U Tomatoes in the-Sacramento Valley of California · Infor- mation on insecticide applications to the 1981 and 1983 fields was not available. 1985- 1986 Fields. Fields of commercial

Parasitism of Heliothis zea (Lepidoptera: Noctuidae) Eggs: Effect on Pest Management Decision Rules for Processinn

U . _ _ _

Tomatoes in the-Sacramento Valley of California

MICHAEL P. HOFFMANN, LLOYD T. WILSON, FRANK G. ZALOM, AND RICHAHD J. HILTON

Department of Entomology, University of California, Davis, California 95616 4

Environ. Entomol. 19(3): 753-763 (1990) ABSTRACT Egg parasitism of Hefiothis zea (Boddie) and other lepidopterous pests was monitored in a field trial of processing tomato cultivars in 1981 and in several late-season commercial fields of processing tomatoes in the Sacramento Valley of California in 1983, 1985, and 1986. Four species of Trichogramnta were present: T . pretiosum Riley, T. thalense (Pinto & Oatman), T. deion Pinto & Oatman, and T. brevicapillunz Pinto & Platner. Actual parasitism of H . zea eggs exceeded 83% in all fields monitored in 1985 and exceeded 62% in most fields monitored in 1986. Mandrrca spp. and Trichoplusia ni (Hubner) eggs were also commonly parasitized by Trichogramma spp. The high levels of H . zea egg parasitism recorded in these commercial fields indicates that the current economic threshold, which is based on the abundance of white N. tea eggs, can be increased to account for the mortality caused by Trichogramma. Procedures to incorporate H. tea egg parasitism into the current integrated pest management program for processing tomatoes are proposed. Acceptable fruit quality at harvest i n fields that exceeded the current economic threshold during the growing season provides additional support for increasing the threshold. The effect of insecticide applications on H . zea egg parasitism is discussed.

KEY WORDS Insecta, Trichogramma spp., Heliothis spp., egg parasitism

CALIFORNIA PRODUCES apprcximately 6,300,000 t of processing tomatoes, Lycopersicon esculentum Aliller, annually on a total of 91,800 ha. Approxi- n~ately 37,000 ha are planted in the Sacramento Valley (Anonymous 1988). The tomato fruitworm, Heliothis t ea (Boddie) (Lepidoptera: Noctuidae), beet armyworm, Spodoptera exigua (Hubner), and the western yellowstriped armyworm, S. praefica (Grote), are the primary lepidopterous pests of processing tomatoes grown in the Sacramento Valley (Lange & Bronson 1981). The cabbage looper, Trichoplusia ni (Hiibner), and hornworms, Man- duca spp., are generall) present in fields, but not at econoniically important levels. H. zea is the most important pest because it feeds within the fruit, resulting in reduced crop quality and marketabil- i t y . The presence of insects, insect parts, excreta, etc., within the harvested crop can result in part or all of the crop being rejected if the level exceeds the 2% standard set by the Canners League of California (1980).

An integrated pest management (IPM) program has been developed for these lepidopterous pests of processing tomatoes. The treatment threshold component of the program is based on relationships between fruit damage caused by larvae during the Season and fruit quality at harvest, and is field-

' Current address: Southern Oregon Experiment Station, Med- ford, Oreg. 97502.

implemented using a dynamic, sequential sampling scheme (Wilson et al. 1983). 'The prorgram also includes a sampling plan for H . zea eggs and an associated treatment threshold based on egg density (Brendler et al. 1985). Basing treatment decisions on egg abundance has the advantage of improved control, because applications of insecticide can be timed to coincide with H. zea egg hatch, and controls are applied before larvae enter the fruit; thus fruit quality is not jeopardized.

The treatment threshold that is based on H. zea egg abundance is inherently conservative, because it was developed under the assumption that egg mortality would be minimal. Egg mortality caused by parasitoids was not considered in the develop- ment of the egg'treatment threshold, because little information regarding their impact was available (Lange & Bronson 1981). However, naturally occurring populations of Tricliogranzma have been found to be important parasitoids of lepidopterous pests in fresh market and processing tomatoes grown in southern California (Oatman & Platner 1971, Oatman et al. 1983a). Roltsch & Mayse (1983) found that Trichogranznia is an important mortality factor of Heliothis spp. on fresh market tomatoes grown in the spring in southeastern Arkansas, and Graham (1970) reported Trichogranzma parasitizing up to 74.6 and 65.1% of Heliothis spp. and T. ni eggs, respectively, on tomatoes in Texas. Meierrose & Aralijo (1986) reported 80.4% parasitism of H. armigera Hubner on tomatoes grown in Portugal,

0046-225X/90/0753-0763$02.00/0 Q 1990 Entomological Society of America

- ~ . ~ . --pT"--"--, -- from applications of insecticides. Insecticide applications to tomatoes generally result in decreased parasitism of Heliothis spp. eggs Oatman et al. 1983b, Meierrose & Arahjo 1986), although Roltsch & Mayse (1983) reported conflicting results when comparing insecticide-treated and untreated tomatoes. Immigration of adult Tricli,, pramma into previously treated fields and emergence of adult Trichogramnia from host eggs parasitized before application of insecticide, can confound the detec- tiori of differences in parasitism betu.een fields.

