Integrated Control of Diamondback Moth and Other Insect Pests Using

Integrated Control of Diamondback Moth and Other Insect Pests Using an Overhead Sprinkler System, an Insecticide, and Biological Control Agents, on a Watercress Farm in Hawaii Larry M. Nakahara, John J. McHugh, Jr.¹, Clarence K. Otsuka, George Y. Funasaki, and Po-Yung Lai Hawaii Department of Agriculture, P 0 Box 22159, Honolulu, Hawaii 96822. ¹Sumida Farm Inc., P 0 Box 146, Aiea, Hawaii 96701, USA

Abstract

The diamondback moth, Plutella xylostella (Linnaeus), was effectively and economically controlled on a 3.84 ha commercial watercress farm at Aiea, Oahu, Hawaii, through the implementation of an overhead sprinkler irrigation system and the establishment of a larval parasite, Cotesia plutellae (Kurdjumov). The intermittent application of water on the watercress field during the early evening hours is believed to disrupt the mating and oviposition activities of diamondback moth adults. The grass sharpshooter, Draeculacephala minerva Ball, thrived in the new environment created by the sprinkler system but was easily controlled with several timely applications of diazinon. The cotton aphid, Aphis gossypii Glover; the green peach aphid, Myzus persicae (Sulzer);the turnip aphid, Hyadaphis erysimi (Kaltenbach); and a recent aphid immigrant, Aphis nasturtii Kaltenbach, were effectively controlled by established predators and timely applications of diazinon. The integrated system to control the diamondback moth and other insect pests of watercress was commercially cost effective. Chemical control Costs were reduced by 89%, while production increased by 93%.

Introduction

The diamondback moth (DBM), Plutella xylostella (Linnaeus) (Lepidoptera: Yponomeutidae), has been established in Hawaii since about 1892 (Zimmerman 1978). It is a major insect pest of crucifers in Hawaii, occasionally causing considerable damage to various commercial crops, including cabbage, Brassica oleracea var capitata; broccoli, B. oleracea var botrytis subvar italica; mustard, B. juncea; Chinese cabbage, B. campestris ssp pekinensis; white-stem cabbage, B. campestris ssp chinensis; radish, Raphanus sativus var longipinnatus; and watercress, Nasturtium officinale. DBM larvae damage watercress by feeding on the leafy portions, petioles, stems, and terminals of the plant. Watercress is an aquatic perennial vegetable crop native to Europe and Asia Minor. Most of Hawaii's watercress crop is grown on the island of Oahu in the Aiea, Pearl City, and Waipahu districts bordering Pearl Harbor, where the supply of spring and artesian well water is plentiful. Watercress is grown in shallow ponds or beds of water and large quantities of clean, continuously flowing water are essential for production. Water temperatures above 25.5°C cause slow or poor growth. Optimum day time air temperatures are 21-29°C. Therefore, optimum watercress growing conditions occur during the cool winter season in Hawaii (McHugh et al 1981). 404 Nakahara, McHugh, Otsuka, Funasaki, and Lai

