Effect of the Biological Control Agent Neoseiulus Californicus (Acari: Phytoseiidae) on Arthropod Community Structure in North Florida Strawberry Fields

436 Florida Entomologist 91(3) September 2008

EFFECT OF THE BIOLOGICAL CONTROL AGENT NEOSEIULUS CALIFORNICUS (ACARI: PHYTOSEIIDAE) ON ARTHROPOD COMMUNITY STRUCTURE IN NORTH FLORIDA STRAWBERRY FIELDS

AIMEE B. FRAULO1, ROBERT MCSORLEY2 AND OSCAR E. LIBURD2 1MacArthur Agro-Ecology Research Center, 300 Buck Island Ranch Rd., Lake Placid, FL 33852

2Entomology & Nematology Department, University of Florida, Gainesville, FL 33852

ABSTRACT

Field experiments were conducted during the 2006-2007 growing season to determine the effect of the predatory mite, Neoseiulus californicus (McGregor) on arthropod community structure when released as a biological control agent for the twospotted spider mite, Tet- ranychus urticae Koch, in north Florida strawberries (Fragaria × ananassa Duchesne). Re- leases of N. californicus were conducted at approximately 1-month intervals from Dec 2006 to Feb 2007 to compare effects of predator release times on arthropod community structure. Evaluations of community structure were conducted 3 times during the growing season. The Shannon-Weaver index of diversity was used to quantify differences among release and non- release plots. Our results indicate that the release of N. californicus does not affect the arthropod diversity in the strawberry system studied. The generalist feeding behavior of N. californicus, coupled with a high level of richness and diversity in the strawberry ecosystem, may diffuse the measurable effect of N. californicus releases on the arthropod community structure. This makes N. californicus a desirable biological control agent for management of twospotted spider mite in strawberries while preserving arthropod diversity.

Key Words: biological control, arthropod assemblage, strawberry ecosystem, twospotted spider mite, pest management

RESUMEN

Experimentos de campo fueron establecidos para determinar el efecto del acaro predador, Neoseiulus californicus (McGregor), en la estructura de las comunidad de artrópodos cuando es liberado como control biológico de la arañita roja, Tetranychus urticae Koch, en Fresas (Fragaria × ananassa Duchesne) en el norte de la Florida. Liberaciones de N. californicus se realizaron en intervalos de un mes desde Diciembre 2006 hasta Febrero 2007, para compa- rar los efectos del tiempo de liberación de los predadores en la estructura de la comunidad de artrópodos presentes. Evaluaciones de la estructura de las comunidades se realizó tres veces durante la temporada de producción. El índice de Shannon-Weaver fue usado para cuantificar las diferencias entre los lotes donde se hicieron las liberaciones y los lotes de control. Nuestros resultados demuestran que la liberación de N. californicus no afecta significa- tivamente la diversidad de artrópodos en el sistema de fresas estudiado. El comportamiento alimentario generalista de N. californicus y el alto nivel de riqueza y diversidad del sistema de producción de fresas, puede dispersar el efecto cuantificable de N. californicus en la estructura de la comunidad. Esta característica hace que N. californicus sea un controlador biológico importante para el manejo de la arañita roja en fresas, al mismo tiempo que se con- serva la diversidad del sistema.

Translation provided by the authors.

Twospotted spider mite, Tetranychus urticae due to increased use of pesticides in modern cul- Koch (TSSM), is a key pest of strawberries tural practices. As a result, more growers are uti- (Fragaria × ananassa Duchesne) in north Florida. lizing biological control as an alternative to chem- High populations of TSSM can reduce foliar and ical management (Huffaker et al. 1969; Escudero ﬂoral development thereby decreasing the quality & Ferragut 2005; Rhodes et al. 2006). However, and quantity of mature fruit (Rhodes et al. 2006). little is known about the non-target effects of bio- Twospotted spider mite populations have become logical control releases on beneﬁcial arthropods in resistant to most acaricides due their short life cy- the strawberry ecosystem. cle and high fecundity (Huffaker et al. 1969; Wil- Phytoseiid mites have been found to be highly liams 2000; Cross et al. 2001; Stumpf & Nauen effective predators in controlling TSSM (Zhi-Qui- 2001; Sato et al. 2004). Outbreaks of TSSM have ang & Sanderson 1995). Two of the most com- become more frequent over the last few decades monly used phytoseiids are Phytoseiulus persimi-

