Effect of mala th ion-ba i t mixture on two parasitoids of the Florida red scale,
Chrysomphalus aonidum (L.)
EPHRAIM COHEN, HAGGAI PODOLER AND MUHAMAD EL-HAMLAUWI
Department of Entomology, The Hebrew University of Jerusalem, Faculty of Agriculture, Rehovot 76-100, Israel
ABSTRACT. Experiments with laboratory populations have shown that immature stages of the hymenopterous parasitoids, Aphytis holoxanthus DeBach and Pteroptrix smithi (Compere) were unaffected by a malathion-bait mixture (0.13% malathion) applied to their host, Chrysomphalus aonidum (L.). However, the emerging adults of A. holoxanthus were highly susceptible and it was clearly shown that malathion absorbed in the scale cover of the host was responsible for the lethal effect. Similar results were obtained with parasitized scale insects which were exposed in a commercial citrus grove to ground spray of malathion (1.3% malathion). An experiment with natural populations of both parasitoids in the citrus grove clearly demonstrated the susceptibility of A. holoxanthus to malathion-bait spray and were consistent with the above-mentioned laboratory experiments. The results are discussed in the light of the predominant status ofP. smithias a natural enemy of the Florida red scale in citrus groves in Israel. No delayed effects related to fertility, sex ratio and life expectancy of both parasitoid species which survived the malathion treatment were observed.
KEYWORDS: Florida red scale; Chrysomphalus aonidum; Aphytis holoxanthus; Pteroptrix smithi; parasitoids; malathion toxicity; natural enemies; Israel; biological control
Introduction
Until the late 1950s, the Florida red scale, Chrysom- phalus aonidum (L.) was a serious pest of citrus groves in Israel. During 1956-57 the parasitic wasps Aphytis holoxanthus DeBach and P~eroptrix smithi (Compere) were simultaneously introduced from Hong Kong. Since then both parasitoids have effectively contained the populations of the pest, usually below the economic threshold. However, while initiallyA, holox- anthus was the predominant species, it has been gradually displaced by P. smithi which emerged as the major parasitoid of the Flc rida red scale (Steinberg, Podoler and Rosen, 1986). This shift in the relative composition of the natural enemy complex coincided with an increase in frequencies of local resurgence of the pest in the citrus groves of Israel. Although the reasons for this change are still not clear, new findings provided some helpful clues for a valid explanation (Steinberg, Podoler and Rosen, 1987). One hypothesis relates the observed change ~:o the continuous applica- tion of malathion-bait spray against the Mediter- ranean fruit fly (medfly), Ceratitis capitata (Weide-
mann). Although A. holoxanthus has a faster rate of reproduction, P. smithi was found to be considerably less susceptible to malathion (Steinberg et al., 1987). Moreover, the recent changes in the relative size of the parasitoid populations may involve the extensive area coverage and drift characteristric of ultra low volume (ULV) aerial treatments which started in the 1960s for medfly control. Apparently, such applications leave insufficient untreated areas as protected niches for development of malathion-sensitive beneficial insects such as A. holoxanthus. The overall diminished effec- tiveness of natural enemies in controlling C. aonidum in Israel also can be attributed to the increasing use of broad-spectrum insecticides which are known to disrupt biological control measures (Ripper, 1956; Bartlett, 1963; Newsome, 1967; Abdelrahman, 1973; Croft and Brown, 1975; Troetschler, 1983). A similar phenomenon was reported in Texas where application of the organophosphorus compound methidathion and the carbamate carbaryl drastically reduced populations of A. holoxanthus, causing an increase in population size of its host (Dean, 1982).
Information about the effects of insecticides on beneficial insects is of great importance in designing integrated pest management (IPM) programmes. As the malathion-bait has been applied extensively,
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regularly and over many years to control the Mediter- ranean fruit fly, its disruptive effects on the two important parasitoids of the Florida red scale were investigated and the results are reported here.