The objectives of the research reported herein were to determine what species of egg parasitoids were present, to quantify rates of parasitism of eggs of H . zea and other lepidopterous pests, and pro- pose a technique to incorporate H . :ea mortality into the existing economic threshold. and to determine the effect commercial insecticide applications have on parasitism of H . zeu eggs b!. Trichogram- m a in late-season commercial processing tomatoes.

Materials and Methods Parasitism was defined in two u a > s for these

studies. H . zea eggs turn black about 4 d after being parasitized by Trichograninza (Graham 1970). Consequently, when observed in the field, H. zea eggs and eggs of other species were considered parasitized if black in color, and u.hite or cream- colored eggs were recorded as unparasitized. The term "field parasitism" is used herein, and repre- sents the rate of egg parasitism based on the percentage of black eggs in the field. However, field parasitism may be biased, because i t requires about 10 d for Trichogramma to develop and emerge from H . zea eggs, whereas H. zea larval eclosion occurs in about 4 d. Consequently, there may be an accumulation of parasitized (black) eggs in the field at any given time. To minimize this potential bias we used the method previously used by Gra- ham (1970) and Roltsch & Mayse (1983). Percent- age of parasitism was determined based on the number of white eggs that were parasitized. Black eggs were not included in the calculation. Because this method of determining percentage of parasitism is less biased by the accumulation of parasitized (black) eggs and thus a more timely estimate, it will be referred to as "actual" parasitism, i.e., as of the present moment.

The eggs of other noctuids may be present in processing tomato fields. Females of Ef. phloxipha- gu Grote & Rc+inson, are known to oviposit on tomato during the early season (Lange & Michel- bacher 1937); however, larvae do not survive. H. virescens (Fabricius) may also be found on tomatoes (Okumura 1974). Because neither species is considered to be a pest of processing tomatoes in the Sacramento Valley and because H . phloxipha-

- ~ ~ ~ ~ ~ ~ r r u ~ m mol a n e r n p r t o k t i n . guish them from H. zea eggs.

1981 and 1983 Fields. Field parasitism of eggs of H. zea, T. ni, and Manduca spp. was recorded from a trial of processing tomato cultivars located on the Department of Vegetable Crops Facility, University of California-Davis, at weekly intervals from 16 July to 17 September 1981. The planting consisted of 21 cultivars planted in a randomized complete block design wi th each cultivar repli. cated four times. Samples consisted of uprooted whole plants; these were thoroughly searched and the number of black and white eggs recorded by species. Because of low egg densities, rates of parasitism are reported for all cultivars combined.

Five commercial processing tomato fields located in the Sacramento Valley were sampled for the same species in 1983. Zalom et a!. (1983) determined that the preferred oviposition site for H. zea on processing tomato plants was the first leaf below flower clusters. These leaves were chosen as the sample, uni t and \\ere examined for the presence of black and white eggs of all target species. All such leaves were examined from 4 to 6 tomato plants located about 5, 25, and 45 m from field edge, for a total of 12 to 18 plants per field per observation. The first samples were taken 12 July and continued weekly until near harvest. Because egg abundance was relatively low, field parasitism was calculated by summing across the three sampling locations in each field on each date. Infor- mation on insecticide applications to the 1981 and 1983 fields was not available.

1985- 1986 Fields. Fields of commercial processing tomatoes grown in the Sacramento Valley were sampled for eggs of H . zea, T. ni, and Man- duca during 1985 and 1986. The first tomato leaf below the highest flower cluster on the tomato plant was the sample unit (Brendler et al. 1985). Sam- pling general$ started in mid-JuIy and continued until just before harvest. Fields were harvested in mid-August or later, and consequently were more likely to have high pest densities and higher levels of damage (Lange 6( Bronson 1981). Not all fields were managed by pest control advisors who used the H. zea egg-sampling technique and treatment thresholds as suggested by the University of Cali- fornia (Brendler et al. 1985). Consequently, insecticides were not necessarily applied at the recommended fruit clamage level or H. zea egg density, or at the optimal time for masimum H . zea larval mortality. Information related to pesticide applications to fields being monitored was obtained from pest control advisors or growers.