Periodic surveys conducted during 1976-1980 showed that the major pests affecting watercress were DBM; green peach aphid, Myzus persicae (Sulzer) (Homoptera: Aphididae); and broad mite, Polyphagotarsonemus latus (Banks) (Acari: Tarsonemidae). For many years, efforts to control DBM infestations on watercress with insecticides were moderately effective. During 1982, however, DBM infestations increased considerably in watercress fields on Oahu resulting in a greater usage of insecticides by growers. Despite the use of insecticides one or more times a week, DBM infestations and damage were heavy on most watercress plantings by the spring of 1982 (Nakahara and Lai 1983). The apparent ineffectiveness of registered insecticides against DBM prompted an increased usage of these chemicals on watercress. As a result, unacceptable residue levels of two registered insecticides, diazinon and endosulfan, were discovered on watercress by State of Hawaii Health and Agriculture officials and five Oahu farms were ordered to halt their harvests in May and June 1982. In September and October 1982, watercress was again recalled from two Oahu farms due to excessive endosulfan residues. The resulting adverse publicity over excessive insecticide usage caused many consumers to refrain from purchasing watercress. This prompted growers to seek other means of controlling DBM populations. The Hawaii Department of Agriculture (HDOA) had been introducing, mass- rearing, and releasing various parasites to control DBM infestations for several years. Previous attempts to establish a DBM larval parasite, Cotesia (=Apanteles) plutellae (Kurdjumov) (Hymenoptera: Braconidae) (Mason 1981), in Hawaii during 1972-1974 from Taiwan and Trinidad were unsuccessful. In November 1980, the Trinidad strain of C. plutellae was re-introduced through the courtesy of the Commonwealth Institute of Biological Control in Trinidad, West Indies, and efforts were made to establish the species on the islands of Maui, Kauai, and Hawaii in DBM infested cabbage fields. Releases were made primarily in large, commercial cabbage fields where insecticides were being applied for DBM control. In August 1982, the HDOA began releasing C. plutellae in watercress fields on Oahu. Earlier, it was observed that watercress grown under an overhead water sprinkler system provided favorable growing conditions through evaporative cooling (McHugh and Nishimoto 1980). It was later found that watercress treated in this way also sustained very little damage from adjacent high DBM populations. As plans were made to install the sprinkler system throughout the farm, an insect monitoring program was developed by the HDOA for a portion of the watercress farm in Aiea. We report herewith results of the studies on the effectiveness of integrated methods to control DBM and other insect pests in the watercress planting.