Fraulo et al.: N. californicus and Arthropod Community Structure 437 lis Athias-Henriot and Neoseiulus californicus IPM or biological control program in north Flor- (McGregor) (McMurtry & Croft 1997; Cloyd et al. ida strawberry while preserving non-target bene- 2006). Oatman et al. (1972) found that although ficial arthropods. P. persimilis was effective in controlling TSSM, it is a type I specialist predator of Tetranychus spe- MATERIALS AND METHODS cies and tends to decimate TSSM populations, al- tering the arthropod complex (McMurtry & Croft A preliminary study was conducted during 1997). However, Colfer et al. (2004) found that re- 2005-2006 (Jan to Mar) to assess the accuracy of leases of generalist species of phytoseiid mites sample methods and level of diversity in the such as N. californicus do not affect the diversity strawberry system. The main study was con- or abundance of arthropod populations. ducted during the 2006-2007 (Oct to Mar) grow- As a type II generalist, N. californicus has a ing season to evaluate the effect of predatory re- broad diet range that includes not only various ar- leases at 3 phenological periods: foliar, floral, and thropods, but also plant sap, honeydew, and pollen fruit development. (McMurtry & Croft 1997). Neoseiulus californicus can adapt to fluctuations in prey populations, pro- Field Preparation viding stable pest suppression over time (Croft et al. 1998; Castagnoli et al. 1999; Escudero & Fer- The field experiment was located at the Uni- ragut 2005; Greco et al. 2005). Rhodes et al. (2006) versity of Florida Plant Science Research and Ed- observed that N. californicus was able to maintain ucation Unit in Citra, Florida (82.17°W, 29.41°N). more consistent control of TSSM populations com- Sixteen research plots of 53.29 m2 with a bare pared with P. persimilis throughout the season in ground buffer of 11 m between plots were planted north Florida strawberry fields. The ability of N. with strawberries, variety ‘Festival’, during the californicus to survive on a broad array of food first week of Oct 2005 and 2006 in raised beds cov- sources contributes to its stability and may miti- ered with 6-mil black plastic mulch. Strawberry gate its effect on community structure and other plants were fertilized through the drip irrigation beneficial arthropods (Jones 1976; Powers & Mc- system once per week with 18.5 kg of ammonium Sorley 2000; Cross et al. 2001; Rhodes et al. 2006). nitrate (Southern States Cooperative, Inc., Rich- There are many natural enemies capable of mond, VA) and 32.7 kg of muriate of potash suppressing TSSM populations (Oatman et al. (Southern States Cooperative, Inc., Richmond, 1985). However, their use in biological control has VA) per ha. Nitrogen was increased in Feb to 27.1 been limited due to their generalist feeding pref- Kg/ha of ammonium nitrate to accommodate in- erences. Field studies conducted between 1964- creased nutrient demand during fruit develop- 1980 in southern California identified 9 phyto- ment. Fungicides were applied 3 times per week seiid mite species and several species of insects in rotation to all experimental plots throughout within the families Thripidae, Cecidomyiidae, the season to combat Botrytis fruit rot (Botrytis ci- Coccinellidae, Staphylinidae, Anthocoridae, Lyga- nerea) and anthracnose fruit rot (Colletotrichum edae, Chrysopidae, and Hemerobiidae as natural acutatum). The fungicides used were Abound® enemies of TSSM (Oatman et al. 1985). Rondon et (azoxystrobin) (Syngenta Crop Protection, al. (2004) conducted laboratory studies evaluating Greensboro, NC), Topsin® (thiophanate) (Cerexa- the big-eyed bug, Geocoris punctipes Say, minute gri, Inc., King of Prussia, PA), Aliette® (alumi- pirate bug, Orius insidiosus (Say), and the pink num tris) (Bayer Crop Science, Research Triangle spotted lady beetle, Coleomegilla maculata De- Park, NC), and Serenade® (Bacillus subtilis) Geer, as predators for TSSM. They found that (Agraquest, Davis, CA). No insecticides or acari- while they feed on TSSM, they preferred other cides were applied to the research plots. Prepara- phytophagous insects, thereby limiting their util- tion and management procedures are described in ity as successful biological control agents. detail in Fraulo & Liburd (2007). Conserving a robust ecosystem is essential to The experimental design used was a random- sustain the myriad of natural enemies that con- ized complete block with 4 treatments and 4 rep- tribute to a sustainable integrated pest manage- lications. Neoseiulus californicus (Koppert Biolog- ment (IPM) program. In this study, field experi- ical Systems, Romulus, MI) was released in all ments were conducted to determine the effect of treated plots at the recommended rate of 1-2 releasing N. californicus as a biological control predators per square meter. Viability was as- agent for TSSM on the arthropod complex in sessed by observing 20-30 predatory mites in a strawberry fields, and evaluated with the Shan- Petri dish with a dissecting binocular microscope non-Weaver index (H’) (Shannon 1948). Our hy- (10-20×) (Leica MZ12.5, McBain Instruments, pothesis was that inundative releases of N. cali- Chatsworth, CA) for 15 min before each release to fornicus to control TSSM in strawberries will not ensure that the mites were vigorously active. The negatively impact other key natural enemies and treatments included releases of N. californicus as arthropod diversity in the strawberry system. If follows: (1) in the “early” season at foliar develop- so, N. californicus could be released as part of an ment, 4 weeks after planting (WAP), (2) during