Fields ranged in size from 12.2 to 41.0 ha and were generally rectangular in shape. Each field was divided into three parallel areas of equal width that ran the length of the field. The centers of the two outermost areas were located approximately

June 1990 HOFFMANN ET AL.: PARASITISM OF Heliothis zea EGGS 755

60 111 from the field edge. The length of each of these was divided into six areas. This resulted in 18 sampling areas per field. Of the six sampling areas per main parallel area, the first and sixth, and second and fifth were centered 20-30 and 60- 90 m, respectively, from the ends of the fields, and the balance was divided between the remaining two areas. The first 10-20 and 40 m on the ends and edges, respectively, of fields were not sampled. Thirty leaves were randomly picked from the central portion of each sampling area in each field. Occasionally, because of irrigation stress, crop ma- turity or disease, tomato plants had few or no flow- ers in some sampling areas of the field; consequently, < s o leaves were sampled within an area on some dates. Eight fields were monitored in 1985 and nine in 1986. Two fields did not have sufficient H . zea eggs and are not included here.

Percentage of parasitism for H. zea eggs was calculated based on records of all eggs observed in each field for each sample date, Le., records across all sampling areas were pooled for each date. To determine actual parasitism, subsamples of up to 10 eggs (for most sample areas in 1985), and nearly all eggs (for all sample areas in 1986), were collected and returned to the laboratory (“2loC, natural lighting) for observation. In 1985, eggs were either dissected in the laboratory after turning dark and examined for the presence of developing Trichogramma, or eggs were placed in 20-ml vials (maximum of 12 eggs per vial) until Trichogram- nm adults or lepidopterous larvae emerged. Vials were obser\*ed almost daily and emerging Tricho- gramnia adults were removed to minimize the chance of unparasitized eggs in the vials being parasitized.

Methods were similar in 1986, except eggs were returned to the laboratory and placed individually (except if eggs stuck together) into gelatin capsules (size 000). Capsules were examined several weeks later for the presence of a dead lepidopterous larva or Trichogramma adults. Eggs were categorized as parasitized if parasitoids emerged or if parasitoids were found to be within eggs (from which nothing emerged) upon dissection. Eggs were categorized as being infertile if they were collapsed and cream colored. Although the exact cause of egg collapse was not known, we placed these eggs in this category because they were similar in ap- pearance to H . zea eggs observed in laboratory colonies from which larvae did not emerge. The remaining eggs that did not fall into the above categories and may have been damaged during the handling process \\ere excluded from parasitism calculations. \Ye examined 3,088 H . zea eggs in the field in 1985 and 2,466 in 1986, and of these, 2,094 and 2,192 were observed in the laboratory. A much smaller number of eggs of T . ni and Man- duca spp. were also observed.

Because rates of parasitism for field-collected white and black eggs were not recorded separately,

-

actual parasitism was estimated by using the equation:

P, == 1OO(L - F)/(100 - F)

where P, = percentage of actual parasitism, L = percentage of all eggs parasitized, and F = percentage of field parasitism.

Fruit Quality at Harvest. To relate H . zea infestations and crop quality, fruit samples were taken from each field near harvest in 1985 and 1986. In 1985, random samples of 600 to 1,800 fruit per field were examined and damage by H. zea larvae was recorded for each of four age classes of fruit, as described by Zalom et al. (1986). In 1986, only mature red fruit were examined, with sample size ranging from 600 to 900 fruit per field. To present both years on an equivalent basis (percentage of mature red fruit with damage), the number of mature red fruit present at harvest in each field, in 1985, was estimated based on fruit counts from five tomato plants. This was necessary because the number of damaged fruit per age class was recorded, but not the total number of fruit in each age class. The resulting means of mature fruit per field were used to calculate percentage of damage to mature fruit. In addition, fruit damage grades (for all lepidopterous larvae) as recorded at official processing tomato grading stations were obtained from growers for most harvested fields.

Effect of Insecticide Applications. During the period 23-27 August 1985, five of the seven tomato fields were treated with insecticide for control of H. zea. To determine if the insecticide applications had a significant effect on H . zea egg parasitism, the changes in percentage of actual parasitism that occurred in the treated fields were compared with the changes that were observed in untreated fields. The observations made just before and following the dates of insecticide application were used to determine the change in percentage of actual parasitism for each field. An unpaired t test was used with fields as replicates (Steel & Torrie 1980). A similar analysis could not be performed in 1986, because no fields were treated during late season, when H . zea eggs were most abundant.