Materials and Methods

The study was conducted during 1982-1983 on a 3.84 ha watercress farm at Aiea, Oahu. The farm was bordered to the south by a highway and to the northeast by another farm producing taro, Colocasia esculenta var antiquorum. A major shopping center surrounded the watercress and taro farms along the eastern, northern, and western sectors. Although various fruit trees, vegetables, ornamentals, and weedy grasses were found along the watercress farm’s perimeter, none was known host of DBM. The watercress farm was divided into 100 smaller ponds or beds, each approximately 12.2 x 24.4 m. Dikes made of 20 x 20 x 40 cm hollow concrete tiles encompassed each bed to regulate water flow and to provide a footpath for access to beds. Samples were initially collected from five beds (about 0.1 ha) adjacent to the highway where no insecticides were applied. Insecticide treatments continued on remaining beds until the sprinkler system was in operation. Subsequently, all insecticide treatments were temporarily Integrated Control of DBM in Hawaii 405 discontinued throughout the farm and the sampling area was increased to include the 14 beds (about 0.4 ha) adjacent to the highway. C. plutellae was first released in the watercress planting on 31 August 1982 and continued at weekly intervals throughout the year. In December 1982, a Taiwan strain of C. plutellae was introduced through the courtesy of the Taiwan Agricultural Research Institute, Taichung, Taiwan, and was subsequently released in February 1983 in various Oahu watercress plantings. In May 1983, rearing of the Trinidad strain was discontinued in favor of the more aggressive and productive Taiwan strain. Weekly releases of the Taiwan strain continued in watercress plantings until August 1983. On 31 August 1982, weekly insect surveys were initiated in the 0.1 ha sampling site. To determine the recovery, establishment, and effectiveness of C. plutellae in the field, 50 4th instar DBM larvae were randomly collected each week after carefully searching insecticide-free areas of the study site. The DBM larvae were brought to the laboratory and reared on insecticide-free watercress until adult emergence. The number of C. plutellae cocoons and adults which emerged from the 50 DBM larvae collected each week was recorded to determine rate of parasitism. This procedure was discontinued when DBM larvae became scarce and difficult to find in the field. Modified sweep net samples were collected weekly from 21 September 1982 to determine abundance of pests and predators (Delong 1932, Rudd and Jensen 1977). Insects and other arthropods were collected with a beating net. Five samples, each consisting of 20 consecutive sweeps with a 30.5 cm diameter beating net equipped with a cone-shaped unbleached muslin bag, were collected each week. Each sample was collected by swinging the net across the canopy of the watercress with sufficient force so that the bottom edge of the net passed slightly above the water line. The force of the net had a beating affect on the watercress, parts of which broke off and became part of the sample. The sampling area was confined to one section of the farm as the sampling method was temporarily destructive to the watercress plants. The net was swung perpendicular to the path of the sampler while walking diagonally across a watercress bed. Five beds with watercress plants at least 20 cm above the water line were randomly sampled each week. The entire contents of each sample, which consisted of various arthropods and plant parts, were placed in a 15.2 x 7.6 x 38.1 cm polyethylene bag with the top loosely tied. After the implementation of the sprinkler system, the wet contents of the beating net were further rinsed in the field. The wash was collected and examined separately for smaller individuals which adhered to the wet net. Samples were processed immediately after collection or frozen for later examination. All samples were collected at mid-morning between 9:00 AM and 10:00 AM under light wind conditions. In the laboratory, each bag was filled with about 250 ml soapy water containing 0.2-0.3 ml of Crystal White detergent and shaken vigorously for several seconds. The contents were then emptied into a 35.6 x 30.5 x 12.7 cm white plastic pan. The bag was rinsed three more times with water and the contents added to the pan. Vegetation and other debris were removed and the pan contents were examined with a headvisor magnifier and a dissecting microscope. Specimens were segregated in vials, identified, and counted. Initially, all beds except for those in the sampling area were treated with combinations of methomyl (0.56 kg AI/ha), diazinon (0.56 kg AI/ha), and Bacillus thuringiensis Berliner (Thuricide HPC at 2.3 l/ha) one to two times/week. Despite these treatments, DBM infestations and damage increased and production declined. All insecticide treatments were temporarily discontinued on the farm on 16 November 1982. Later, as other pest problems developed, limited usage of diazinon was incorporated into the control program. On 2 December 1982, an intermittent overhead sprinkler irrigation system was put into operation at the watercress farm to replace the use of insecticides. Unlike 406 Nakahara, McHugh, Otsuka, Funasaki, and Lai chemigation (Chalfant and Young 1982), the system discharged only water as a means of controlling DBM. The 3.84 ha field was divided into seven sections with two to three valves/section. The valves were either 5.08 or 7.62 cm diameter electrically actuated Richdel valves. Each valve controlled the flow of water of 8 to 14 sprinkler heads. In each section, water was allowed to discharge for 5 min at 30 min intervals. The cycle was repeated throughout the day from 8:00 AM to as late as 10.00 PM. A Dramm Rain Robot 14 Station Controller was used to set sprinkler duration. In this operation, runoff water from the watercress field was recirculated through the sprinkler system. A Berkeley B-3 TPM 15 horsepower pump, powered by a 240 volt three phase General Electric Tri Clad motor, spinning at 3500 rpm, was used to pump water from a collection basin and move it through the sprinkler system at a maximum of 1514 1/min and at an operating pressure of 4.17 kg/cm². A spot Systems Screen filter, SMS 8-36-7, with two 75-mesh stainless steel screens and a manual backwash for cleaning, was incorporated into the main line for filtering organic material and other debris which could cause clogging of the sprinkler heads. Two types of sprinkler heads were installed. Full circle Weather Tec 10-30 impact heads, with a main orifice of 0.4 cm and a back jet orifice of 0.24 cm, were used in the interior portion of the field. Part Circle Weather Tec 15-20 impact heads, with an orifice of 0.44 cm, were used along the perimeter. Water was discharged at the rate of 28.6 1/min and 24.9 1/min for the Full Circle and Part Circle heads, respectively. A total of 212 sprinklers were spaced 12.2 m apart in the farm. Sprinkled water overlap was 90-100%. All pipes used were class 200 Polyvinylchloride (PVC) plastic. Pipe diameters ranged from 1.9 to 15.2 cm. Pressure relief and air relief valves were incorporated into the main line at four different locations.

