monitoring populations of the almond seed wasp, eurytoma amygdali, with sex pheromone traps and...

Entomol. exp. appl. 62: 9-16, 1992. �9 1992 Kluwer Academic Publishers. Printed #1 Belgium. 9

Monitoring populations of the almond seed wasp, Eurytoma amygdali, with sex pheromone traps and other means, and optimal timing of chemical control

B. I. Katsoyannos, N. A. Kouloussis & A. Bassiliou University of Thessaloniki, Department of Agriculture, Laboratory of Applied Zoology and Parasitology, 54006 Thessaloniki, Greece

Accepted: July 18, 1991

Key words." Eurytoma amygdafi, Hymenoptera, almond pest, sex pheromone, population monitoring, chemical control

Abstract

During the four years 1986-1989 we monitored an adult male population of the almond seed wasp, Eurytoma amygdali Enderlein, in the region of Thessaloniki, using sex pheromone traps, each containing 25 living virgin females. The emergence of adults from infested almonds of the previous year was also monitored in cages in the field, as well as the progress of fruit infestation and egg hatching in the almonds of the Retsou variety. Finally, two chemical control experiments were done against the newly hatched larvae to determine the optimal time for chemical control.

During the 4-year study the start of adult captures occurred between April 13 and April 24, and the maximum between April 17 and May 11. In most cases, adult emergence from infested almonds in field cages began with a delay of 2 to 14 days in relation to the start of trap captures, and was affected by factors such as the date of cage installation. In all years most eggs hatched within 12-18 days of oviposition.

A treatment with phosphamidon at a concentration of 0.06 ~o, applied to tree branches of the Retsou variety with a hand-sprayer on May 23, 1987, when 54.1 ~o of the eggs had hatched, was very effective (final infestation in July was 4.7~o as compared to 89.1~o of the untreated control). Three treatments with phosphamidon 0.06~o, applied each on different tree branches, on May 14, 20, and 25, 1988, when the percentage of egg hatching was 7.8 Yo, 65.3 Yo, and 93.5 %, respectively, were all very effective (final infestation in July was 1.6~o, 3.6~o, and 4.2~o respectively, as compared to 93.6~o of the untreated control). However, the presence of mines in the perisperm and outer endosperm, caused by the feeding larvae before they were killed, was more conspicuous in the almonds treated when the percentage of egg hatching was high.

Our data suggest that the almond seed wasp can be effectively controlled with a single treatment of a systemic insecticide against the newly hatched larvae, preferably applied when the percentage of egg hatching is low to medium (between 10 ~o and 50 ~o). In the area of Thessaloniki, during 1986-89, 10 ~o and 50 To of egg hatching occurred about 21 and 27 days respectively after the beginning of male adult captures in pheromone traps.

I0

Introduction

The almond seed wasp, Eurytoma amygdaB Enderlein (Hymenoptera, Eurytomidae) is the most important pest of almonds in the Eastern Mediterranean countries, destroying up to 90~o of the crop of certain susceptible varieties (Mentjelos & Atjemis, 1970; Plant, 1971, 1972; Talhouk, 1977; Arambourg et al., 1983).

The wasp has one generation per year and overwinters as a developed larva inside the infested almond, which usually remains mummified on the tree. The diapause terminates during the winter (Tzanakakis et al., 1991) and the adults emerge the next spring, when fruit susceptible for oviposition are available. A small part of the population, however, completes its life cycle in two or more years due to a prolonged diapause. The emerging females oviposit inside the endosperm of unripe, green almonds and the growing larvae feed on the developing endosperm and destroy it.

For the control of this serious pest, cultural measures such as collection and destruction of infested almonds, and also chemical control measures are recommended. The most commonly used method is the application of a systemic insecticide against the newly hatched larvae which are inside the endosperm. According to some workers (e.g. Talhouk, 1977) this treatment should be applied 10-15 days after the appear- ance of the first adults, whereas according to others (Mentjelos & Atjemis, 1970) 18-22 days after the maximum of adult emergence, and when most of the eggs deposited by the wasps have hatched. The start and progress of adult emergence are currently monitored by placing cages containing infested almonds from the previous year in the field, and counting the emerging adults. Discrepancies in advice on the optimal time for spraying, coupled with the difficulty of monitoring the adult wasp population, has resulted in multiple insecticide sprayings by growers, which are often applied at inappropriate times and, hence, are ineffective.