Results and Discussion

Parasitoid Species Complex. Four species of Trichogramma were reared from H . ;ea eggs during 1985 and 1986: Trichogranznia pretiosum Ri- ley, T . thafense (Pinto & Oatman), T . &ion Pinto & Oatman, and T . breuicapillunz Pinto & Platner. Preliminary results, based on a subsample of 78 male Trichogramnza taken from two fields in 1986, showed the relative frequency of occurrence of T . pretiosum, T . thalense, T . brevicapillum, and T . deion to be 0.61, 0.29, 0.05, and O.OG, respectively. T . pretiosun and T . brevicapillum were also recorded from Manduca spp. eggs.

756 ENVIRONMENTAL ENTOMOLOGY

Table 1. Parasitism of the eggs of T. ni and Manduca spp. in fields of commercial processing tomatoes, sac Valley ‘?,B *-, .” ,.M

July August September

1-15 16-30-

% % -

1-15 16-31 1-15 16-31

n n n n % n % % %

T. nt \

20 0 7 0 7 0 4 0 0 . -

1981 (Field) 6 0 20 0 109 0 72 0 1983 (Field) 5 0 104 0 29 0 1985-1986 (Field) 3 0 27 0 61 0 17 11.8 6 33.3 o - 1985-1986 (Actual) 0. - 6 0 46 15.2 17 70.6 2 50.0 0 -

Manduca 1981 (Field) 1 0 10 0 33 3.0 25 8.0 31 19.4 4.4 59.1 1983 (Field) 2 0 5 0 7 0 11 0 0 - 4 50.0 1985-1986 (Field) 0 - 2 0 9 1 1 . 1 12 25.0 9 0 0 - 1985-1986 (Actual) 0 - 2 0 8 37.5 10 70.0 5 80.0 o - n = total number of eggs recorded during the interval.

Parasitism of Trichoplusia ni and Manduca. Actual parasitism of eggs of T. ni and Manduca spp. was greatest in late season, reaching 70.6 and 80.0%, respectively, for each species (Table 1). Field parasitism was consistently lower than actual parasitism for both species, in particular for T. ni. Parasitism o f T . ni and Manduca spp. by naturally occurring populations of Trichogramma spp. has been reported to be of importance in tomatoes in other areas. Parasitism of T. nt eggs by T. semifumatum Perkins in tomatoes grown in Texas (based on total eggs observed for the entire season) was 65.1 and 12.3% in 1964 and 1965, respectively (Graham 1970). T . pretiosum was the only species recorded from eggs of T. nZ and M . sexta L. collected from plantings of tomatoes grown in South- ern California (Oatman et a]. 1983a). On average, 53.4 and 49.5% of T. ni and M . sexta eggs were parasitized by this parasitoid. Roltsch & Mayse (1983) reported that T . ni and M . sexta eggs were commonly parasitized by T . exiguum Pinto & Plat- ner in commercial fresh market tomatoes planted in the spring in Arkansas. Pinto et al. (1978) con- cluded that the distribution of T. semifumatum is limited to Hawaii, and that the name was frequently incorrectly applied to T. pretiosum.

As reported by Oatman et al. (1983a) and Pinto et al. (1986), T . deion and T. pretiosum parasitize eggs o f Trichoplusia spp. and Manduca spp., and T. thalense is known to parasitize T. ni (Pinto & Oatman 1985). Consequently, these lepidopterous species, which are generally of minimal economic importance in processing tomatoes, may act as important alternative hosts for Trichogramma populations in the Sacramento Valley and help ensure that the latter are available to parasitize the eco- nomically more important populations of H . zea that typically occur in late summer. Other alternative host reservoirs, such as weeds and adjacent native or agricultural habitats, may also act as sources of parasitoids.

Because held sampling did not begin until J I I ~ ~ , the abundance and parasitism of T . ni and Mart- duca spp. before this are unknown. Consequently, their importance to early season buildup of Tricho. granima is also unknown. However, the results indicate that during our sampling period, T. ni eggs were most abundant from mid-July through Au- gust (Table 1). The seasonal occurrence of Man- duca spp. eggs was less clear, probably because an insufficient number of eggs was observed.

Parasitism of H . sea. Of 32 H . zea eggs observed in the field in 1981, only 3 of the 6 eggs recorded on the last sample date of the season were parasitized. In 1983, peak percentage of field parasitism of H . zea eggs, based on the 187 eggs observed, ranged from 46 to 100% in four of the five fields sampled (Fig. la-d). In the fifth field, there were only seven eggs recorded, and none was parasitized. The maximum level of actual parasitism of H . zea eggs exceeded 83 % in all fields monitored in 1985 (Fig. 2a-g). Five of the eight fields in 1986 had peak levels of parasitism >62% (Fig. 3a-h). Early harvest of two fields in 1986 precluded sampling later in the season when levels of parasitism may have been higher.

