Studies on the ectoparasitoid, Anisopteromalus calandrae How. (Hymenoptera: Pteromalidae) as a biocontrol agent against the lesser grain borer, Rhyzopertha dominica (Fab.) in Saudi Arabia

Studies on the ectoparasitoid, Anisopteromalus calandrae How. (Hymenoptera: Pteromalidae) as a biocontrol agent against the lesser grain borer, Rhyzopertha dominica (Fab.) in Saudi Arabia

Pergamon PII: J. stored Prod. RPS.Vol. 32, No. 2, pp. 137-140, 1996 Copyright 0 1996 Elsevier Science Ltd Printed in Great Britain. All rights reserv...

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Pergamon PII:

J. stored Prod. RPS.Vol. 32, No. 2, pp. 137-140, 1996 Copyright 0 1996 Elsevier Science Ltd Printed in Great Britain. All rights reserved SOO22-474X(9QOOOO5-7 0022-474X/96 %15.00 + 0.00

Studies on the Ectoparasitoid, Anisopteromalus calandrae How. (Hymenoptera: Pteromalidae) as a Biocontrol Agent against the Lesser Grain Borer, Rhyzopertha dominica (Fab.) in Saudi Arabia KHALAFALLA

S. AHMED

Department of Biological and Geological Sciences, Faculty of Education, Ain Shams University, Cairo, Egypt (Accepted 7 February 1996)

Abstract-Anisopteromalus calandrae How. was reared in the laboratory on full grown larvae of Rhyzopertha dominica (Pab.). The incubation period of the parasitoid’s egg was 36 h at 26’C and 27 h at 3O’C. The larval stage lasted 6.9 and 5.4 days, the prepupal stage lasted 23.6 and 17.8 h, and the pupa lasted 5.4 and 4.6 days at 26 and 30°C, respectively. The total developmental time (from egg to adult) averaged 18.9 and 14.6 days at 26 and 30°C, respectively. Sex ratio was 2.1$1& in the field and 2.3?:1$ in the laboratory. The daily and total numbers of eggs laid/female were 6.7, 150.4 and 8.3, 132.6 at 26 and 30°C, respectively. The parasite female and male, fed on honey, lived for 32.6 and 25.5 days at 26’C, respectively. Percentages of parasitism recorded in the laboratory were, respectively 69.5, 43.3, 30.1, 16.8 and 0 on R. domenica, Sitophilus granarius, Bruchus rujimanus, Trogoderma granarium and Oryzaephifus surinamensis. The parasitoid was active in the field from February to November, but reached its peak in July with a 59.3% parasitism on R. dominica. Copyright 0 1996 Elsevier Science Ltd Key words-biocontrol,

parasitoid,

Anisopteromalus calandrae, Rhyzopertha dominica

INTRODUCTION Rhyzopertha dominica (F.) is an important pest of stored wheat and corn (Metcalf and Flint, 1962) in many countries (Egypt, Kaschif, 1959; U.S.A., Storey, Sander and Walker, 1983; and India, Jacob and Mohan, 1973) including Saudi Arabia (Al-Taher and Abo-Zuheira, 1987). One of the most active parasitoids of this pest is the pteromalid Anisopteromalus calandrae How. which also attacks other stored grain pests e.g. Trogoderma granarium Everts (Kapil and Chaudhary, 1973), Sitophilus oryzae L., Sitophilus granarius (L.) (Sweetman, 1964), Sitophilus zeamais Motsch. (Williams and Floyd, 197 1) and Callosobruchus chinensis (Okamoto, 1971). As A. calandrae is recorded from store pests in Saudi Arabia (Rostom et al., 1990) the present work was conducted to investigate its biology under local conditions and the extent of parasitism of R. dominica. The study also examined the role that it could play against other stored product pests. MATERIALS

AND METHODS

A. calandrae was reared on R. dominica at 26 ) 2°C and 60 f 5% r.h. in glass jars (13 x 7 cm) covered with pieces of muslin cloth fixed by rubber bands. Pairs of the parasitoid were confined 137