The recent discovery that virgin females of the almond seed wasp produce an attractive

sex pheromone for males and the first encourag- ing field results that were obtained by using traps containing virgin females (Pittara & Katsoyannos, 1985), led us to use sex pheromone traps as a tool for monitoring the adult population of the wasp and for determining the optimal time for chemical control.

In this study we present the results of four years' monitoring of an almond seed wasp population with the use of sex pheromone traps. We also compare the trap-catch data with the data on adult emergence from field cages, in an attempt to evaluate the precision of field cages data. More- over, we present data concerning the progress of fruit infestation and egg hatching during these four years, as well as the results of two experiments that were aimed at determining the optimal timing of chemical control in relation to egg hatch and trap-catch data.

Materials and methods

GeneraBties. The study was conducted during the spring and summer of 1986, 1987, 1988, and 1989, in the almond orchard of the University Farm of Thessaloniki, located in Mikra near the airport of Thessaloniki (Northern Greece). The orchard contained 60 well developed almond trees of 10 different varieties. One of these varieties, the local Retsou variety, is especially susceptible to almond seed wasp attack. Seven trees of this variety, planted next to each other in the orchard, were used for the observations and the experiments.

Population monitoring with sex-pheromone traps. In early April of each year three Pherocon 1C traps (Zoecon Corp. Ca., USA) were suspended in the trees of the Retsou variety, at a height of 1.5-2 m above the ground and at a spacing of ca. 10 m. As no synthetic pheromone is available to date, 25 living virgin, 1-8 day-old females were used as pheromone releasers. The females were placed in a 6 cm high, 5 cm diam. cylindrical, wire-screen cage, containing a glass vial with a 10% sugar solution. This cage was placed in the middle of the lower, sticky part of the trap. The virgin

females emerged from mummified infested almonds collected from the same orchard during the winter, and stored at a low temperature (4-6 ~ in the dark. To obtain adults, samples of 250 almonds were periodically transferred from the low-temperature storage to 25 ~ C. As adults of E. amygdali are sexually mature upon emergence (Pittara & Katsoyannos, 1985), females were segregated from the males as soon as they emerged in order to avoid matings. Counts of male catches in the traps were made every 2 days, and the living females in the traps were replaced every 5 days.

Emergence from field cages. Wooden, 30 x 30 x 30 cm cages, with wire screens on three sides, were used to house 120-200 mummified infested almonds, collected from the Retsou trees on the day of a cage installation. The cages were placed at the point where the trunk of a tree branches into the main limbs. To provide protec- tion from rain a transparent polyethylene cover was suspended horizontally about 1 m over the cage. The cages were inspected every two days and the adults that emerged were counted and removed.

During 1986 and 1987 one field cage was used and installed on April 14 and March 30 respectively. During 1988 and 1989 three field cages were used, installed with a time difference, to investigate whether the emergence of the wasps is influenced by the time of cage installation.

Monitoring of infestation and egg hatching. Samples of 20 almonds of the Retsou variety were taken at regular intervals (every 2--4 days in 1986 and 1987, every 2 days in 1988 and 1989) throughout the experimental period of each year and were dissected under a binocular microscope in the laboratory. The number of eggs and larvae in each almond was counted in order to monitor: a. the degree of infestation (percent of fruit with eggs), b. the average number of eggs deposited per fruit and, c. the percentage of egg hatching.

Chemical control experiments. Two experiments were conducted, one in 1987 and the other in

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1988, to evaluate the effectiveness of systemic insecticide treatments in relation to the percentage of egg hatching, the trap catches, and the emergence of adults in field cages.

In both trials the systemic insecticide phosphamidon (Dimecron-50) was used at a concentration of 0.06?0, as in similar experiments conducted by Mentjelos and Atjemis (1970). The treatments were applied with a hand-sprayer, to 'run-off of the solution, on tree sectors (branches of about 2 x 2 m outer dimensions) of the Retsou variety. Untreated branches of the same trees were used as controls.