Materials and methods
Insect cultures
Host: Chrysomphalus aonidum (L.). The insects were reared on squashes (var. Banana) under controlled conditions of 27°C, 65% relative humidity (r.h.) and at a photoperiod of 16L:8D. Populations were main- tained by introducing new squashes at appropriate intervals and allowing a batch of crawlers to settle, yielding approximately 2000 scale insects per squash.
Effect of malathion on two parasitoids
were smeared with malathion-bait mixture using a fine brush. Control hosts were treated with water only. The experiments were conducted in four replicates (150 scale insects per replicate) at 27°C, 65% r.h. and 16L:18D photoperiod. After the last application the number of emerged adult parasitoids was recorded and, 2 weeks later, the covers of the hosts were care- fully removed and the insects were thoroughly examined for mortality of developmental stages of parasitoids using a stereoscopic microscope.
Parasitoids: Aphytis holoxanthus DeBach and Pterop- trix smithi (Compere). Squashes with 5-week-old scale insects were placed in standard rearing cages (86 x 82 × 61.5 cm) containing adult parasitoids of either species for parasitization. Before adult emergence the squashes with parasitized hosts were transferred to dark cages (24× 16× 15cm) and the emerging wasps, being attracted to light, were collected in glass tubes inserted into the roof of the cages. Fine droplets of honey served as food for the adult parasitoids.
The initial cultures of C. aonidum and ofA. holox- anthus were obtained from the Israel Cohen Institute for Biological Control, the Citrus Marketing Board, Rehovot, Israel. The starting culture ofP. smithi was obtained from samples of parasitized Florida red scale collected in a commercial citrus grove in the Gaza strip.
Malathion-bait
An emulsifiable concentrate (EC 80%) of malathion [diethyl(dimethoxyphosphinothioylthio)succinate] was mixed with a protein hydrolysate bait (Naziman, Tamogan, Israel). A formulation containing 1.3% malathion plus 10% bait is being commercially used to control C. capitata in citrus groves of the Gaza strip.
A 1:10 concentration of malathion (0.13%), found to be without any noticeable effects on the host scale insects (Cohen, Podoler and E1-Hamlauwi, 1987), was used in the laboratory experiments.
Application of malathion
Laboratory. Immature stages, at the defined age, of A. holoxanthus and P. smithi were obtained by sequential parasitization (for 24 h) of 5-week-old female scale insects. After the first parasitization, two consecutive exposures of the same batch after 5 and 9 days to A. holoxanthus, and 12 and 16 days to P. smithi, took place. The experiments were conducted in four replicates (150 scale insects per replicate). Twenty- four hours after the last exposure, the hosts which now contained the corresponding pupae, larvae and eggs,
Field. Ground application of malathion on alternate rows with partial coverage (100ml of spray per tree) which is the outline procedure in the Gaza strip for controlling the Mediterranean fruit fly, was the method employed in this experiment. Squashes infested with scale insects (150 per squash) that had been sequentially parasitized according to the pro- cedure described above, were placed on trees in the interior of the canopy (at a height of 1.80m) in a commercial citrus grove in the Gaza strip. A total of 12 squashes were used in this experiment. Six squashes were exposed to a commercial application of malathion-bait in the spray row, and six more were placed on trees in the adjacent alternate untreated rows and served as controls. Five hours after the malathion- bait application the squashes were returned to the controlled conditions of the laboratory. During the period in the field, no significant parasitization by natural population of parasitoids was expected. Adult emergence and mortality of developmental stages were recorded as previously described.
In another set of experiments the effect of com- mercial malathion-bait on the natural population of the parasitoids was studied. Valencia oranges infested with Florida red scale were collected at random from malathion-bait-treated as well as from adjacent untreated trees in the same commercial citrus grove (six replicates). Scale insects with existing emergence holes were removed. The fruits were placed in cages under the controlled laboratory conditions and the emergence of adults of the two parasitoid species was recorded over 14 days. After the end of adult emergence the scale insects were carefully examined for dead parasitoids (immatures and adults) under- neath their covers.
