N.J. Mills and collaborators L. Dixon, S.C. Welter, R.A. van Steenwyk
As an exotic pest, the codling moth has very few natural enemies in California. The aim of the project is to increase parasitism of the codling moth in pears by importing new parasitoid species from Central Asia. A total of eight different parasitoid species have been acquired from several locations in Central Asia, China and Europe. The three most important parasitoid species, that generate from 30-60% parasitism in Kazakhstan, are currently being field released with a view to establishing them in California. Two of these parasitoids, Liotryphon caudatus and Mastrus ridibundus, are in culture in our insectary to provide greater numbers for field release. Through this project a total of 41,080 individuals of the solitary cocoon parasitoid, L. caudatus, have been field released at 41 locations in California and 95,530 individuals of the gregarious cocoon parasitoid, M. ridibundus, have been field released at 34 locations. Microdus rufipes, a solitary larval parasitoid, that we are unable to culture in the insectary, has also been field released but only 253 have been released at 5 locations. Both of the cocoon parasitoids have been recovered from a number of release sites, and in 1997 we recovered both species in orchards where no in-season releases had taken place, indicating successful overwintering of the parasitoid populations in the field. Of the two cocoon parasitoids, M. ridibundus appears to be most active in pear orchards, generating up to 38% parasitism of the overwintering codling moth in trap bands.
Codling moth, Cydia pomonella (L.), is a key pest in pear production in California. The recent development of multiple resistance to insecticides in codling moth populations has caused growers and researchers to reexamine pear pest management practices. It is unlikely that codling moth management will be able to rely solely on chemical insecticides, whatever products may arise in the future, due to the perennial problem of resistance and the development of secondary pests. A more robust and sustainable management program for codling moth must integrate a range of complementary controls.
Although the codling moth has been known in California for more than 100 years, it is an exotic pest in North America, and does not have a typical natural enemy complex working to maintain a natural balance in the abundance of this pest. As a result its abundance is constrained only by the availability of susceptible fruit and nuts and it continues to exert considerable pressure on pear production in California. In Central Asia, the original home of the codling moth, pears are seldom attacked due to the low level of codling moth pressure in this region. The importation and establishment of specializedparasitoids of the codling moth from its native Central Asian region would help to restore a naturalbalance to codling moth populations in California and contribute significantly to the control of codlingmoth in pear orchards adopting an integrated management program with minimal reliance oninsecticides.
The overall aim of this project is to restore the natural balance in codling moth populations in pear orchards in California through the importation and release of specialized parasitoids from the region of origin of the codling moth in Central Asia. The objectives for the project are:
1: To import the most important parasitoids of the codling moth from Kazakhstan, with the assistance of a collaborator recently established in Almaty.
2: To field release the parasitoid species and monitor their establishment and impact on codling moth in pear orchards in California.
PROCEDURES AND RESULTS
Objective 1. To import the most important parasitoids of the codling moth from Kazakhstan, with the assistance of a collaborator recently established in Almaty.
Foreign Exploration in Kazakhstan
The origin of the codling moth is Central Asia, perhaps Kazakhstan, where apple forests commonly grow in the foothills of the Tien Shan mountains and where specialized parasitoids help to maintain codling moth populations at a low level of abundance (Figure 1). 1 visited this region around Almaty in Kazakhstan from June 24 - July 7, 1997 to collect the two most important parasitoids of the codling moth, the larval parasitoid Microdus rufipes, and the cocoon parasitoid, Mastrus ridibundus, for field release in California pear orchards. There I was able to collaborate with Andrey Slivkin of the Institute of Zoology, Kazakh Academy of Sciences, in the banding of apple trees for trapping parasitized codling moth larvae.
This year the season was not as late as we had experienced in 1996 as the spring temperatures had been warmer than usual. However, after the very large crop of 1996, the fruit set on both the wild apple trees and the experimental orchards was rather less this year. We again searched the wild apple trees for evidence of codling moth attack at the end of the first generation in late June, but were unable to find any strikes. For the last three years we have consistently found very few apples damaged by codling moth in the natural forest trees at this time of the year. It is possible that some further attack occurs later in the year, but wild apples are unlikely to provide a good source for the collection of parasitized codling moth larvae.