These results indicate that parasitism by naturally occurring populations of Trichogramma is an important mortality factor of H . zea eggs in late- season processing tomatoes grown in the Sacra- mento Valley. These findings are similar to those reported by Graham (1970). He determined that T. semifumatum parasitized up to 74.6% of He- liothis eggs in late summer and fall planted to-b matoes. Oatman & Platner (1971, 1978) reported average levels of parasitism by naturally occurring populations of T . pretiosun to range from 41.4 to 74.9% in unsprayed plantings of tomatoes in South- ern California. Similar results were reported by Roltsch & Mayse (1983), primarily due to T . exiguum. In addition, H . armigera Hubner has been reported to be heavily parasitized by T . rhennna

w - 757 June 1990 HOFFMANN ET AL.: PARASITISM OF Heliothis zea EGGS

a, u

ce 0

0 Z

- l b a - C o l u s a Co. I 1 l o o - 1983 C o l u s a Co. I - % Parasi t ism 75 - --c- White Eggs

50 - - -

/

4 25 - \

- . f . - f l : - - \ - - I I

Y O 1 0 co. c Sutter Co. d

75 1

19 8 28 17 19 8 28 17 Ju ly August Sept . Ju ly August Sep t .

Fig. 1. Field parasitism and abundance of Heltothis zea eggs (presented as l o x observed) in four commercial fields of processing tomatoes during 1983. Sacramento Valley, California.

Voegele & Russo and to a much smaller extent by Telenomus spp. on tomato in Portugal (Meierrose & Aratljo 1986).

In 1983,1985, and 1986, the seasonal occurrence of H . zea eggs was relatively similar. In early to mid-August, H . zea egg densities began to increase and peaked 2 to 3 wk later (Fig. 1-3). This temporal distribution is similar to that reported for H . zea adults captured in blacklight traps and coincides with the greatest potential for fruit damage (Lange & Bronson 1981). A small percentage of the H . zea eggs \\ere either infertile or apparently were killed in the handling process. Infertile eggs accounted for 1.7 and 5.9% of the H. zea eggs recorded in 1985 and 1986, respectively. Eggs, which did not fall into any definable category and were presumed to have been killed in the handling process, accounted for 2.5 and 3.0!%, respectively.

These results demonstrate that a large percentage of the white eggs observed in the field are parasitized, but because of the time required (4 d) for parasitized eggs to turn dark, they arecurrently considered viable. Consequently, the treatment threshold, \vhich is based on the abundance of H . zea eggs, is conservative and may be modified to include mortality due to Trichogramma. Current- ly, field samplers record only white H . zea eggs found in samples of 30 tomato leaves. By estimating the percentage of these eggs that are actually parasitized, the threshold can be adjusted.

The ratio of black to white eggs per 30 leaves can be used to estimate the percentage of white

eggs that are parasitized (actual parasitism). The relationship between the ratio of black to white H. zea eggs as recorded in the field and actual parasitism (Fig. 4) fit the following model:

Pa = 76.2b:w/(0.03 + b:w), (r2 = 0.93, P < 0.01, n = 34) (2)

where P, is actual parasitism, and b:w is the ratio of black to white H . zeu eggs recorded in a field sample. The best fit was determined using the Mar- quardt iterative approach (SAS Institute 1985,584- 586). All observations from 1985 and 1986 before late-season insecticide sprays were included.

As described in the current IPM program for processing tomatoes, if four white H. zea eggs are recorded in a 30-tomato leaf sample, an insecticide application is recommended. If when using the new proposed protocol, a field sampler records one black and four white eggs, approximately 70% of the white eggs are parasitized (Fig. 4). Conserva- tively (rounding to the next lowest whole number), only two of the four eggs are viable. Under these conditions, and using the equation:

T, = 4/(0.01(100 - [76.2b:w/(0.03 + b:w)l)) (3) where T, is the new threshold and 4 is the current threshold, the treatment threshold can be increased to 12 (rounded to next lowest whole number) white eggs per 30-leaf sample. Table 2 depicts a range of black/white ratios of H . t ea eggs and the modified thresholds. A modified version of this table could be used by pest managers to adjust treatment

758 ENVIRONMENTAL ENTOMOLOGY Vel. 19, no. 3

- b a Freder ick Eas t

I

28 17 19 8 19 8 28 17 July August Sept. July August Sept.

m Q, > m a, -I

0 M \ m CT, m w a,

ce 0

0 z L 0

E m c-, ._. .C

a

100

75

50

25

0 . .