438 Florida Entomologist 91(3) September 2008

the “mid” season at floral development, 8 WAP, (3) was collected by the method described in the pre- “late” in the season at fruit development, 12-16 liminary sampling, identified, and recorded. Un- WAP, and (4) “no release” untreated control. known taxa were identified at the Department of Plant Industry, Gainesville, FL. Data were col- Preliminary Study lected throughout the season and compared to determine the effect of N. californicus releases on Field preparations for the preliminary study arthropod assemblages in the field within each are described above and in Fraulo and Liburd distinct period. (2007). The goal of the preliminary study was to We employed 4 sampling methods in order to determine an appropriate sample size and to eval- increase the probability of encountering a higher uate diversity with the Shannon-Weaver diver- diversity of taxa and to avoid bias, as follows: (1) sity index. Data were collected at 12 WAP, during In situ (visual inspection), (2) foliar sampling, (3) the “late” season of the 2005-2006 field season to pitfall traps, and (4) yellow sticky traps. assess the overall effect of N. californicus on the In situ Sampling. Twenty-four strawberry arthropod assemblage in the strawberry field. plants from the interior rows of each plot were vi- One yellow sticky Pherocon® AM Trap (YST) sually inspected once weekly for 2 weeks during (Trécé, Inc., Adair, OK), 28 cm × 23 cm surface each sample period. The visual inspection con- area with 56 squares of 6.45 cm2 (1 in2) forming a sisted of a scan for 30 s for each plant. This en- grid on the board was hung on a garden stake 30 abled us to sample the larger arthropods occur- cm above plants. Each trap was placed in the cen- ring in the field including macro-hymenopterans, ter row of each of the 24 treatment plots. Traps hemipterans, and coleopterans. were collected weekly for 5 weeks and placed into Foliar Sampling. Four young trifoliate leaves Zipper Seal Storage Bags© (American Value, Dol- from the inside of the plant crown and 4 old trifo- gencorp, Inc., Goodlettsville, TN) and transported liates from the outer-crown were taken randomly to the Small Fruits and Vegetable IPM Labora- from each treatment plot. Samples were con- tory at the University of Florida, Gainesville, FL ducted weekly for 2 weeks after each of the 3 pred- to be examined under a dissecting microscope (10- atory releases. The leaves were placed in a ziplock 20×) (Leica MZ12.5, McBain Instruments, Chat- bag and transported to the laboratory where they sworth, CA). To develop a sub-sample protocol, 3 were visually inspected under the dissecting bin- YSTs were randomly chosen from all samples and ocular microscope for leaf-dwelling and minute each of the 56 one-inch squares on each trap was arthropods. examined to determine the arthropod families Pitfall Traps. Traps were constructed of white found per square. The families observed on each polypropylene deli containers 14 cm deep and square of the YST were counted and compiled into 10.5 cm in diameter (Fabri-Kal Corp., Kalamazoo, a comprehensive list, and recorded. A cumulative MI) filled with 0.15 L of 10% dish soap and water frequency distribution was plotted for each solution. The traps were placed in the soil under square to determine the optimal sub-sample size. the black plastic mulch in one of the 2 center rows These data were used to create a sub-sampling of each treatment plot to capture cursorial soil ar- scheme for data analysis in the main study. The thropods and soil dwellers (Southwood 1966). The frequency tables of the families with their key traps were left in the field for 48 h each week for taxonomic characteristics were recorded and used a 2-week period after each of the 3 predatory re- for primary identification during the main study. leases. Yellow Sticky Traps. One trap per plot was Main Study placed in one of the 2 center rows at foliar height, approximately 30 cm above ground to capture We evaluated the effect of N. californicus by winged arthropods. The YST were left in the field sampling at 1-month intervals 2 weeks after each for 48 h each week for a 2-week period after each release date, based on the homogeneity of the pre- of the 3 predatory releases. In the laboratory, a liminary results, field observations, and previous proportion of each trap surface area was observed research by Garcia-Mari & Gonzalez-Samora for analysis based on results of the preliminary (1999). Arthropod sampling was conducted during samples. the 2006-2007 field season at (a) 2 months after planting (“early” season), (b) 3 months after Statistical Analysis planting (“mid” season), and (c) 4 months after planting (“late” season). Individuals were identi- The arthropod assemblages among treatments fied to family or genus depending upon the level of in both the YST and pitfall traps throughout the functional variation within the taxon, based on season were analyzed with a Non-Metric Multidi- notes from the preliminary study described above mensional Scaling (NMS) ordination with PC- and previous research (Jones 1976; Cross et al. ORD 4 (Kruskal 1964). This method is well-suited 2001; Arevalo et al. 2006; Klein et al. 2006). The for describing patterns in community data and number of individuals present from each taxon does not assume normality (McCune & Grace 2002).