Effect of malathion absorbed by scale cover
Plastic cylinders (3" 0 cm inside diameter and 2.5 cm high), surrounding groups of about 50 5-week-old female scales, were glued to squashes with plastic glue and covered with a piece of silk cloth. Four fertile A. holoxanthus females (8 h old) were placed inside each cylinder for a period of 24 h and 10 days later the vials were randomly divided into five groups (four replicates per treatment). Scale insects of two groups were smeared with malathion-bait mixture (0.13°70 malathion) whereas insects of the three other groups were treated with water. Two days after the above
CROP PROTECTION Vol. 7 April 1988
EPHRAIM COHEN et al.
treatments, scale covers were exchanged among insects of the different groups, as indicated in Table 2. This procedure was carried out by carefully removing the scale cover with a fine entomological pin and attaching a new cover to the host using a tiny droplet of egg white. The number of adult parasitoids which emerged through the scale covers in the various experimental groups were recorded.
Ecological parameters
Life expectancy (ex) was calculated by following the daily survival rate of emerged adult parasitoids in the control and in insects exposed to malathion at the egg, larval and pupal stage. Each treatment group, com- prising 20-30 emerged adults of either A. holoxanthus or P. smithi, was placed in a glass tube (8x 1- 5cm) and provided with tiny droplets of honey for nutrition. Fertility was determined 5y placing newly emerged adults of these treatment groups into plastic ovi- position cylinders (2.5cm inner diameter, 3 .0cm high) attached to squashes infested with scales. The oviposition period for A. holoxanthus (four pairs/vial, seven replicates) and for P. smithi (three pairs/vial, 10 replicates) was 48 h and 3 ,:lays, respectively. Suitable hosts were not a limiting factor in this experiment. Oviposition was recorded by removing the scale covers and counting directly the easily detected eggs of A. holoxanthus. In the case of the endoparasitoid P. smithi, the scale covers were removed several days later and young larvae within the hosts were counted. The sex ratio was calculated after adult emergence in the relevant treatment groups.
Results and discussion
The differential effects of the malathion-bait, when applied to the Florida red scale, on survival of the two hymenopterous parasitoids are summarized in Table 1. The laboratory population of A. holoxanthus was highly susceptible to the in:secticide after laboratory or field application. Under the controlled laboratory conditions (Table 1), where all scale insects were exposed to the toxicant, no adult parasitoids emerged
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even when the hosts were treated immediately after parasitization (egg stage). This is noteworthy as, under our laboratory conditions, the duration of develop- ment from egg hatch to adult emergence was about 14 days, i.e. the insecticide absorbed in the scale cover was still toxic to the emerging parasitoid. A similar trend, albeit less dramatic, was observed following exposure to malathion in the citrus grove (Table 1). The number of emerging adults was significantly lower following exposure to malathion-bait. Nevertheless, certain dif- ferences related to the two modes of application exist. The commercial treatment in the citrus grove does not achieve complete coverage; a proportion of the scale insect population was therefore not exposed to the insecticide. It is assumed that the uninterrupted development and emergence of parasitoids in those malathion-free scale insects could explain the relatively high emergence rate ofA. holoxanthus adults after field exposure. On the other hand, scale insects which were exposed to malathion-bait received a tenfold higher concentration of the poison (1.3%) than with the laboratory treatment. This is probably the reason for the considerable increase in mortality of immature stages of A. holoxanthus found underneath the scale insect covers (from 13-6% to 20.2%, see Table 1). Possibly malathion at this high dose penetrated through the scale insect cover and poisoned immature stages.
The important role of the scale insect cover in absorbing malathion and thus affecting the survival of emerging parasitoids is demonstrated in Table 2. Replacement of scale covers per se had no detrimental effect on the emergence ofA. holoxanthus (Table 2, A vs B), yet treated covers significantly reduced the number of emerging adults when placed on untreated scale insects (Table 2, D). On the other hand, when scale covers from treated insects were replaced by those of untreated individuals ( Table 2, E), the number of emerging parasitoids was similar to that of the controls (Table 2, A and B).
