TECHNICAL BULLETIN 135

BIOLOGY AND BIOLOGICAL CONTROL OF PARABEMISIA

MYRICAE (KUWANA) (HOMOPTERA:ALEYRODIDAE)

IN CYPRUS

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G. M. Orphanides _ .0

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AGRICULTURAL RESEARCH INSTITUTE

MINISTRY OF AGRICULTURE AND NATURAL RESOURCES

NICOSIA CYPRUS

SEPTEMBER 1991

ISSN 0070-2315

All responsibility for the infonnation in this publication remains with the author(s). The use of trade names does not imply endorsement of or discrimination against any product by the Agricultural Research Institute.

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BIOLOGY AND BIOLOGICAL CONTROL OF PARABEMISIA MYRICAE (KUWANA) (HOMOPTERA:ALEYRODIDAE)

IN CYPRUS

G.M. Orphanides

SUMMARY

In Cyprus, the Japanese bayberry whitefly, Parabemisia myricae (Kuwana), was fIrst detected on citrus in 1983. A bio-ecological study in 1987/88 revealed that the insect devel­ops a maximum of nine generations per year and overwinters at the young larval stage. High­er population levels were found in spring and autumn than during summer and winter. Sig­nifIcantly more eggs were laid on the upper leaf surface, while most of the larvae were found on the lower leaf surface. More larvae were also found in the East and North than in the West and South quadrants. A parasitoid of uncertain origin, Eretrrwcerus sp., showed an im­pressive effectiveness in the biological control of the Japanese bayberry whitefly in the is­land.

llEPIAH'I'H

~tllV KuJtQO, 0 aAEu~<MllC; twv EOJtEQLOOELOO>V, Parabemisia myricae (Kuwana), (3QE8l]xE yLa Jt~tll qJOQ<i to 1983. ~E (3LO-OLXOAOYLXi] lA£A.Etll xatu to 1987/88 JtaQ<ltllQi]8l]xE OtL 0 aAEuQWollC; EXEL J.tEXQL EvvEa yEVEEC; to xQ6vo xaL OLaXEL!-L61.;,EL oto ot60LO tllC; VEaQi]c; JtQOvUlUPllC;. Katu tllv uvmSll xm to <p8LV6JtwQo m JtA1l8uol-LOL tou Evt6!-Lou i]tav JtLO '\jJllAOL JtOQU to XELlUbva xm to xaAoxaLQL. ~lll-LOvtLxU JtEQwo6tEQO auyu tou Evt61-LOu (3QE8l]xav otllv Jtuvw EJtL<pUVELa twv <pUAAWV, EVW otllV xutw EJtLcpUvELa (3QE8ljXav JtEQW06tEQEC; JtQOvU!-LqJEC;. MEyaM'tEQoc; aQL8!-L6c; JtQOVU!-LcpWv (3QE8l]xE EJtWllC; oto avatoALx6 xm to (36QELO !-LEQoC; twv MvoQUlv. Eva W<pEALI-LO Evt0l-LO ajj$mllC; JtQOEAWOllC;, to Eretmocerus sp., i]tav JtoM aJtOtEAEOI-LOtLX6 otll (3LOAOYLXi] xataJtoAE!-LllOll tou aAEuQWoll otllv KUJtQo.

INTRODUCTION tion levels and gradually spread to other ci­trus-growing areas of the island. In 1985 it

The Japanese bayberry whitefly (JBW), was found at Ayios Theodoros and Mazotos Parabemisia myricae (Kuwana) was found in Larnaca district, in 1986 at Akhelia, Pa­and described in Japan (Kuwana, 1927). phos and in 1987 at Akaki in Nicosia dis­Rose et al. (1981) considered it native to Ja­ trict. It appears that the abundance of citrus pan and possibly other parts of Asia. Among groves and an original freedom from effec­the areas where the JBW has been found are tive biological enemies offered excellent Asia (Mound and Halsey, 1978; USDA, conditions for the dispersal and rapid popu­1978), Hawaii and California (USDA, 1978), lation build-up of this new exotic invader in Israel (Sternlicht, 1979), Turkey (CAB Inter­ some areas. national Institute of Entomology, 1986 cited The damage caused by the JBW is most­by Swirski et al., 1987) and Greece (S. Mi­ ly indirect through the excretion of honey­chelakis, personal communication). It has dew by the immature stages. The honeydew been reported on several plants including ci­ covers the leaves, supports the growth of trus and avocadoes (Mound and Halsey, sooty mold and mixes with airborne dust to 1978; Rose et al., 1981; Swirski et al., form a crust which hinders photosynthesis 1986). In California Rose et al. (1981) consi­ and respiration of the tree. Direct damage dered the JBW a potentially serious citrus through the extraction of sap from the leaves pest when found under no effective natural is significant only at extremely high insect control conditions. densities.