July August Sept. J u l y August Sept.

r

100 - He idr lck Rd. 98 e - f He idr lck Rd. 99 Spray Aug. 23 I

19 8 28 17 19 8 28 17 J u l y August Sept. July August Sept.

100

75

50

25

h 19 8 28 17

J u l y August Sept. Fig. 2. Percentage of actual parasitism and abundance of Heltothts t ea eggs (presented as 1Ox observed)

recorded in commercial fields of processing tomatoes during 1985. Fields are identified by grower's name. An arrow indicates date of application.

759 June 1990 HOFFMANN ET AL.: PARASITISM OF Heliothis zea EGGS

O0-

75 b 1986 B u t t o n & Turkov ich - % Parasit ism Spray July 21

---e--- Whi te eggs Spray Ju ly 21

a - Davey Rd. 1 13

50 - 25 -

t

I

1

I 41 -

0

a, m e,

0 M cn m W a,

> l o o -

-1 7 5 -

\ 5 0 -

O’ 25-

.e 0

0 z

-

c ’ He id r i c k Rd. 102 d Davey Pedr i ck Rd.

- -

- I - - - - I I

L 0

E tn c.,

m m

.C

.-

2 160- 6e

120-

80 -

L m

Meek g - He id r i c k Rd. 22 h / ‘\ I I I

I

a m 3

c

19 8 28 17 19 8 28 17 J u l y August Sept. July Augus t Sept.

e - M a r t i n e l l i f 100- Kentucky Ave. Spray Aug. 8 Spray Ju ly 24

75 -

50 -

I

19 8 28 17 19 8 28 17 July August Sept. July Augus t Sept.

- -.---1w,.-* .̂ - - _/------ - -- -7

760 ENVIRONMENTAL ENTOMOLOGY Vol. 19, no. 3

h g 100-

-e ,c - - - - - - - - - - --- ------ - -: .....................

- I *. 25 -$ Pa I 76.2b:w/(0.03 + b:w)

.- --. 95% Confidence Limits

0 2

1 . 1

8 0.0 0 . 5 1 .0 1 . 5 2 . 0 2.5

Ratio of Black:White Eggs (b:w)

Fig. 4. Relationship between the ratio of black and white Heliothis zea eggs as observed in the field and actual parasitism during 1985 and 1986.

decisions based on field records of black and white eggs.

Black H. zea eggs were recorded in all fields sampled before or without insecticide applications in 1985 and 1986. However, they were only present in 44.7 9% of the samples. In the absence of black H. zea eggs, an alternative procedure to estimate actual parasitism would be to collect and observe the white eggs recorded when at or above the treatment threshold. Within a practical time frame (48 h) for a management decision to be made, those H . zeu eggs that turn black, indicating parasitism, would be subtracted from the treatment threshold using the following equation:

E, = E, - E, (4)

where E, = the adjusted number of viable eggs, E, = the number of white H. zea eggs (four or more) collected in the field sample of 30 tomato leaves, and Eb = the number of the field-collected eggs that turn black in the 48-h period. Egg Abundance and Fruit Quality at Harvest.

Fruit quality samples taken from fields near harvest during 1985 and 1986 (Table 3) provided additional evidence that the current H. zea egg treatment threshold could be increased if the effect of Trichogramma were considered. In 10 of the 15 fields, the number of white eggs recorded was near or exceeded the recommended treatment level of four per 30 leaves and several of these fields were not treated with insecticide. Yet only in the Hei-

drick Rd. 22 field, which \Cas abandoned (because of poor market conditions) and not treated with insecticide, was fruit damage excessive (Table 3). Although the rejection level of harvested loads at grading stations is 2%, damage levels in the field can exceed this amount because 75% of damaged fruit is lost or discarded in the harvest and transport process (F.G.Z. et al., unpublished data). Damage in the field could be 4%, but only 1% would be recorded at the grading station. I n addition, tilc fruit damage levels recorded at harvest in these fields overestimate damage by 62%, because of GI, inherent bias associated with sampling of frui t (Wilson et al. 1983). Consequently, with the ception of the Heidrick Rd. 22 field, all fields had <2% within-field damage.