In 1987 the treatment was applied on May 23, as soon as egg hatching exceeded 50?0 (54.1% egg hatching on May 22). Six tree sectors bear- ing ca. 200 almonds each, were sprayed. In 1988 three treatments were applied, on different branches each, on May 14, 20, and 25, when the percentage of egg hatching was 7.8 ~o, 65.3 ?o, and 93.5 ~o respectively. Two tree sectors, each bear- ing ca. 500 almonds, were sprayed on each of the three application dates.

The effectiveness of the treatment was measured by sampling almonds from sprayed and untreated branches during July, when the larvae were fully developed, recording the number of infested and uninfested almonds. Because we observed mines in the perisperm and outer endosperm during the examination of the treated almonds, apparently caused by the feeding larvae before they were killed by the insecticide, addi- tional almonds were sampled from each treatment in September 1988, at harvest. These almonds were examined under a binocular microscope for presence of mines in the perisperm and outer endosperm. The maximum depth of each mine and its diameter (average diameter of mea- surements at 2 different points) were measured.

Results and discussion

Monitoring of the adult population, progress of the infestation and egg hatching

The results of the monitoring of the adult population with sex pheromone traps, the emergence

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of males and females in field cages, and the progress of egg hatching, for the years 1986-1989, are illustrated in Figure 1.

1986. The first males were caught in the traps on April 17, the same day as the emergence of the first male adults in the field cages was observed. The maximum of trap captures occurred between April 22 and 24, and coincided with the maximum of male emergence in the field cages. Maximum emergence of females was a few days later, as a result of protandry known for this insect (Plaut, 1971; Talhouk, 1977); this was also evident in the subsequent years.

On April 28 the rate of infestation (oviposited almonds) was 57.6~o, and two days later it reached 100~o. Egg hatching was 5.6~o on May 8, 53.7~o on May 12, and 73.9~o on May 22. At the beginning of the infestation, just a few days after adult emergence, we usually found one egg per almond but later, when the degree of infestation reached its maximum, almonds contained an average of 5.4 eggs each. In the subsequent years the situation was similar: Initially almonds contained one egg each, whereas later when the degree of infestation reached its maximum almonds contained 6.9 (1987), 3.9 (1988), or 8.3 (1989) eggs each.

1987. The first males were caught in the traps on April 24 and the maximum was observed on May 11. However, the first adults in the field cage emerged 14 days later, on May 8, when the degree of infestation had already exceeded 20 ~o. Possi- bly the females that had caused that infestation, as well as the males that had been caught by the traps before the beginning of adult emergence in the field cages, originated from infested almonds exposed in the field to conditions more favourable for adult emergence than the caged almonds, e.g. in branches exposed to more direct sunlight. An- other possibility is that these females had immi- grated from other orchards. The latter hypothesis is however less probable, since the almond seed wasp is a poorly dispersing species (Plaut & Mansour, 1973). Interestingly, despite the delay in emergence in the cages, the peak of male emer-

gence in the field cages again coincided with the peak of male captures in the traps. The sex ratio of the emerged adults, in this and the subsequent years, was in favour of the females, a phenome- non that has also been reported by some workers (cf. Plaut, 1971). A total of 283 males and 509 females emerged in the field cages during the four years of study (sex ratio 1:1.8).

Fruit infestation reached 20~o on May 7, and 100~/o by May 11. Egg hatching was 12.7~o on May 17 and 54.1~o on May 22. The majority of eggs hatched within 15 days.

1988. The first males were caught in the traps on April 21 and the maximum was observed on May 5. The first adults emerged on May 1 in the field cage that was installed on March 20, on April 27 in the cage which was installed on April 1, and on April 25 in the cage which was installed on April 11, i.e. 10, 6 and 4 days after the first trap captures respectively. Probably, the date of almond collection and installation of the field cages affected the pattern of wasp emergence.

Fruit infestation reached 75~o on May 7, and 100~o on May 13. Egg hatching was 8.2~o on May 15 and 44.7~o on May 17. The majority of eggs hatched within 12 days.