On the basis of toxicological assays by feeding, P. smithi was reported to be relatively tolerant to malathion, compared withA, holoxanthus (Steinberg et al., 1987). This insensitivity also was observed in the
TABLE 1. Mortality of immature and adult Aphytis holoxanthus and Pteroptrix smithi when host scales with different stages of parasitoids beneath were treated with malathion-bait
Parasitoids emerging Hosts (%) containing when exposed as: parasitoids dead as:
Field Bait 28.2 31.0 8.8* 1.0 11 '0" Field Control 34.8 38" 8 24.0 1.0 5.4
* Values differ from control at P=0.05 (t test). Values (percentages) were analysed after angular transformation.
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study reported here (Table 1). Treatment with malathion-bait in the laboratory had no significant detrimental effects on immature stages nor on adult emergence (Table 1). However, commercial applica- tion when the parasitoid was in the pupal stage (Table 1) resulted in a significant reduction in adult emergence (from 24.0 to 8" 8). Similarly, the mortality of parasitoid adults under the host cover was greatly increased (11 vs 5.4). Again, the high concentration of malathion in the commercial spray was apparently related to the mortality of the parasitoids.
The results obtained with the natural populations of both parasitoid species (Table 3) resemble those with the laboratory populations. A reduced number of A. holoxanthus adults emerged from treated compared with control hosts (47 vs 132), whereas adult emer- gence of the tolerant P. smithi was unaffected. These results are consistent with the percentage of hosts con- taining emergence holes. The higher sensitivity of A. holoxanthus to malathion also is demonstrated by the presence of dead adults underneath the scale covers. As malathion-poisoned bait is massively and routinely applied in citrus groves against the Mediterranean fruit fly, it is not surprising that sensitive non-target organisms such as beneficial insects are affected (Ehler and Endicott, 1984; Ehler et al., 1984; Hoy and Dahlsten, 1984). Armoured scales are protected from the toxic effect of malathion by their covers (Cohen et al., 1987); however, it appears that the toxicant absorbed in the scale insect cover is protected from extensive degradation and therefore remains toxic to
Effect of malathion on two parasitoids
the extremely susceptible emerging parasitoids. Malathion is less detrimental to P. srnithi than to A. holoxanthus. This relative insensitivity, in conjunction with the current practice of using malathion-bait ULV sprays to control the Mediterranean fruit fly, may be prime reasons for the predominance ofP. smithi as the natural enemy of C. aonidum in citrus groves in Israel. Other ecological factors, such as the attractiveness of the poisoned bait to adults, have not been investigated and should not be overlooked.
Adults ofA. holoxanthus and P. smithi that survived the malathion treatment did not differ from the control in life expectancy, fertility and sex ratio of the off- spring. The life expectancy ofA. holoxanthus was 11.4 clays in the control and 11-0-11.8 days in the various treatments. Fertility in the various treatment groups was 97-99% of that of the controls, which averaged 5.1 eggs/female. Females constituted 67% of offspring in the controls, and 66-67% in the various treatment groups. For P. smithi the results were as follows: life expectancy was 11.2 days in the control, 10 .6-11.7 days in the treatments; fertility was 95.4-100% of the controls, which averaged 9.4 eggs/female; percentage of female offspring was 66"8 in the control, 65 .3- 67.2 in the treatment groups.
TABLE 2. Emergence of Aphytis holoxanthus after Chrysomphalus aonidum scale covers were treated with malathion-bait
Emerging adults* Treatment (x _+ SD)
20.0 ± 2 .7 a
19.0 _ 1.8 a 11 '3 ± 1.3 b
13"0 ± 2.2 b
1 7 . 0 ± 2 . 7 a
A. Untreated scale cover left undisturbed B. Untreated scale cover placed over untreated
scale body C. Scale cover treated in situ D. Treated scale cover placed over untreated
scale body E. Untreated scale cover placed over treated
scale body
* Values with the same letter do not differ significantly (at P=0'95).