In Cyprus, the JBW was first detected on The purpose of this investigation was to citrus in the Limassol area in 1983 (Depart­ study the bioecology of the JBW and deter­ment of Agriculture, unpublished records). mine its pest potential, with the ultimate ob­In spite of repeated chemical control meas­ jective to develop an effective pest manage­ures against it, it attained explosive popula- ment strategy.

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MATERIALS AND METHODS

The study was carried out at Akhelia, Ay­ios Theodoros and Mazotos. Starting from early February in 1987, when some whitefly adults appeared, several leaves with newly­laid eggs only were marked and checked ev­ery 10 to 21 days. When the fIrst adults of the first generation emerged, new leaves with newly-laid eggs were marked again and the procedure was repeated throughout the year in order to determine the maximum number of generations per year. Concurrent­ly two screen cages 1.5x1.5x2 m were set up at Akhelia for a more accurate study of the JBW life history when pest populations in the open fIeld were low, because of chemical treatments.Heavily infested citrus plants in pots were kept in one of the cages. When the fIrst adults emerged from the overwintering generation, new plants were placed in the cage and exposed to the whitefly adults for oviposition. After having been infested, they were removed and placed in the other cage where they were kept for adult emergence. This procedure was followed throughout the year.

The egg and larval distribution on the leaf surfaces were determined by counting large numbers of the relevant insect stage. Leaves were examined all around the tree at man's height and the sample size depended on the availability of infestation. The larval distribution in the four cardinal quadrants was determined by counting the insects on one leaf at man's height in each direction.

RESULTS AND DISCUSSION

Biology Within-tree distribution. Eggs are oval and pedicelate, measuring approximately 0.2xO.9 mm. Immediately after deposition they are whitish, but they gradually tum black before hatching. They were laid selectively allover newly-formed leaves and sometimes on the green tender shoot tips and newly-formed fruit. Ovipositing females had a preference for the upper leaf surface, as signifIcantly more eggs were generally found on this site (Table 1). The absence of signifIcant differ­ence in the number of eggs found on the two leaf surfaces in April and May could be ex­plained by three factors: a) the high adult whitefly population levels existing in those

months, b) the relatively low availability of leaves suitable for oviposition, and c) the presence of honeydew, excreted by larval in­stars settled on the lower leaf surface, that drops onto the upper surface of underlying leaves, inhibiting oviposition. The correla­tion coeffIcient between eggs laid on the upper leaf surface and those on the whole leaf was 0.99 (P<O.OI).

Table 1. Distribution of Japanese bayberry whitefly eggs on the two leaf surfaces of grapefruit and lemon trees at Akhelia in 1989

Leaf Surface MarchI

Eggs/leaf surface

April2 May3 June4 Mean5

Upper Lower

80.3 a 8.8 b

155.0 a 147.1 a

64.3 a 57.9 a

37.4 a 7.6 b

81.6 a 47.8 b

1,2.3.4.5 Means from 86, 52,60,60 and 258 leaves, re­spectively

Upon emergence, the crawlers search for a suitable place to settle mostly on the lower leaf surface. Counts of 11237 settled larvae revealed 97.9% on the lower leaf surface and 2.1 % on the upper leaf surface (Table 2).