Fraulo et al.: N. californicus and Arthropod Community Structure 439

The ordination was conducted by the Sørensen distance measure (McCune & Grace 2002) with a random starting configuration. The autopilot set- ting on medium thoroughness was used to determine the dimensions of the ordination (McCune & Grace 2002). Fifteen runs with real data with 200 iterations were used. To assess the strength of the ordination, the Monte Carlo option with 30 runs of randomized data was selected. Data were square-root transformed if the correlation of variation among rows and columns were greater than 50% (McCune & Grace 2002) and outliers were removed to strengthen the structure of the data. Fig. 1. Distribution frequency used in the prelimi- Rare families that were present in numbers too nary trial to calculate optimal sub-sample size for low to be included in the ordination were recorded squares on yellow sticky card trap (YST). in a comprehensive list for each treatment and were included in diversity calculations. All taxa found were included in the calculation of the Sh- season (Dec) we compared the plots treated with annon-Weaver diversity index and results among N. californicus releases and untreated plots treatments were compared by analysis of vari- (without N. californicus releases). The arthropod ance (ANOVA) followed by mean separation with assemblages found in pitfall traps showed a weak LSD test (SPSS 2004). To convert the results of structure (axis 1, P = 0.13; axis 2, P = 0.13; axis 3, the Shannon-Weaver index into a true diversity P = 0.32) indicating that N. californicus releases measure, the exponential of the entropy value did not have a significant effect on the arthropod was calculated (Jost 2006), as follows: assemblages. When data were square-root transformed and outliers were removed, the NMS ordi- s nation remained non-significant (axis 1, P = 0.13; Dpipi= exp– ∑ ln = exp()H′ axis 2, P = 0.29; axis 3, P = 0.48). Results from  NMS ordination of the YST also were not signifi- i = 1 cant (axis 1, P = 0.52; axis 2, P = 0.68; axis 3, P = 0.48). The coefficient of variation was low where pi = the proportional abundance of taxon. (39.17%) indicating that transformation of data D = true diversity measure. has no effect on data structure. During the “mid” season (Jan) no significant RESULTS differences were recorded in assemblages collected in the pitfall traps (axis 1, P = 0.29; axis 2, Preliminary Study P = 0.26; axis 3, P = 0.26) by the NMS ordination. Yellow sticky traps also showed no significant dif- Sub-sampling procedures demonstrated that ferences among treatments (axis 1, P = 0.29; axis 28 squares on the YST consistently included at 2, P = 0.13; axis 3, P = 0.23). Transformations least 90% of the arthropod families recorded (Fig. were not recommended as it did not affect data 1). Therefore, 28 squares (47% of the trap area, structure. excluding borders) were observed for analysis in In the final NMS ordination, no significant dif- the main study. The Shannon-Weaver index indi- ferences among treatments were found in the late cated no significant differences in level of diver- season (Feb), for pitfall trap data (axis 1, P = 0.13; sity among any of the treatments in the prelimi- axis 2, P = 0.16; axis 3, P = 0.32). When outliers nary study (F = 0.5; df = 3, 12; P = 0.69). were removed from the data set results remained non-significant (axis 1, P = 0.13; axis 2, P = 0.16; Main Study axis 3, P = 0.13). Yellow sticky traps showed no differences among arthropod assemblages with Arthropod community structure following re- introduction of