From my previous trips to Almaty in 1995 and 1996, it was clear that parasitized codling moth could be more effectively collected from the provenance trial orchards just below the foothills of the Tien Shan mountains. These orchards are situated at elevations between 500 and 1,000 m and comprise a number of different varieties of apple including Star Crimson and Aporte, both of which appear to be more frequently attacked by codling moth than other varieties. Another frequent apple variety in these orchards is the 'Summer' apple which matures in July. However, this latter variety is seldom attacked by codling moth.
We were again successful in sending large rolls of 3 inch-wide corrugated cardboard by air mail to our collaborator, Andrey Slivkin, in Almaty in January 1997. We increased the number of rolls of corrugated banding from 10 to 18 rolls this year and Andrey Slivkin arranged to have trees in five orchards banded in May. All five orchards were new this year and were chosen for susceptible apple varieties, good fruit set and some initial evidence of codling moth attack. One orchard was situated about 50 miles east of Almaty in the town of Chilik, three were around the town of Issyk also to the east of Almaty, and the fifth orchard was in Kaskellen about 10 miles west of Almaty. The Chilik orchard was rather small and only 50 trees had sufficient fruit to warrant banding, but in each of the other four orchards from 200-400 trees were girdled with corrugated cardboard bands in late May.
Fruit damage in these orchards was, in general, very much lower this year than we had seen in previous years. I estimated the percentage of fruit attacked in each orchard to be about 6% at Chilik, 2% (Karakemir), less than 1% (Koktobe) and no visible damage (Issyk) at the three orchards around Issyk, and the orchard in Kaskellen had no detectable damage. The estimated rates of codling moth damage in 1996 were 5% at Issyk and 4% at Kaskellen, although from different orchards. Parasitoids were again observed searching through the orchards for codling moth cocoons to attack, as had been the case in 1996, but the extent of recovery of parasitized larvae from the bands was reduced this year due to the lower abundance of codling moth in the bands.
The bands were removed from the orchards in late June and the codling moth cocoons cut out from the bands for transfer back to our quarantine in Berkeley. The bands from the Kaskellen and the Issyk orchards confirmed our visual observations from the fruit, as no codling moth larvae were recovered. Although the Chilik site had the greatest level of observed fruit damage, the orchard was small and the degree of parasitism seemed to be lower than in other orchards. The best recoveries of parasitoids were from the Karakemir and Koktobe orchards near the town of Issyk.
During my visit to Almaty I also visited the Talgarsky mountain orchard as this is close to some natural apple forests. Although there was no attack of the fruit by codling moth in this orchard, there had been some damage due to leafrollers. There are two leafroller species that occur in orchards in this region, Archips rosanus and Pandemis chondrillana. At the time of my visit the leafrollers were in the pupal stage, but the old egg masses present on the trunks were white and crusty, similar to the fruit tree leafroller, indicating that they were predominantly of P. chondrillana. There were from 0-5 leaf rolls present on a tree in this orchard and in almost every leaf roll there was a parasitoid cocoon. From a collection of about 200 leaf rolls, 42 were empty, 4 contained leafroller pupae, 136 contained cocoons of a Diadegma species, and 18 contained cocoons of other parasitoids. This very high level of parasitism by the Diadegma species is very interesting and indicates some potential for biological control of leafrollers in California. However, the cocoons were heavily attacked by a variety of hyperparasitoids and as yet no adult parasitoids have emerged to determine their identity.
Parasitoids of Codling Moth from Eurasia
A continuous culture of codling moth larvae is maintained in the insectary at the Center for Biological Control in Berkeley, reared on organically-grown thinning apples. Ten to twelve bins of thinning apples are collected in May and stored in a cold room at 2°C before use. Codling moth larvae are reared on apples in enclosed cardboard trays (24 x 24 x 3 inches), with a non-diapausing culture maintained at 25°C and a 16 hr daylength, and a diapausing culture at 20°C and a 12 hr photoperiod. Non-diapausing codling moth larvae are used for the rearing of larval parasitoids, whereas diapausing prepupae can be stored for the rearing of cocoon parasitoids.