K. S. Ahmed

138

Table 1. Duration (mean It SD. (range)) of the immature stages of A. calundrae at 26 f 2 and 30 f 2°C at 60 + 5% r.h. (15 females were used at each temperature) (probability at each stage i 0.001) At 26 f 2°C

Stage

Egg(h) Larva (d) Prepupa (h) Pupa (d) Total developmental period(d)

36.2 f 6.9 f 23.6 f 10.6 f 18.9 k

6.5 (30-41) 0.6 (67.5) 2.3 (1628) 0.7 (8-11) 2.0 (1620)

At 30 f 2°C

r-value

21.3 f 0.4 (24-29) 5.4 & 0.7 (56) 17.8 + 0.9 (15-18) 7.4 f 0.8 (6-8) 14.6 f 1.83 (12-15)

41.3 51.4 167.5 100.8 36.3

individually in the jars and provided with drops of honey as food and host larvae, prepupae or pupae for egg deposition. Hosts were replaced daily until the death of the female. To determine the susceptibility of pest species to infestation by A. calundrue, 10 larvae, prepupa, or pupae were taken from pure cultures of T. grunarium, Sitophilus oryzue (L.), Bruchus rufmanus Boheman and Oryzaephilus surinamensis (L.) and exposed to mated females of A. calandrae under the conditions specified above. Sex ratio was determined from monthly field samples of infested wheat grains (2 kg month-‘). The ratio was also determined for the progeny that developed from 20 females in the laboratory. For seasonal abundance, grains infested with R. dominica were collected from stores in the Eastern Province, Saudi Arabia during 1992. Biological experiments were carried out at 26 f 2°C and 30 &-2°C in a series of ‘Precision’ low temperature incubators, each with 60 f 5% r.h. adjusted by the method reported by Solomon (1951), and an L12:D12 hours photoperiod. The longevity of honey-fed males and females was recorded daily. Student’s r-tests was carried out to assess the significance of the results. RESULTS

AND DISCUSSION

Duration of immature stages

The duration of immature stages of A. calandrae are presented in Table 1. The parasitoid spent most of its developmental period as a larva and pupa. An increase in the temperature from 26 to 30°C significantly (t-test, P < 0.001) reduced the duration of immature stages by nearly 20% (Table i).The total developmental period of the parasitoid (egg to adult) averaged 18.9 f 2.0 and 14.6 + 1.8 days at 26°C and 30°C respectively. Similarly, adult A. calandrae required 14 days to emerge from parasitized S. granarium (Sweetman, 1964) and C. chinensis (Okamoto, 1971). Okamoto (1971) reported an 8-day delay of emergence of adult A. calundrae when younger larvae of C. chinensis were used. Host-parasitoid

relationship and seasonal abundance

Mated females of A. calandrae were recorded from full grown larvae, prepupae and pupae of R. dominica and infestation was most frequent during the relatively short prepupal stage (Table 2). While attacking the host, the A. calundrae female pierces the host’s body with its ovipositor causing paralysis and then lays one egg on the outside of the integument. The hatched larva may use the hole made by the mother or make its own hole to extract the body fluid. Unlike many other adult parasitoid females, A. calandrae does not feed on the body fluid of the host (Ahmed, 1989). The females may feed on flower nectar. The parasitoid was active from February to November and reached its peak in July. It seems that a positive correlation existed between activity and atmospheric conditions which in turn were Table 2. Percentage of parasitism on different developmental stages of R. dominica, collected from infested wheat grains during 1992 (50 of each host stage per month were checked) % of parasitism Host Larva Prepupa Pupa

Jan

Feb

Mar

Apr

May

Jun

Jul

Aug

Sep

Ott

Nov

Dee

0 0 0

2.3 3.3 2.1

4.1 3.2 4.4

7.0 9.1 1.7

13.2 19.0 12.1

24.6 29.6 28.0

41.1 59.3 54.2

36.0 48.9 40.1

21.2 39.5 16.3

16.0 13.4 23.2

3.9 4.0 2.1

0 0 0

Biocontrol agents

139

Table 3. Egg laying activity of A. culandrae at constant temperatures and 60 _+5% r.h. on R. dominica (30 females were used at each temperature) Temperature (“C)