N. californicus (axis 1, P = 0.52; leases of N. californicus for biological control of axis 2, P = 0.71; axis 3, P = 0.71). Removing outli- TSSM was analyzed during various periods ers did not affect data structure (axis 1, P = 0.29; throughout the growing season. The NMS ordina- axis 2, P = 0.32; axis 3, P = 0.58). tion conducted following releases of N. californi- The true diversity index based on the Shan- cus during “mid” season sampling showed a weak non-Weaver index (“D”) showed a significant ef- community structure and did not provide any fect on arthropod diversity in the YST in the groupings of the data related to the treatments “early” season (F = 5.35; df = 3,12; P =0.01), but imposed (Fig. 2). A similar lack of structure was not in the pitfall traps (F = 0.3; df = 3,12; P = observed in ordinations for the “early” and “late” 0.83). “Mid” season YST and pitfall traps showed sampling dates (data not shown). In the “early” no significant effect on diversity (F = 1.3; df = 440 Florida Entomologist 91(3) September 2008

Fig. 2. Non-Metric Multidimensional Scaling (NMS) ordinations of arthropod communities in “mid” season pitfall traps (a, b) and yellow sticky traps (c, d) showing weak data structure along axis 1 and 2 (a, b), and axis 1 and 3 (c, d) with no signiﬁcant differences (P < 0.05) among treatments. = Early release; = Mid-season release; = Late release; × = No Release (control).

3,12; P = 0.7; and F = 0.3; df = 3,12; P =0.57, re- plots (personal observation), as did six-spotted spectively). Yellow sticky traps (F = 2.8; df = 3,12; thrips Scolothrips sexmaculatus (Pergande) and P = 0.08) and pitfall traps (F = 6.5; df = 3,12; P = Geocorid bugs Geocoris spp. Late in the season, 0.6) also showed no significant difference among numbers of taxa decreased, and an increase of treatments late in the season (Tables 1 and 2). Bradysia spp. (Sciaridae) was observed. Overall, the visual and foliar samples did not produce sufficient numbers of arthropods to con- DISCUSSION duct robust statistical analysis. However, they should not be dismissed because they revealed in- Ordination results confirmed the lack of treat- teresting phenological trends and important nat- ment effects observed through the analysis of ural predators of strawberry pests. Early in the variance. If the treatments had affected commu- season thrips (Frankliniella spp.) and Chalci- nity structure, points representing the same doidea populations were significantly higher in treatment would have clustered together in the the treated plots compared with the untreated ordination figures (Klein et al. 2006), but this was plots (F = 4.81; df = 1, 30; P = 0.04, F = 8.44; df = never observed. Ordination used to describe the 1, 30; P = 0.01, respectively) During the “mid” sea- community patterns and the measures of diver- son high numbers of Pachybrachius spp. and a sity both indicated that presence of N. californicus dramatic decline in aphid population directly fol- did not disrupt the natural ecology of the system. lowing an increase in syrphid abundance were ob- Neoseiulus californicus was released at several served (Tables 3, 4, 5, and 6). Foliar sampling in- times during the season and persisted through dicated that as the season progressed, the abun- the experiment, not disrupting arthropod assem- dance of Coccinellids increased in all treatment blages while significantly reducing TSSM popula- Fraulo et al.: N. californicus and Arthropod Community Structure 441

TABLE 1. MEAN (± SE) VALUES OF SHANNON-WEAVER DIVERSITY INDEX (D) FOR EACH SAMPLE PERIOD FOR YELLOW STICKY TRAPS.