The parasitoid species that have been collected through foreign exploration in Europe and Central Asia are presented in Table 1 and those parasitoids held in culture in Berkeley are noted in Table 2. Notes on the more important of these parasitoids are as follows:
Liotryphon caudatus: This solitary ectoparasitoid of cocooned prepupal codling moth has been maintained in culture in Berkeley since July 1991. It attacks codling moth prepupae under the bark by paralyzing them and laying an egg externally on the paralyzed host. Parasitoid development is completed in 3-4 weeks depending on temperature. An effective rearing procedure has been developed for the production of L. caudatus on diapausing codling moth cocoons. Mature codling moth larvae are collected into strips of corrugated cardboard 3/4 x 12 inches where they spin cocoons. The strips of cocooned hosts are then placed in a parasitoid oviposition cage for 24 hr before being incubated in 515gallon emergence drums to await parasitoid adult emergence. In 1994, a different Liotryphon species was obtained from Kazakhstan. This species is more difficult to rear on codling moth and we have not been able to obtain a release permit, as the identity of this species can not yet be determined.
This gregarious ectoparasitoid of late instar codling moth larvae has been maintained in culture in Berkeley since September 1991. The small parasitoid adults enter infested fruit to find their hosts and will attack all later larval instars of the codling moth. The host larva is paralyzed and then a series of eggs are laid externally on the host. Parasitoid development is completed in 2-3 weeks depending on temperature. This parasitoid species can readily be reared on larger codling moth larvae (diapausing or nondiapausing stock) in glass vials and does not require the presence of the host plant to secure host attack in captivity.
This solitary endoparasitoid attacks young larvae of codling moth (1st and 2nd instar) and kills prepupae inside their cocoons. It is one of the most important parasitoids in Kazakhstan, where it regularly achieves levels of parasitism between 40-60%. We have tried to maintain this species in culture in Berkeley since May 1993. In 1992, we were unable to achieve successful mating in quarantine, but this problem has been overcome in transferring the culture to our insectary. Detailed observations during the season indicate that this species will only attack host larvae in apples and that the exudates produced by codling moth larvae on the surface of the apple are essential for parasitoid attack. However, we have been unsuccessful in being able to multiply this species in the insectary either using larger oviposition cages or single females exposed to individual infested apples. It seems that the only way to establish this important parasitoid in California pear orchards is to make large scale field collections in Kazakhstan for direct field release from quarantine in Berkeley.
This solitary larval-prepupal endoparasitoid was maintained in culture in quarantine in Berkeley for only two generations. The adult parasitoids mated successfully in captivity but could not be induced to attack codling moth. Additional attempts during 1993 and 1994 using infested thinning apples also proved unsuccessful. Similar difficulties in culturing this parasitoid have been experienced in Canada during the 1960s. It seems probable that this species is not well adapted to the attack of codling moth and uses this host only incidentally. However, in 1995 this species was also collected from codling moth in Kazakhstan, a new record for this region suggesting that this species may be increasing its range eastward from Europe. We will not be considering this species for field release in California.
This gregarious ectoparasitoid of codling moth cocoons was obtained from Kazakhstan for the first time in 1994. Its biology is similar to that of Liotryphon caudatus in that it attacks the prepupal stage of the codling moth. This is a poorly known parasitoid, but local sources of literature from Kazakhstan indicate that it is often responsible for relatively high levels of parasitism. In contrast to L. caudatus, however, M. ridibundus is gregarious producing 4-7 individuals on a single codling moth host. This species also differs from L. caudatus in its behavior; it crawls inside the cardboard strips used for codling moth cocooning in the insectary rather than ovipositing through the strips, and it is frequently active on the floor of the rearing cages. This suggests that M. ridibundus is more likely to attack cocoons that spin up in the crotch of branches or at the base of the trunk, whereasL. caudatus is adapted to the attack of cocoons concealed beneath the bark of the main trunk. Overwintering diapause in M. ridibundus appears to be determined by daylength rather than the accumulation of sufficient cold temperatures through winter, which should facilitate its successful establishment in California.
To field release the two parasitoid species and monitor their establishment and impact on codling moth in pear orchards in California.