Results and Discussion DBM

DBM infestations in watercress were apparently more difficult to control in 1982 than in previous years. Increased resistance to available insecticides and favorable environmental conditions may have been contributing factors. During 1980-1981, other vegetable farmers in Hawaii had experienced greater difficulty in controlling DBM resulting in an emergency registration of Pydrin. Although Pydrin was effective in controlling DBM populations, it was not registered for use on watercress. In addition, an unusually wet winter followed by a wet summer may have contributed to DBM increase due to the increased availability of adult food sources, primarily flowering weeds, near watercress farms. Total rainfall at nearby Waipahu Sugar Company was 742 mm (2.7 times above normal) during the period December 1981 to April 1982 and 137 mm (1.9 times above normal) during the period May to September 1982 (NOAA 1981, 1982). DBM populations and damage were high when the study was initiated. The number of DBM individuals collected in samples reached peak numbers of 155.6 larvae/20 sweeps on 13 October 1982 and 22.8 adults/20 sweeps two weeks later (Figure 1). Adult numbers declined to 0.4 individuals/20 sweeps on 4 November 1982 following heavy rains from 26 to 28 October 1982. Insecticides (methomyl, diazinon, and Thuricide HPC) appeared to be ineffective in controlling DBM infestations in non-surveyed beds and all treatments were discontinued on the entire farm on 16 November 1982. Watercress production declined considerably as plants in most ponds were severely damaged. Harvesting was discontinued for the next four weeks. With a reduction in the availability of watercress, DBM larval counts also declined with peak counts occurring at three to four-week intervals. Integrated Control of DBM in Hawaii 407

DBM adults DBM larvae C.plutellae (parasite) adults

Overhead sprinkler system 0:00 am 10:00pm

1982 1983 Figure 1. DBM adult and larval populations in relation to C. plutellae adult populations and an overhead water sprinkler system during 1982 and 1983 in watercress at Aiea, Oahu, Hawaii. Dashes indicate portions of the sprinkler system were turned off during this period

On 2 December 1982, the intermittent overhead sprinkler system began discharging water daily on the entire farm from 8:00 AM to 6:00 PM. DBM larval counts persisted at damaging levels and the operation of the sprinkler system was extended to 10:00 PM from 23 December 1983. The DBM population subsequently declined. No DBM adults and larvae were collected in samples between 8 February to 25 July 1983 and between 1 February and 28 June 1983, respectively. During mid-June to early September, treatment by the sprinkler system was reduced to only selected areas of the farm. The system was turned off for several days at a time on ponds requiring maintenance. All ponds were cleared of debris that had accumulated over a period of two years and prepared for replanting. DBM adults and larvae were recovered during this period and persisted until sampling was discontinued in November 1983. The overhead sprinkler system was very effective in reducing DBM infestations. Operation of the overhead sprinkler system during the daytime creates favorable growing conditions for the watercress. However, leaving the sprinkler system on from dusk through the early evening hours is believed to disrupt the mating and oviposition activities of DBM adults. According to Harcourt (1957), mating begins at dusk on the day of emergence. Oviposition begins shortly after dusk, reaching a peak two hours later. In addition, droplets of water discharged through the system may contribute to adult and larval mortality by knocking individuals off the plants and into the ponds causing them to drown. Heavy rainfall may also contribute to adult mortality as suggested by the decline in DBM adults on 4 November 1982 following heavy rains (210 mm recorded at Waipahu Sugar Company) during the three-day period in late October. Since the entire farm was treated with the overhead sprinkler system, no comparisons could be made with untreated watercress. Efforts to establish control sites on other nearby watercress farms were unsuccessful as other growers quickly adopted the new technology and converted their operations to include overhead sprinkler systems. 408 Nakahara, McHugh, Otsuka, Funasaki, and Lai