Sample date

Treatment Dec Jan Feb Preliminary

Early 2.9 ± 0.16 c 9.4 ± 1.00 7.1 ± 0.68 8.6 ± 0.41 Middle 2.5 ± 0.20 b 8.6 ± 0.30 8.8 ± 0.91 8.7 ± 1.40 Late 3.9 ± 0.34 a 7.5 ± 0.66 5.7 ± 1.00 8.2 ± 0.14 No-release 3.1 ± 0.28 b 8.2 ± 0.53 6.3 ± 0.47 7.0 ± 0.95

Means with the same letter within columns are not significantly different (P < 0.05) based on LSD test. Dates with no letters represent dates with no significant differences. tions as observed in a related study (Fraulo & Chalcidoidea populations were present through- Liburd 2007). The Shannon-Weaver index on YST out the field early in the season. Neoseiulus cali- indicated a significant difference on community fornicus is a known predator of thrips. However, structure between treated and untreated plots in adult thrips migrate into flowering strawberry the “early” season. However, this effect was short plants and take shelter within the styles of the lived and was non-significant for the remainder of strawberry flower where N. californicus cannot the season. This early disruption may be due to access them (Cross et al. 2001). Increased levels of sparse and clumped populations within arthropod the superfamily Chalcidoidea, which are parasi- communities at the beginning of the season and toids of thrips, were also observed in higher num- did not have a significant overall effect. bers in the plots with high numbers of thrips. The majority of predators in the strawberry Aphids were abundant in all treatments dur- system are generalist feeders and N. californicus ing the “early” season and decreased throughout itself is a generalist predator. Feeding preference the season. Decreasing numbers of aphids in con- likely moderated the impact on the arthropod as- junction with increased numbers of Syrphidae are semblage. Our results indicate that the release of consistent with studies conducted in north Wales N. californicus does not have a statistically signif- showing that Syrphidae can cause considerable icant effect on the assemblage and community reduction in aphid numbers (Cross et al. 2001). functioning of arthropods in the strawberry sys- This function was not affected by the presence of tem. Its release did not affect the balance and reg- N. californicus. Foliar sampling indicated that as ulation of the natural ecosystem in our study. the season progressed, the abundance of sixspot- Generalist feeding behavior coupled with a high ted thrips (S. sexmaculatus) and Geocoris spp. in- level of richness and insect diversity in the straw- creased in all treatment plots (both are predators berry system may be key factors in reducing the of TSSM). effect of N. californicus releases on the structure Our findings from this and previous release of the strawberry system. studies demonstrate that releasing N. californi- There were no overall non-target effects on cus in the field at the recommended rate of 1-2 N. natural enemies. Major insect families (Thripi- californicus per m2 when TSSM populations are dae, Cecidomyiidae, Coccinellidae, Staphylinidae, low (≤70-80 TSSM per trifoliate) provides season- and Lygaedae) as cited by Oatman et al. (1985) long control of TSSM and does not disrupt other and Rondon et al. (2004), were present through- natural enemies of seasonal pests (Jones 1976; out our study. Thrips (Frankliniella spp.) and Fraulo & Liburd 2007). A one-time application of

TABLE 2. MEAN (± SE) VALUES OF SHANNON-WEAVER DIVERSITY INDEX (D) FOR EACH SAMPLING PERIOD FOR PITFALL TRAPS.