1989. The first males were caught in the pheromone traps on April 13 and the peak was observed on April 17. In the field cage that was installed on April 1, adult emergence began on April 15, two days after the first trap captures. The difference in the emergence between this field cage and the field cages that were installed 10 days earlier or later were not as great as they were in 1988.

In this year the level of fruit infestation was 20~o by April 17 and 100~o by April 23. Egg hatching was 10.1~o on April 29 and 48.5~o on May 7. The majority of eggs hatched within 18 days.

Chemical control experiments

The infestation rate of almonds treated with phosphamidon and untreated almonds is given in

13

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11 15 19 2 3 2 7 1 5 9 13 17 21 2 5 2 9 2

APRIL MAY JUNE

Fig. 1. Phenological data of Eurytoma amygdali, during 1986-1989. A: Captures of males in sex pheromone traps, B: Number of males that emerged in field cages, C: Number of females that emerged in field cages, D: progress of fruit hatching.

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Table 1. These data were derived from samples taken in mid-July when the larvae inside the almonds were fully grown. Table 1 shows that the phosphamidon treatment conducted in 1987, when egg hatching had just exceeded 50%, was very effective.

In 1988 the three chemical treatments conducted on respectively May 14, 20, and 25, where all very effective. However, the effectiveness of the treatment of May 14, when egg hatching was still low, was slightly greater than that of May 20, when egg hatching was medium to high, and still greater than that of the treatment of May 25, when egg hatching was very high. Also, the earlier the treatment the shorter and the shallower were the mines made by the young larvae (before they were killed by the insecticide) in the perisperm and the outer endosperm of the almonds (Table 2) and, as a consequence, the better the quality of the almonds.

Relation between population monitoring methods and optimal timing for chemical control

The results of the chemical control experiments indicate that treatments made within the egg hatching period of 10-15 days are all effective. However, treatments conducted when egg hatch-

ing is rather low to medium (e.g. between 10% and 50~o) have a more favourable effect on almond quality than the later treatments, when egg hatching is high (e.g. about 90~o). Therefore we consider that the optimal time for chemical treatment is when egg hatch is low to medium (10 %o-50~o).

The period between 10-50% of egg hatching varied considerably from year to year. As a consequence, for optimal timing of chemical treatment population monitoring is required. The most reliable method for determining the precise timing for chemical treatment is the sampling of almonds and counting of the eggs and neonate larvae under a binocular microscope. This is a laborious task, since the minute eggs of E. amygdafi are hardly discernible because of their similar colour with the surrounding endosperm. On the other hand, timing based on field cage emergences cannot be considered as reliable, for they are influenced by factors such as the date of almond collection and cage installation. With the exception of 1986, the beginning of adult emergence in the field cages was observed a few to several days after the beginning of male catches in the sex pheromone traps, and hence the actual beginning of the flight.

The data from the sex pheromone traps, especially those concerning the beginning of the flight, provided more precise results than the field cages

Table I. Infestation of almonds ofthe Retsouvariety. Samples taken a tmid July from branches treated with phosphamidon 0,06~ on different dates and from untreated control branches

Date of (%) treatment egg hatching

during treatment ~

Infestation at mid July

No. 2 (%) Effectiveness (%) almonds examined infested almonds (Abbott)

1987 May 23 54.1 102 4.7 94.3 Control - 92 89.1 -

1988 May 14 7.8 610 1.6 98.3 May 20 65.3 891 3.6 96.2 May 25 93.5 763 4.2 95.5 Control - 668 93.6 -

1 Measured on the day of the treatment or on the previous day. 2 Of the total of 786 infested almonds 92.1% contained only one larva each, 7.8% contained two larvae, and 0.1% (only one)

contained three larvae. Of the 61 almonds with two developed larvae, 52.5~ had double seeds,

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Table 2. Mean dimensions of the mines made by E. amvgdafi larvae (before they were killed by the insecticide) in the perisperm of almonds of the Retsou variety. Almonds were treated with phosphamidon on the trees at three different dates and then sam- pies were taken m September at harvest

Date of (%) No. treatment egg hatcing mines examined

during treatment

Mean dimensions of mines ~

Diameter Depth (ram) (mm)

1988 May 14 7.8 39 1 48a 0.24a May 20 65.3 46 2.20b 0.36b May 25 93.5 31 2.57c 0.42c

Means followed by a different letter are significantly different at the 0.01 ~ o level (LSD test).

and could be used to predict the time when egg hatching reached 10-50~o (optimal time for chemical control). As shown in Table 3, in the area of Thessaloniki 10 ,~ o and 50 }o of egg hatching occurred, during our 4-year observations, respectively about 21 and 27 days after the beginning of trap captures. The maximum of trap captures could also be used for this purpose, but in this case the observed deviations were greater.