Further support, and perhaps the most convirlc- ing from the producers’ standpoint, for increasirlg the H . zea egg threshold comes from tomato f ru i t quality grades recorded from harvested loads of tomatoes at official grading stations. All harvestetl loads were found to be at acceptable worm damage levels with only t\vo loads reaching the 1% level (Table 3). These grades include damage by all species of lepidopterous larvae; thus, the actual damage due specifically to H. zeu could have been < I % . Loads with grades ~ 2 % would be rejected.

Influence of Insecticide Treatments. Informa- tion concerning the insecticide applications made to fields in 1981 and 1983 was not available. In 1985, the Davey, Walker, and Meek fields were each treated once with fenvalerate on 19 July, 20 July, and 1 August, respectively, for control of ar- myworms, before the late season increase in H. zea egg abundance. Fields treated specifically for H . zea infestations included the following: Frederick East and West (25 August, fenvalerate), Meek (27 August, fenvalerate), Heidrick Rd. 99 (23 August, fenvalerate + methomyl) and Walker (24 August, fenvalerate + methomyl). The applications made specifically for control of H. zea resulted in an average 46.9 (SD = 16.6)% reduction i n parasitism of H. zea eggs, whereas parasitism increased 23.0 (SD = 17.45)% during a similar time period in untreated fields (Fig. 2). This difference was significant (P < 0.01). In most instances, parasitism returned to near prespray levels 1 to 2 wk later.

In 1986, no insecticides were applied specifically for late-season H. zeu infestations. However, the following fields were treated earlier in the season

Table 2. Partial field chart for adjusting Heliothis sea treatment threshold based on ratio of black to white eggs present in field samples of tomato leaves

White eggs

4 5 6 7 a 9 10 1 1 12 13 14 15 Black eggs

1 12 1 1 11 10 10 9 9 9 8 8 8 8 2 14 13 13 12 12 12 11 11 1 1 10 10 10 3 14 14 14 13 13 13 12 12 12 12 11 1 1 4 15 15 * 14 14 14 13 13 13 13 12 12 12 5 15 15 15 14 14 14 14 13 13 13 13 13

Bold-faced numbers indicate egg density at which treatment is recommerided

-. _ _ - --- --- .. ___.

June 1990 HOFFMANN ET AL.: PARASITISM OF HeliOthiS zea EGGS 761

Table 3. Maximum egg densities for Heliothis zea during 1985 and 1986 seasons and tomato fruit quality at harvest

Max. no. white" Insecticideb ' fruit Harvested loads/grade (%)" Field applied with H. tea

30 eggs/ leaves damage 0 Trace 0.5 1.0

1985 Davey 2.4 No 3.0 All Frederick (E) 9.4 Yes 0.6 Not harvestedd Frederick ( W ) 10.8 Yes 2.0 All Meek 3.6 Yes 0.3 All Heidrick Rd. 99 5.3 Yes 0.0 61 7 Heidrick Rd. 98 3.9 No 1.8 87 15 6 1 Walker 11.2 Yes 0.4 70 5

- -

- -

1986 Button & Turkovich Davey Rd. 113 Davey Pedrick Rd. Heidrick Rd. 102 Heidrick Rd. 22 Kentucky Ave. Martinelli Meek

4.8 No 1.6 No 3.9 No 1.5 No

16.9 No 4.6 No 3.7 No 3.9 No

1.3 0.3 1.4 0.2 7.6 0.2 1.7 3.1

57 19 1 1 1 19 7 1

Not harvested 176e 2 - -

Not harvested

- 5 1 - 39 7 1 -

-

- - - -

(1 Based on a sample of up to 540 leaves per field. b Insecticide applications for control of H. lea made within 4 d following maximum egg count. 'State of California grade categories expressed as percent of load by weight with insects, insect parts or direct insect damage (all

d Not harvested because of market conditions, not because of H. sea damage. species). Typical load weight is 22.7 t .

Trace grades included in 0% grade category.

for other pest species: Button and Turkovich (21 July, fenvalerate + parathion + methamidophos), Davey Hd. 113 (21 July, parathion), Martinelli (24 July, methomj.1) and Kentucky Ave. (8 August, endosulfan + carbaryl).

Levels of H . ;ea egg parasitism in the Kentucky Ave. field were lower than other fields monitored in 1986 (Fig. 3e). This may have resulted from the application of carbaryl, which has been shown to be extremely toxic to Triclzogramma adults and developing immatures on cotton (Stern 1963). It also has a long period of persistent toxicity (Dutt & Somchoudhury 1980).