Sample date

Treatment Dec Jan Feb

Early 5.4 ± 0.76 4.7 ± 0.77 3.8 ± 0.42 Middle 5.0 ± 0.44 3.7 ± 0.44 3.7 ± 0.09 Late 5.2 ± 0.62 3.7 ± 0.54 4.4 ± 0.37 No-release 5.8 ± 0.63 3.8 ± 0.46 3.9 ± 0.47

No signiﬁcant differences (P < 0.05) among treatments on any sampling date. 442 Florida Entomologist 91(3) September 2008 48 94 48 spp.) 3 2 1 1 spp.) 1 4 5 2 spp.) 3 — 1 6 spp.) 2 8 5 2 spp.) 52 hybrachius hybrachius c rankliniella Hippodamia Pa Sphaerophoria F Bradysia ygaeidae ( . Ichneumonidae 3 8 4 4 Coccinella ( MuscidaeSciaridae ( 17 14 14 19 Syrphidae ( Thripidae ( PERIODS

44 —1 —2 —1 SAMPLING 3 11 43 36 THE

.) .) 11910 )16179 .) . spp spp.) — — 1 1

spp spp spp DURING

sp.) 23 17 24 8 Tachinidae 2 4 4 2 TRAPS

Alticinae hybrachius hybrachius Hippodamia c rankliniella Sphaerophoria Pa F Bradysia STICKY

ygaeidae ( YELLOW

Coccinellidae ( Chrysomelidae ( Cecidomyiidae 10 8 1 Syrphidae ( Thripidae ( IN

FOUND

Dec Jan Feb 59 83 91 SPECIMENS

EMLNR EMLNR EMLNR OF

sp.) 39 39 — 23 Staphylinidae — 2 1 — NUMBER

spp.) 5 5 50 10 Sciaridae ( rankliniella F Bradydia UMULATIVE 3. C E = early treatment, M = middle treatment, L = late treatment, and NR = no release. L = late treatment, M = middle treatment, E = early treatment, ABLE StaphylinidaeCucujidae — 2 — — 1 — Cicadellidae 11 — 3 3 4 2 Lepidoptera 1 — — — ChrysomelidaeCicadellidae — — 2 — 11 1 17 Chalcidoidea 5 61 66 78 53 Drosophilidae 1 — — — AcanalonidaeAleyrodidaeAphididaeBethylidaeBibionidaeCecidomyiidaeChalcidoidea 2 2 1 383 16 643 — 2 579 26 11 — — 539 1 10 14 Aphididae 34 Acanalonidae Aleyrodidae 5 1 6 — 5 9 Tachinidae — Braconidae Bibionidae 4 12 2 1 10 17 5 3 5 3 2 11 3 3 8 1 Cecidomyiidae 1 Aleyrodidae Aphididae 1 2 3 — 3 5 1 Chalcidoidea Cicadellidae Chrysomella 4 — 6 6 4 8 6 — 33 1 — 7 1 26 2 33 2 3 2 31 1 2 7 — DolichopodidaeDrosophilidae 7 17 3 — 4 — 3 — Drosophilidae Ichneumonidae 4 4 1 — 3 2 — 1 L Nitulidae 2 1 2 — IchneumonidaeLepidopteraMuscidae — — 1 4 1 8 4 — Leiodidae 7 1 9 Dolichopodidae 30 L — 2 1 4 1 4 1 5 Phoridae Psychodidae — 2 — 6 2 1 1 2 NitulidaePhloeothripidae 3 — 2 — 4 2 3 — Nitulidae Muscidae 23 13 15 15 Staphylinidae 1 — 1 2 — 1 1 1 PhoridaePlatygatroidaePsychodidaeSciaridae ( Thripidae ( 1 3 — 1 16 — 3 — 7 10 Phoridae 7 — Phloeothripidae Psychodidae 1 10 — 5 14 — 40 2 — 9 — Araneida 1 Dolichopodidae 10 1 7 1 3 1 4 3 T Fraulo et al.: N. californicus and Arthropod Community Structure 443 spp.) 1 — — — spp.) 4 1 — 8 spp.) 9 7 14 15 rankliniella Geocoris F Bradysia Staphylinidae — — 1 2 Thripidae ( 29 . 47 —— PERIODS