In conclusion, our data suggest that the almond seed wasp can be effectively controlled with a single treatment of a systemic insecticide, such as phosphamidon. The treatment is directed to the newly hatched larvae and should be applied when egg hatching is between 10~ and 50~ When these percentages will occur can be predicted with

adequate precision by means of sex pheromone traps baited with virgin females, as long as synthetic pheromone is not yet available.

Acknowledgements

This work has been conducted within the research programme 'Investigations on the ecology, phys- iology, and behaviour of the almond seed wasp', which was funded by the Greek Ministry of Industry, Energy, and Technology (PRO-PE- 1985-86). We thank the director of the Arbori- culture Section of the University Farm of Thessaloniki Dr. M. Manolakis for permitting us to use the almond orchard, the agronomist D.

Table 3. Approximate number of days from respectively the beginning and the maximum of captures ofE. ano'gdali males in sex pheromone traps until 100; and 50~ egg hatch

Year Number of days from begin of trap captures until

Number of days from maximum of trap captures until

I0~ 50~ 10% 50~ egg hatch egg hatch egg hatch egg hatch

1986 22 25 16 19 1987 23 28 6 11 1988 24 29 10 15 1989 16 25 12 21

Mean: 21.2 26.8 11.0 16.5 SD : 3.6 2 1 4.2 4.4

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Kyparissoudas for providing us with a number of traps and our graduating students K. Stigas and Ch. Chryssochoides for technical assistance. Many thanks are also due to Prof. M.E. Tzanakakis for reading the manuscript and mak- ing valuable suggestions, and to Dr. D. S. Koveos for his help in the preparation of the figure.

References

Arambourg, Y., G. Fauvel & H. Chevin, 1983. Eurytoma amygdali End. et sa pr&ence en France. Un nouveau chal- cidien ravageur de l'amandier. Arboric. Fruiti&e 358: 27- 28.

Mentjelos, J. & A. Atjemis, 1970. Studies on the biology and control of Eurytoma amygdali in Greece. J. econ. Entomol. 63: 1934-1936.

Pittara, I. S. & B. I. Katsoyannos, 1985. Male attraction to virgin females in the almond seed wasp Eurytoma amygdali

Enderlem (Hymenoptera, Eurytomidae). Entomol. Hellen- ica 3: 43--46.

Plaut, H. N., 1971. On the biology of the adult of the almond seed wasp, Eurytoma amygdali End. (Hym., Eurytomidae), in Israel. Bull. ent. Res. 61: 275-281.

Plaut, H. N., 1972. On the biology of the immature stages of the almond wasp, Eurytoma amygdaIi End. (Hym., Eury- tomidae) in Israel. Bull. ent. Res. 61: 681-687.

Plant, H. N. & F. Mansour, 1973. Studies on the behavlour, dispersal, and damage potential of the almond wasp, Eurytoma amygdali. Entomol. exp. & appl. 16: 415-421.

Talhouk, A. S., 1977. Contribution to the knowledge of almond pests in East Mediterranean countries V. The fruit- feeding insects Eurytoma arnygdali End., and Anarsia lineatella Z. Z. ang. Entomol. 83: 145-154.

Tzanakakis, M.E., E.J. Karakassis, G. Tsaklidis, E. Ch. Karabina, I. Ch. Argalavmi & I. G. Arabatzis, 1991, Time of diapause termination in the almond seed wasp, Eurvtoma amygdali Enderlein (Hym., Eurytomidae), in northern Greece under certain photoperiods and temperatures. J. Appl. Entomol. 111: 86-98.

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