References
ABDELRAHMAN, I. (1973). Toxic i ty o f mala th ion to the natural enemies o f California red scale, Aonidiella aurantii (Mask.) (Hemiptera : Diaspididae). Australian Journal of Agriculture Research 24, 119-133.
BARTLETT, B. R. (1963). T h e contact toxicity o f some pesticides res idues to h y m e n o p t e r o u s parasites and coccinellid predators. Journal of Economic Entomology 56, 694-698 .
COHEN, E., PODOLER, H. AND EL-HAMLAUWI, M. (1987). Effects o f the ma la th ion -ba i t mix tu re used to control Ceratitis capitata (Wiedemann) (Diptera: Tephr i t idae) on ci trus on the Florida red scale, Chrysomphalus aonidum (L.) (Diaspididae: Hemip- tera), and its parasitoid Aphytis holoxanthus DeBach (Aphelinidae: Hymenopte ra ) . Bulletin of Entomological Research 77, 303-307 .
CROFT, B. A. AND BROWN, A. W. A. (1975). Responses o f a r th ropod natural enemies to insecticides. Annual Review of Entomology 20, 285-335 .
DEAN, H. A. (1982). Reduced pest s tatus o f the Florida red scale on Texas ci trus associated wi th Aphytis holoxanthus. Journal of Economic Entomology 75, 147-149.
TABLE 3. Effe~fc~mmer~ia~lyappliedma~athi~n-bait~nde~e~pmentalstages~ftheparasiticwasps,Aphyt~sh~l~xanthusandPter~ptrixsm~thiinthe citrus grove
Hosts with:
Dead Emerging Emergence
Parasitoid Treatment t adults~ holes (°70) Larvae Pupae Adults
"I" Orange fruits naturally infested with parasitized Chrysomphalus aonidum were exposed to the routine sprays of poisoned bait in a commercial citrus grove (see text for details). :1: Results are averages of six replicates, each of 500 scale insects. * Values differ from control at P=0.05 (t test). Values (percentages) were analysed after angular transformation.
C R O P P R O T E C T I O N Vol. 7 Apri l 1988
EPHRAIM COHEN et aL 95
EHLER, L. E. AND ENDICOTT, 17. C. (1984). Effect of malathion- bait spray on biological control of insect pests of olives, citrus and walnut. Hilgardia 52, 1--47.
EHLER, L. E., ENDICOTT, P. C., HERTLEIN, M. B. AND ALVARADO-RODRIGUEZ, B. (1984). Medfly eradication in California: impact of malathion-bait sprays on an endemic gall midge and its parasitoids Entomologica experimentalis et applicata 36, 201-208.
HoY, J. B. AND DAHLSTEN, D. L. (1984). Effects of malathion and Staley's bait on the behavior and survival of parasitic Hymenoptera. Environmental Entomology 3, 1483-1486.
NEWSOME, L. D. (1967). Consequences of insecticide use on non- target organisms. Annual Review of Entomology 12, 157-286.
RIPPER, W. E. (1956). Effect of pesticides on balance of arthropod populations. Annual Review of Entomology 1,403-438.
STEINBERG, S., PODOLER, H. AND ROSEN D. (1986). Biological control of the Florida red scale, Chrysomphalus aonidum, in
Israel by two parasite species: Current status in the coastal plain. Phytoparasitica 14, 199-204.
STEINBERG~ S., PODOLER, H. AND ROSEN, D. (1987). Competition between two parasites of the Florida red scale in Israel. Eco- logical Entomology 12, 299-310.
TROETSCHLER, R. G. (1983). Effects on nontarget arthropods of malathion bait sprays used in California to eradicate the Mediterranean fruit fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae). Environmental Entomology 12, 1816- 1822.
Received 16 February 1987 Resubmitted 28 September 1987 Accepted 26 October 1987