Table 2. Distribution of the Japanese bayberry white­fly larvae on the two leaf surfaces of grape­fruit and lemon trees at Akhelia in 1989

Larvae/leaf surface Leaf Surface April! May2 June3 Mean4

Upper 0.39 0.62 1.20 0.65a Lower 34.59 30.38 24.45 30.56b

1.2.3.4 Means from 100, 200, 60 and 360 leaves, re­spectively.

The correlation coeffIcient between the lar­vae settled on the lower leaf surface and those on the whole leaf was 0.99 (P<O.01). The larval distribution in the four cardinal quadrants varied in time, but on the average signifIcantly more larvae were found in the East and North than in the West and South quadrants (Table 3).

Life history. The JBW overwinters at the larval stage. Last-instar larvae start appear­ing from the third decade of January on­wards, reach a peak in the fIrst half of Febru­ary and gradually drop to insignifIcant numbers in the fIrst half of March. Thereaft­er, they are very rare and their development

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Table 3. Distribution of the Japanese bayberry white­fly larvae in the four cardinal directions on grapefruit and lemon trees at Akhelia in 1989

Larvae/leaf

Orientation April1 May2 June3 Mean4

East 24.48 52.38 69.80 47.53a North 48.00 50.32 27.00 45.79a West 44.04 13.80 2.00 20.23b South 23.40 7.50 3.80 11.30b

1,2,3,4 Means from 25, 50, 15 and 90 leaves, respec­tively.

is completed towards the middle of April. Adult emergence follows the same trend but with about 15 days delay. The development of the over-wintering generation of JBW was greatly affected by the climatological condi­tions and probably by the physiological con­dition of the hostplant on which larval devel­opment occurred. Consequently, inter- and intra-location variations in the insect's devel­opment occurred. Adult emergence from the overwintering generation on a certain host­plant always coincided with the presence of new growth on the hostplant. Insect devel­opment was faster on lemons and grapefruit than on oranges and sour oranges.

The eggs of the fIrst generation are gen­erally laid from the fIrst week of February onwards according to climatological condi­tions. The fIrst settled fIrst-instar and last­instar larvae generally appear at the begin­ning of March and first half of April, respec­tively, and the adults towards the end of April. These adults originate from eggs laid up to the fIrst week of March. Adult emer­gence from the fIrst generation continues for about a month, overlapping with the onset of the third generation. Thus from the onset of the second generation onwards (end of April) there is overlapping of generations and the insect can be found in all developmental stages. In one year it can complete a maxi­mum of nine generations (Fig. 1). Starting from around the fIrst decade of October, all eggs laid hatch and develop through larval stages to give the overwintering generation. No newly laid eggs are generally found after the end of November. Some whitefly adults may be found during December but they per­ish.The JBW reached high population levels in spring and autumn, while it was not abun­

dant in winter and very rare in summer. The very low numbers in the summer are due to the application of insecticides against other pests and to the adverse (dry) climatological conditions. From September onwards the presence of whitefly infestation becomes easily detectable.

Figure 1. Seasonal life history of the Japanese bay­berry whitefly, Parabemisia myricae (Ku­wana), during 1987/88. 1-9:maximum num­ber of generations; shaded areas indicate the minimum duration of each generation.

Biological control The only biological control agents of this

pest determined so far in Cyprus, are the pre­dator Chrysoperla carnea (Stephens) and the parasitoid Eretmocerus sp. The former is a very common general predator but its impact on the pest was not apparent. Eretmocerus mundus Mercet, recorded in Cyprus on Be­misia tabaci (Gennadius) in 1981, did not parasitize the JBW. The parasitoid Eretmoc­erus sp., was recovered for the fIrst time at Mazotos in late 1987 from a signifIcantly high number of parasitized mw last-instar larvae. Adult parasitoid activity was noticed in the fIeld in late January and late March 1988, when adult parasitoids were seen tap­ping fourth-instar larvae of the overwinter­ing and fIrst generation, respectively. In March and April, last-instar larval mortality, mostly due to parasitism, was so high (about 90%) that the whitefly populations at Mazo­tos, starting from the second generation, were almost annihilated. During the summer whitefly populations remained so low that no parasitism could be easily detected. Para­