If the population density of H. zea eggs were assumed to remain relatively constant over the period of the above-discussed comparison, then the reduction in potential (actual) parasitism resulting from the insecticide applications can be estimated using the following equation:

where T, = percent reduction in potential actual parasitism, P,,,, and = mean percent actual parasitism in sprayed fields just before and on first observation following insecticide treatments respectively, and SP, = the mean change in actual parasitism in unsprayed fields. Based on the pre- and post-insecticide records of actual parasitism from 1985, the insecticide applications resulted in a 67.7% relative reduction in potential (actual) parasitism of H. zea eggs by Triclzogramma.

These results show that the insecticide applications made in late season, when H . zea eggs are most abundant, may reduce H . zea egg parasitism. Although difficult to discern from these studies, it

would be interesting to learn if early-season applications of insecticides for other pest species affect the level of H . =ea egg parasitism later in the season. The effect of both the early- and late-season applications may have been moderated by movement of adult Triclzogramma into fields following insecticide applications. Tricltogramma are capa- ble of rapid dispersal (see review by Keller et ai. 1985). The emergence of Trichogramma from eggs parasitized before insecticide applications could be another moderating factor. When contained within a host egg, developing Trichogramma are less sus- ceptible to most insecticides (Bull & Coleman 1985). In addition, adult Trichogramma may be concen- trating in late-season fields of processing tomatoes because the availability of other suitable host crops at this time of the year is rapidly declining due to maturation or harvest.

In addition to the above-mentioned factors, method of application, type of insecticide applied, and time of application may also affect the effect that insecticides have on Trichogranzma. Oatman et al. (1983b) and Meierrose & Arafijo (1986) showed insecticide applications resulted i n decreases in parasitism of Heliothis spp. eggs. However, Roltsch & Mayse (1983) reported conflicting results, and Graham (1970) found little decrease in parasitism after three applications of the chlorinated hydro- carbon, TDE. Microbial insecticides appear to have little direct effect on parasitism rates (Oatman et al. 1983b). Fenvalarate, frequently used for control of H . zea in processing tomatoes in the Sacramento Valley, was shown to be one of the least detrimental to emerging adult T. brasiliensis Ashmead (Varma & Singh 1987).

~ - _ _ . c --

762 ENVIRONMENTAL ENTOMOLOG~ V O ~ . 19, no, 3

Because actual parasitism decreases following insecticide applications, use of the ratio of black/ white eggs to predict actual parasitism following insecticide applicatiotis m a y be inappropriate. However, there is normally only one insecticide application macle for late-season H. zea control, usually being the last application of the season before harvest.

I m pI ern e n t a t i on. I+fore t he implement at ion of the current 11’M program for processing tomatoes, an average of 1.9 insecticicle applications were m a d e to fields per season in the Sacramento Valley (Flint h K l o ~ i s k y 1985). In ip~emen ta t ion of the program resiiltetl in a 40% reduction in the number of insecticicle applications, a n d i t was estimated that growers saved $17.54/ha ($y.lO/acre) over pre- IFkl control costs for lepidopterous pests (Antle & l’ark 1986). Fifty-seven percent of the producers in the Sacramento Valley e i ther adopted or adapt- ed the program by 1986 (Crieshop e t al. 1988).

Ostlie & Pedigo (1987) noted that current economic thresholds f requent ly ingore the contribu- tion of natural enemies to pest mortali ty. The results presented in this pape r appea r to be the first example of a mortali ty factor, due to a parasitoid, being directly incorporated in to an economic threshold. Because linkages between researchers, extension and pest managers developed dur ing the implementation of the original processing tomato IPM program already exist, field validation and implementation of the modified IPM program will be greatly facilitated.

A combination of alternative insect hosts a n d relatively low insecticide use apparent ly provides the appropr ia te environment for Trichogramma to have a n important impact on H . zea populations in late-season processing tomatoes. Incorporation of this mortality factor into the cu r ren t t rea tment threshold has the potential to fu r the r reduce the number of insecticide applications required for H . zea control in processing tomatoes grown in the Sacraniento Valley of California.

Acknowledgment

The authors acknowledge Les Ehler, Earl Oatman, and the anonymous reviewers for critical review of an earlier draft of this manuscript. We also wish to acknowledge the assistance of Earl Oatman, Department of Entomology, University of California, Riverside, for identification of Trichogramma specimens, the various tomato growers for the use of their fields, and C. Weak- ley, E. Chin, L. Hesler, G. Routh, S. Klienhaus, and D. Jones for their efforts i n the laboratory and/or field. This research was supported i n part by the University of Cal- ifornia Statewide IPM Program.

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Received for publication 10 April 1989; accepted 6 October 1989.

Documents

U Tomatoes in the-Sacramento Valley of California · Infor- mation on insecticide applications to the 1981 and 1983 fields was not available. 1985- 1986 Fields. Fields of commercial