21 1— 18 SAMPLING .) 3 spp

spp.) 2 2 2 4 THE

spp.) 4 2 1 2 DURING

hybrachius c rankliniella Pa F Bradysia TRAPS

ygaeidae ( PITFALL

Aphididae 11 2 6 5 Aphididae 1 — 1 1 Thripidae ( IN

FOUND

1— Dec Jan Feb SPECIMENS

EMLNR EMLNR EMLNR —1 OF

.) spp spp.) 1 5 3 1 NUMBER

spp.) — 1 1 2 Alticinae rankliniella F Bradysia UMULATIVE 4. C E = “early” treatment, M = “mid” treatment, L = “late” treatment, and NR = no release. treatment, “late” L = treatment, “mid” M = treatment, “early” E = ormicidae 35 26 6 42 Nitulidae — — 1 — Araneida 3 1 1 — ettigoniidae — 2 — — ABLE AphididaeApoideaBibionidaeCecidomyiidaeChalcidoideaChironomidaeCicadellidae 19Drosophilidea 9 8 — 2 — — 5 7 — — 4 1 — 9 7 2 1 Cecidomyiidae — 3 17 — 1 — Cicadelidae — Collembola Chalcidoidea — 2 1 — Cucujidae Gryllidae — — Drosophilidae 2 4 Miridae — — 1 50 6 85 1 2 132 1 — 2 1 — 65 1 — Braconidae — — 2 Chrysomellidae — Chalcidoidea — 1 — Cecidomyiidae — — 1 Formicidae Collembola ( Lygaeidae — — — — 1 — 1 — 1 1 — — 10 — — 1 1 24 — 1 13 11 39 2 Chrysomelidae ( Collembola 41 21 23 31 Formicidae 44 9 2 2 Sciaridae ( CucujidaeElateridaeF IchnueumonidaeLepidoptera 1 — — — — — 1 — — — 1 — L — — — Phoridae Muscidae 2 Sciaridae ( — — — — 1 1 — — Muscidae Vespidae — — — 1 2 — — — MiridaeMuscidaeMutillidaeNematode 1 2 1 — — 2 — — — 2 — — — — — Araneida Staphylinidae — Tettigoniidae 1 1 4 — — — 3 — — 2 — 2 PhloeothripidaePhoridaeSciaridae ( StaphylinidaeT Thripidae ( —Araneida 1 1 2 3 — 3 1 Scollidae 2 1 1 2 1 2 5 2 — — 1 — T 444 Florida Entomologist 91(3) September 2008

TABLE 5. CUMULATIVE NUMBERS OF SPECIMENS RECORDED DURING VISUAL EVALUATIONS.

Dec Jan Feb

EMLNREMLNREMLNR

Tettigoniidae 3133 ———— 4724 Apoidea 6 9 5 ———— 0132 Syrphidae (Sphaerophoria spp.) 3314161368 21—1 Araneida — — 1 2 1 8 4 2 — — — Lepidoptera 1111 ———— —— 1— Muscidae 1222 ———— 1— 1 2 Chrysomelidae 1 — — — ———— 1—— 1 Coccinelidae (Hippodamia spp.) 1 — — — 12—— 1——— Lygaeidae (Tristicolor spp.) ———— ———— ——— 1 (Pachybrachius spp.) ———— 8 2 6 121—— 1 Sciaridae (Bradysia spp.) ———— ———— 52283914 Cicadellidae ———— ———— —1——

E = “early” treatment, M = “mid” treatment, L = “late” treatment, and NR = no release.

TABLE 6. CUMULATIVE NUMBERS OF SPECIMENS RECORDED DURING THE FOLIAR EVALUATIONS.

Dec Jan Feb

EMLNREMLNREMLNR

Aphididae 43 64 28 40 — 1 4 4 1 1 — — Aleyrodidae 29 22 22 2 2 2 2 2 — — — 3 Thripidae (Frankliniella spp.) 72111441414—3—3 (Scolothrips sexmaculatus)—122 63101041 32 Chalcidoidea — — 1 — ———— ———— Lepidoptera 1 — — — ———— 6 6 2 9 Syrphidae (Sphaerophoria spp.) ———— 9 8 9 9 4 5 1015 Lygaeidae (Geocoris spp.) ———— ———— 3 —— 9

E = “early” treatment, M = “mid” treatment, L = “late” treatment, and NR = no release.

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