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sitism became again detectable from October onwards when whitefly population levels were relatively high. During autumn 1988, the whitefly fourth-instar larvae were again practically decimated and pest populations were reduced significantly. Thereafter, JBW infestation at Mazotos remained almost non­existent. Parasitization in a citrus grove at Ayios Theodoros, 10 km away, was detected for the first time in April 1988 at very low levels, but by October it increased considera­bly and a maximum of 94% total mortality of last-instar larvae, most of which due to para­sitism, was observed. During 1989 and 1990, the parasitoid controlled the JBW very effectively at Mazotos and Ayios Theodoros as the pest existed at almost nondetectable levels. At Akhelia, the JBW was free from parasites and its population levels were so high that they warranted chemical control treatments. Twenty live adults of Eretmoc­erus sp. obtained from parasitized whitefly larvae collected at Ayios Theodoros were re­leased at Akhelia in June 1989 in a citrus grove regularly treated with insecticides. Surveys conducted in March 1991 revealed a relatively low pest population level and an abundance of parasitoids indicating that Eretmocerus sp. has been established also at Akhelia.

The origin of the Eretmocerus sp. recov­ered in the present studies at Mazotos and Ayios Theodoros is uncertain. It was initial­ly thought that it could very likely be a case of accidental ecesis and consequently of for­tuitous biological control. Unpublished re­cords of the Department of Agriculture though, show that in May 1985 a small num­ber of pupae of Eretmocerus sp. (Californian origin) were introduced from Israel for estab­lishment. However, fewer than 10 adult in­sects survived, and these were moribund at the time of their release at Ayios Theodoros (Krambias, personal communication). Con­sequently, it is not known whether the Eret­mocerus sp. of the present studies is an in­digenous parasitoid, an accidental introducti­on, or the decendant of the release at Ayios Theodoros. Whatever the origin of the para­sitoid might be, the biological agent showed a remarkable ability of controlling the JBW and of surviving on extremely low popula­tion densities during the summer. The white­fly is presently an insignificant pest because its population levels dropped to an innocuous

rarity. Successful biological control of the JBW was also reported by Rose and DeBach (1982) in California where a parasitoid, again Eretmocerus sp., demonstrated an im­pressive effectiveness in controlling this pest.

ACKNOWLEDGEMENTS

The author wishes to express his appreci­ation for the insect identification which was carried out through the C.A.B. International Institute of Entomology: D.J. Williams & J.H. Martin identified the Japanese bayberry whitefly, A. Polaszek Eretmocerus sp., and B.R. Subba Rao Eretmocerus mundus Mer­cet. Thanks are also due to Mr. A. Georghi­ou, Mr. C. Hadjiyiannis, Mrs. E. Antoniou, Mrs. M. Panayiotou and Mrs. A. Papasolo­montos for technical assistance.

REFERENCES

Kuwana, I. 1927. On the genus of Bemisia (Family Aleyrodidae) found in Japan, with description of a new species. Annotationes zoologicae jap­onensis 11:245-253.

Mound, L.A., and S.H. Halsey. 1978. Whitefly of the world. In A systematic catalogue of the Aley­rodidae (Homoptera) with host plant and natu­ral enemy data. British museum (Natural His­tory) and John Wiley and Sons, Chichester, New York, Brisbane, 340 p.

Rose, M., and P. DeBach. 1982. A native parasite of the bayberry whitefly. Citrograph 67: 272­276.

Rose, M., P. DeBach, and J. Woolley. 1981. Poten­tial new citrus pest: Japanese bayberry white­fly. California Agriculture 35(3/4):22-24.

Sternlicht, M. 1979. Parabemisia myricae, a new pest in Israel. Hassadeh 59:1830-1831 (In He­brew).

Swirski, E., Y. Izhar, M. Wysoki, and D. Blumberg. 1986. Overwintering of the Japanese bayberry whitefly, Parabemisia myricae, in Israel. Phy­toparasitica 14:281-286.

Swirski, E., D. Blumberg, M. Wysoki, and Y. Izhar. 1987. Biological control of the Japanese bay­berry whitefly, Parabemisia myricae (Kuwa­na) (Homoptera:Aleyrodidae), in Israel. Israel Journal ofEntomology 21:11-18.

United States Department of Agriculture. 1978. A whitefly [Parabemisia myricae (Kuwana)]­California-new continental United States re­cord. Cooperative Plant Pest Report 3(44/47): 617.

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