Oviposition period mean f S.D. (range in days)

26 + 2 30 f 2

22.7 & 2.3 (20-26) 15.2 f 1.9 (14-20)

Daily eggs laid mean f S.D. (range)

Total eggs laid/q mean f SD. (range)

6.7 rt 0.3 (5-9) 8.3 _+0.9 (7-l 1)

150.4 + 7.9 (125-143) 132.6 + 8.3 (108-126)

related to abundance of the host (Table 2) (Rostom et al., 1990). Disappearance of the parasitoid in December and January may indicate that it avoids adverse conditions by passing these months as a diapausing egg similar to bethylid species (Ahmed, 1989). This disappearance coincides also with the scarcity of host (Rostom et al., 1990). Sex ratio

The sex ratio of field collected material was close to that from material that was bred in the laboratory. In field samples of parasitized host stages the sex ratio of A. calandrae was females to males 2.1:1 (416?:198&. In laboratory samples, the sex ratio was 2.3 females to 1 male (2093$!:916&; the results are virtually identical. Fecundity

Daily egg production of A. calandrae was 6.7 + 0.3 (5-9) and 8.7 + 0.9 (7-l 1) at 26 + 2°C and 30 + 2°C respectively. As shown in Table 3, production significantly increased with the rise of temperature (t-test, P < 0.005). On the other hand, the total eggs laid per female decreased significantly (t-test, P < 0.001) with the rise of temperature as the life span during which oviposition occurs was reduced (Table 3). This marked reduction in the life span may be due to the higher metabolic rate and energy utilization causing death sooner during hot conditions (Ahmed, 1987). The rise of temperature may trigger hormonal activity, accelerating the utilization of more vitelline precursors producing more eggs in a shorter time and compensating for the reduction of life span (Telfer, 1965; Englemann, 1970; Ahmed, 1987). Host susceptibility

The percentage of parasitism of R. dominica was higher than in other species tested (t-test, P < 0.001) (Table 4); reducing to nil in the case of 0. surinamensis. The parasitoid seems to prefer the less hairy and less active larvae. The sequence after R. dominica was S. granarius followed by B. rqfimanus then T. granarium (Table 4). Longevity

Mated female A. calandrae fed on honey, lived significantly longer (32.6 + 6.2 (32-37) days} at 26 f 2°C than at 30°C (25.7 f 3.1 (21-30) days) (t-test, P < 0.001). The respective figures for males were 25.5 + 2.3 (22-30) and 11.7 f 1.9 (9-12) days (t-test, P < 0.001) at the same temperatures. According to Bare (1942) A. calandrae females lived for 39 days and males for 22 days at room temperature. He stated that “A. calandrae could be easily reared in laboratory cultures”. Maintaining A. calandrae on R. dominica at 26°C would give good results in rearing and propagating the parasitoid for a future field release.

Table 4. Percentage of parasitism by A. calandrae on different coleopteran species at 26 + 2°C and 60 f 5% r.h. (30 larvae were exposed separately from other types during each treatment) (t, r-value; P, probability compared with R. dominica) Host species

t

% of parasitism mean + SD.

Rhyzopertha dominica

69.5 + 7.2

Sitophilus granarium Bruchus rufimanus Trogoderma granarium Oryzaephilus surinamensis