During 1997 we field released Liotryphon caudatus, Mastrus ridibundus and Microdus rufipes. From 200 to 2,000 individuals of both L. caudatus and M. ridibundus were released at one time at a field site, depending on the size of the orchard. Releases took place either early in the year in March or later in the season from August to the end of October and were confined to orchards in which insecticides were not being applied. For L. caudatus, 3,400 were released at 8 sites in March and 2,100 were released at 12 sites in October bringing the total number of L. caudatus released in northern California to 41,080 individuals at 41 different sites. In the case of M. ridibundus, we focused more attention on this species during the 1997 season, releasing 2,000 individuals at 6 sites in March and 48,350 at 23 sites in September and October. This very successful set of releases brings the total number of M. ridibundus released in northern California to 95,530 individuals at 34 different sites. Recoveries of M. rufipes from Kazakhstan this year were disappointing, due to the low abundance of codling moth. As a result only 31 parasitoids were field released in late July and early August, bringing the total releases of this species to 253. The parasitoid releases this year took place in pear, walnut, and apple orchards to maximize the probability for establishment of the parasitoid in the region. The pear release sites were in the Sacramento Delta and in Mendocino County. In general, the success of biological control introductions is increased by releasing individuals in as wide a geographic range and over as diverse a set of sites as possible.
We monitor the establishment and impact of the parasitoids by banding trees in the orchards to recover codling moth larvae descending from the fruit to pupate. The bands are placed out in late June to collect the diapausing codling moth larvae and are recovered from the orchards in November. The bulk of the recovered codling moth and parasitoids are allowed to complete diapause by storage at 2°C for four months and then were allowed to emerge at 20°C in the insectary. The emerging parasitoids that have developed from successful attacks of codling moth in California are then added to our insectary culture. However, the codling moth cocoons recovered from a smaller sub-sample of bands from the orchards are dissected to determine the level of parasitism at the release sites.
Table 3 shows the number of orchards monitored from 1992 to 1997 and the number of orchards in which the parasitoids were recovered at the end of the season. Note in Table 3 that Mastrus ridibundus was released for the first time in 1995. Recoveries of Liotryphon caudatus have been sporadic and the extent of parasitism from this species, so far, has remained lower than is typically seen in Kazakhstan (Table 4), although we have recorded up to 36% parasitism by this species in walnut orchards in the Sacramento Valley. However, M. ridibundus has been recovered more consistently than L. caudatus and, in general, the extent of parasitism recorded from overwintering cocoons in the trap bands has been greater (Table 4). This year we did not release any parasitoids in Courtland and yet we recovered both of the cocoon parasitoids from the trap bands, with 38% parasitism by M. ridibundus. These recoveries indicate that parasitoids released in previous years must have successfully overwintered and established populations in this location. With a recorded 38% parasitism, M. ridibundus is generating the same extent of parasitism as is typically recorded in Kazakhstan. No recoveries have yet been made from the small-scale releases of Microdus rufipes.
The three most important parasitoids attacking the codling moth in Kazakhstan are Liotryphon caudatus, Mastrus ridibundus and Microdus rufipes. Rearing techniques for the parasitoids have proved very effective for the production of the cocoon parasitoids Liotryphon caudatus and Mastrus ridibundus, but we have been unable to develop sufficiently effective rearing techniques for Microdus rufipes. Extensive field releases of L. caudatus from late 1992 and of M. ridibundus from 1995, and particularly in 1997, has led to within-season recoveries from codling moth bands in several different climatic zones, and to between-season recoveries from Courtland. These latter recoveries are very encouraging, as this provides us with substantial evidence that the parasitoids are becoming established in at least one pear production region. From our field recoveries so far, it appears that M. ridibundus will be the most important parasitoid of the codling moth in California and that it is likely to have a significant impact on overwintering codling moth populations in orchards that are free from insecticide treatments. With increasing emphasis on mating disruption and IGR's for the management of codling moth in the future, it seems likely that parasitism from these imported parasitoids will become a characteristic of commercial orchards as well as reducing codling moth populations in non-managed sites throughout the state.
Substantial field releases of M. ridibundus were achieved in 1997 allowing releases of this relatively new parasitoid species throughout the state. From field collections of M. rufipes in Kazakhstan over the last two years it is clear that this species is most readily collected from first generation codling moth, as overwintering second generation collections have produced very few individuals the following spring. Although field releases of M. rufipes have been small, so far, field collections in Kazakhstan in 1998, through continued collaboration with Andrey Slivkin, will concentrate more heavily on banding trees during the first generation with the hope that greater numbers can be obtained for field release in July 1998. The opportunity to import and establish the dominant parasitoids from Kazakhstan (Mastrus ridibundus and Microdus rufipes) is an important step in the management of codling moth throughout California.
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