Surveys of other farms indicated that farm size may also be an important factor in obtaining DBM control with overhead sprinkler systems. DBM control was more effective on the 3.84 ha farm than on smaller plantings, some as small as 0.1 ha. The smaller plantings had a high incidence of flowering weeds which may have served as refuge and food sources for DBM adults. Weeds growing along the farm perimeters were more accessible to DBM adults on small farms than on large farms. In addition, the 3.84 ha farm used concrete hollow-tile banks that remained weed-free. On other farms where earthen banks were used to separate beds, weed control was difficult. A total of 28,355 C. plutellae adults was released in watercress fields around the Pearl Harbor Basin area during the study. Most of the Trinidad strain (10,519 adults) and only 480 adults of the Taiwan strain were actually released in the study site. Of the 950 DBM larvae held in the lab from the weekly collections, C. plutellae was the only DBM parasite recovered despite the establishment of another DBM parasite, Diadegma insularis (Cresson), on other vegetable crops on the island. DBM larvae parasitized by C. plutellae, were first recovered three weeks after the parasite’s initial release. Parasitism rate during September through December 1982 ranged from 0-1 7% (average 5%). No DBM larvae were sampled for parasites during 1983 due to very low DBM populations in the field. Efforts to collect 4th instar DBM larvae during September 1983 were also unsuccessful due to insufficient numbers. C. plutellae adults were periodically recovered in low numbers by sweepings from 13 October 1982 to 16 November 1982 (Figure 1). Thereafter, no adults were collected until 20 September 1983 when adults were again recovered in sweep net samples. C. plutellae adults were recovered weekly until the study was terminated in November 1983. Although C. plutellae was not effective in controlling DBM from September to December 1982, parasite abundance during September to November 1983 suggests otherwise. The ratio of adult parasites collected versus DBM larvae collected was 14 times higher during the latter period (1 parasite:7 DBM larvae) as compared to the former (1 parasite:100 DBM larvae). The increase in parasite activity in 1983 may be due to the subsequent establishment of the Taiwan strain in the Pearl Harbor Basin area. The low incidence of C. plutellae in 1982 samples suggests that lab-reared adults and first generation progeny may have been the primary constituents of these recoveries since Trinidad parasite releases were being made concurrently. C. plutellae establishment and increase were also noticeable in other watercress farms in the Pearl Harbor Basin following the release of the Taiwan strain in 1983. In addition to the overhead sprinkler system and C. plutellae, a granulosis virus also affected DBM larvae. Observations in the field and the laboratory suggest that granulosis virus may be a contributing factor to DBM control in Hawaiian watercress.

Grass Sharpshooter

Adults of the grass sharpshooter (GSS), Draeculacephala minerva Ball (Homoptera: Cicadellidae), were first recovered from sweep net samples on 24 January 1983. Later, GSS nymphs were collected on 9 March 1983. GSS infestations increased rapidly during the next two months as efforts to control the populations without the use of insecticides were pursued (Figure 2). Alternative control methods were sought to take advantage of the marketing strategy of producing a pesticide-free product. Initial trials using a surfactant solution (Triton B-1956) were not effective in controlling GSS. GSS reached a peak of 78.6 adults and 166.4 nymphs/20 sweeps on 10 May and 17 May 1983, respectively. On 23 May 1983, the first of three primary applications of diazinon was made on the watercress. Each primary treatment was followed by a secondary application of diazinon two to three weeks later as surveys and lab studies indicated that most of the GSS 1st instar nymphs had emerged from eggs deposited in the watercress stems Integrated Control of DBM in Hawaii 409

