameters recorded were: percent survival to adult and developmental time to adult (days). Preliminary laboratory studies confirmed that the two thrips species survived as well on excised shoots as on rooted plants. In a separate experiment, adult longevity of each thrips species was measured on the same host plants mentioned above and in vials with no food (controls). Ten newly emerged adults (5 females:5 males) of P. sp. near ichini, reared from S. molle or P. ichni, reared from S. terebinthifolius Brazil haplotype A, were placed in each vial containing a plant shoot and moist filter paper. There were 7–8 replicates per treatment. Vials were checked every other day, and survival and pre-oviposition period was recorded. Experiments were terminated when all adults had died.

3.1. Development of E. utilis on different S. terebinthifolius genotypes No differences were detected for survival, developmental time, adult longevity, fecundity or fertility of E. utilis reared on different Florida S. terebinthifolius genotypes (Table 1). In addition, pupal weight did not differ between plant genotypes, but female pupae (18.2 ± 0.8 mg) were larger than male pupae (16.9 ± 0.5 mg) (genotypes: F3,59 = 2.11, P = 0.11; sex: F1,59 = 5.48, P = 0.02; genotype  sex: F3,59 = 0.3, P = 0.8). No differences were detected for survival to adult, developmental time to adult, or adult longevity when E. utilis was reared in vials on either Florida hybrid B or Brazilian haplotype D (Table 2). 3.2. Development of two thrips species on different S. terebinthifolius genotypes and on S. molle Survival of P. sp. near ichini to the adult stage was highest on S. molle, followed by Brazil haplotype D and Brazil haplotype A (Table 3). Survival was low on all S. terebinthifolius Florida genotypes tested (