43.3 * 5.3 30.1 * 3.9 16.8 + 1.8 0

-

P -

119.4

0.001

161.9 249.2 -

0.001

0.001 -

K. S. Ahmed

140 GENERAL

DISCUSSION

AND OVERVIEW

The present study showed that A, calandrae can be a control agent against a wide range of stored product pests in Saudi Arabia. Besides R. dominica, A. calandrae attacks, paralyses and finally destroys S. granarius, B. rufimanus and T. granarium. Similarly, A. calandrae has been known to act as an ectoparasite on larvae and pupae of C. chinensis in Japan (Okamoto, 1971), Lasioderma serricorne (F.) (Bare, 1942) and S. zeamais (Williams and Floyd, 1971) in India. It seems that A. calandrae has the ability to synchronize its life cycle to each of these hosts and that it becomes abundant during their availability. Hot conditions in Saudi Arabia accompanied by poor storage have encouraged grain infestation by over 12 granivorous coleopteran species (Rostom et al., 1990). Home storage and shops where materials were taken, with no chemical control measures, presumably encouraged the reproduction of the parasitoid to reach a high level (59%). At these stores, temperature was kept at around 30°C by natural means, so that activity of the parasitoid was measured at that temperature. A mass release programme of A. calandrae is recommended to minimize pest infestation and/or keep the pest population under control. A. calandrae attacked R. dominica especially during the prepupal stage. Similar results were obtained by Okamoto (1971) as A. calandrae preferred the younger larvae of C. chinensis. Such stage preference and elongation of developmental period may reflect a certain tendency of A. calandrae to synchronise its life cycle with that of the host according to the suitability of its food. REFERENCES Ahmed K. S. (1987) Studies on the biology of Psocoptera. Ph.D. thesis, University of Wales, UK. Ahmed K. S. (1989) Biological and morphological aspects of the parasitoid Scleroderma ephippium (Saunders) (Hymen.; Bethylidae). Bulletin de Sociefe entomologie d’Egypte 68, 307-320. Al-Taher K. F. and Abo-Zuheira R. A. (1987) Insects infesting stored wheat in the Kingdom of Saudi Arabia and their method of control (in Arabic). 15 pp. Saudi Arabian Ministry of Agriculture and Water and FAO, UTFN, SAU, 002, SAU, KIAj.2

15.

Bare C. 0. (1942) Some natural enemies of stored tobacco insects with biological notes. Journal of Economic Entomology 35, 185-189.

Englemann F. (1970) The Physiology of Insect Reproduction. 307 pp. Pergamon Press, Oxford. Jacob S. A. and Mohan M. S. (1973) Predation on certain stored product pests by the red flour beetle. Indian Journal of Entomology 35, 95-98.

Kapil R. P. and Chaudhary J. P. (1973) Record of nine new hymenopterous parasites for Khapra beetle, Trogoderma granarium Everts. (Coleoptera, Dermestidae). Indian Journal of Entomology 35, 353-355. Kaschif A. H. (1959) Lariophagus distinguendus Frost, ectoparasite on Rhyzopertha dominica Fab. Bulletin de Societe entomologie d’Egypte 43, 184. Metcalf C. L. and Flint W. P. (1962) Destructive and Useful Insects, Their Habit and Control, 1087 pp. McGraw Hill Book Company, New York and London. Okamoto K. (1971) The synchronization of the life cycles between Callosobruchus chinensis (L.) and the parasite Anisopteromalus calandrae Howard. Japanese Journal of Ecology 21, 233-237. Rostom Z. F., Osman S. A., Mussa A. E., Abo-Hadeed A. H. and Abd-Elsalam K. (1990) Stored grain insects and fungi and their effects on grain and animal feed deterioration. A project report for King Ado-El-Aziz City for Science and Technology, King Faisal University, Saudi Arabia. Solomon M. E. (1951) Control of humidity with potassium hydroxide, sulphuric acid and other solutions. Bulletin of Entomological Research 42, 554.

Storey C. L., Sander D. B. and Walker D. (1983) Insect populations of wheat, corn and oats stored on the farm. Journal of Economic Entomology 76, 1323-1330.

Sweetman H. L. (1964) The Principles of Biological Control. Brown Comp. Iowa, USA. Telfer W. H. (1965) The mechanism and control of yolk formation. Annual Review of Entomology 10, 161-184. Williams R. N. and Floyd E. H. (1971) Effect of low temperature on hymenopterous parasites Choetospila elegans and Anisopteromalus calandrae of the maize weevil. Journal of Economic Entomology 64, 1438-1439.