0 Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov 1982 1983 Figure 2. GSS adult and nymphal populations in relation to insecticide applications (arrows) during 1982 and 1983 in watercress at Aiea, Oahu, Hawaii and petioles by that time. GSS eggs did not appear to be affected by the diazinon treatments. A total of five applications were made each at the rate of 0.56 kg AI/ha using ground power sprayer equipment. The overhead sprinkler system was turned off during each insecticide treatment and remained off for about 24 h. Beds scheduled for harvesting were left untreated. Primary treatments on 3 August and 1 November 1983 were initiated when counts of GSS exceeded an economic injury level of 20 nymphs/20 sweeps. GSS damage to new growths of watercress was first noticeable in mid-April 1983 and reached a peak by mid-June. Symptoms started with a slight wrinkling of the leaves, followed by interveinal mottling, and ended with the entire leaf turning yellow and dropping prematurely. Similar symptoms were reported by Holdaway (1945) following a serious outbreak of GSS on Oahu during September 1944. He noted crinkling of the young leaves, yellow blotches on less mature leaves, and a general yellowing of the older leaves. Holdaway also reported that this injury was associated with GSS infestations and ceased when the leafhoppers were brought under control. As with the GSS outbreak described by Holdaway, damage was greatly reduced in the study site as GSS was brought under control by diazinon treatments. Damage is believed to be directly related to feeding injury rather than to a disease. Although turnip mosaic virus was recovered from many samples showing the mottling symptoms, it was also recovered from plants displaying no symptoms. Since watercress is grown vegetatively, most plants may be symptomless carriers of the virus. GSS may have thrived in the new watercress environment created by the overhead sprinkler system because of the dramatic reduction in pesticide usage on the watercress. Few GSS were recovered in surveys conducted in grasses along the perimeter of the farm indicating that the large population of GSS was due to its breeding in the watercress. Since no GSS parasites were recovered in watercress throughout the study, the absence of natural enemies may also have been a factor in the increase. This is consistent with the observations of Napompeth and Nishida (1971) who suggest that established egg parasites in Hawaii do not attack the GSS when it infests watercress.

Aphids

Aphids feed on the terminals and leaves of watercress causing crinkling and stunting damage which affects the quality and yield of the product. Several species of aphids were found on the watercress during this study, while previous surveys during 1976-1980 410 Nakahara, McHugh, Otsuka, Funasaki, and Lai showed only the green peach aphid, M. persicae, to be the predominant aphid pest. In this study, the cotton aphid, Aphis gossypii Glover (Homoptera: Aphididae), was the predominant aphid followed by M. persicae; the turnip aphid, Hyadaphis erysimi (Kaltenbach) Homoptera: Aphididae); and a recent immigrant, Aphis nasturtii Kaltenbach (Homoptera: Aphididae). The increase in aphid diversity is believed to be due to the reduction of insecticide use in the planting which allowed other species of aphids to become established. No aphids, for example, were collected in samples during 1982 when frequent insecticide applications were made to control DBM. Aphids were first collected in sweep net samples on 24 January 1983 (Figure 3). The counts remained low until late February. The number of aphids collected in samples increased rapidly during March accompanied by a rise in the number of aphid predators (syrphid and coccinellid larvae). A decline in aphid counts on 12 April 1983 suggests that predators, primarily syrphid larvae, were responsible for the reduction in aphid numbers. The use of diazinon to control GSS populations was also effective in controlling subsequent aphid populations.

Diazinon 1

Aphids Predators

0 I 1982 1983

Figure 3. Aphid populations in relation to predator populations and insecticide applications (arrows) during 1982 and 1983 in watercress at Aiea, Oahu, Hawaii

Several predators were observed preying on aphid colonies. About 72% of the predators collected were larvae of two species of the syrphids, Allograpta obliqua (Say) and Toxomerus marginatus (Say). A. obliqua is a common predator of aphids and whiteflies in Hawaii. Its effectiveness is frequently undermined by the parasite, Ooencyrtus guamensis Fullaway, which parasitizes the larval stage of syrphids. O. guamensis, however, was never recovered in the watercress planting. In addition, several species of coccinellids, constituted about 28% of the total numbers of aphid predators collected in sweep net samples. These were Scymnus loewii Mulsant, Coccinella septempunctata brucki Mulsant, and Brumoides suturalis (Fabricius). Integrated Control of DBM in Hawaii 41 1