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22 j . ent. SOC. sth. Afr. Vol. 55, NO.1, 1992predator Chilocorus bipustulatus (L.) (Coleoptera: Coccinellidae) comprise the major bioticmortality factors operating against this pest in Israel.This paper deals with population censuses of FWS in Israel, the effect ofparasite populations on this pest of citrus and the recovery rate of released importedparasites.

MATERIALS and METHODSDescription of plots: This study was carried out in two study plots, atShefayim and Gan Efraim, both in the coastal plain of Israel. The citrus variety plantedin Shefayim was Shamouti orange, whereas both Shamouti and Valencia oranges wereplanted in Gan Efraim. Both groves were ca. 40 years old. The area of each study plotwas ca. 25 ha.The Shefayim grove was sampled during the period between May 1983 and

May 1987. This grove was sprayed with mineral oil before sampling commenced and onJune 27, Ig86 during the sampling period with oil plus a nutrient, potassium nitrate. Noother insecticides were applied to this grove at least 8 years prior to sampling and duringthe entire sampling period, with the exception of state-wide Mediterranean fruit flytreatments. These consist of lJLV malathion bait sprays applied in aerial strips.

The study plot in Gan Efraim was sampled between June I983 and June 1987.It was not treated with insecticides during the entire sampling period, with the exceptionof Mediterranean fruit fly treatments. However, it was located within a larger grovewhich did receive broad-spectrum pesticide treatments.Sampling: Sampling was carried out once a month in each study grove.Twenty-four trees were chosen randomly at the outset of this study and were sampled oneach occassion. Each tree was divided in 4 quadrants at the compass directions. Fourtwigs per quadrant were randomly sampled. The sampling universe consisted of twigs atthe tree's periphery and up to a height of 1.5 2 m from the ground. Each twig was ca.2 0 em in length, with a variable number ofleaves. Samples were taken to the laboratoryfor processing. The following parameters were determined with the aid of a stereomicroscope: number and stage of FWS, status of each individual, i.e. alive or dead andcause of death when known. The FWS undergoes three molts during its development.The larval instars are defined as LI, L2 and L3. Subsequent to the last larval molt, threeadditional periods in the scale's development are defined on the basis ofwax morphologyand reproductive state: young female (Yfl, pre-ovipositional female (POf) and ovipositional female (Of). Males are not known. Five stage categories of the FWS were definedfor the purposes of this study as: IL l +L2, 2 L3, 3 Yf, 4 - POf, 5 Of. L 1 and L2were sampled as one stage category because these ins tars are not attacked by parasites.Parasitism was determined by turning over scales and observing the presenceof a characteristially darkened ventrum. A visible change in color is detectable when theparasite has reached the later stages of development. Percent parasitism was calculatedon the basis of hosts susceptible to parasitism in each sample. To identify the speciescomposition of parasites in these samples, all scales in stage categories susceptible toparasitism (L3 - Of) were incubated in doth-covered plastic cups at ca. 26C for onemonth. Life tables: Life tables were constructed by the procedure described bySchneider et al. (1987). Briefly, the procedure consists of the following steps: (I )separating scale generations, (2) producing survival curves with a non-increasingsequence of population densities from the initial highest to the final lowest density using


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Argov et al.: Parasitism oj Florida Wax Scale in Israel3-cycle moving averages (Sokal & Bryant 1967). This method is based on the idea thatduring a given time interval each individual has three possible fates: remaining in thesame stage (s), progressing to the next stage (p), or dying (d). An assumption of thismethod is that mortality is proportionally the same in all stage categories at eachsampling occasion. This assumption, although not entirely true, does not distort theresults because the great majority of scales at anyone sampling occasion are at one ortwo stage categories. The number of scales entering each stage is calculated by summingPi where i is the stage category.ExampleTime Stage categoryinterval P2 2 P3 3 kdi1000

300 2002 500 300237 262 1003 200 237a 34 454 70 50kPi 537 296

In the above example, 1000 scales entered the first stage category, 537 entered the second stagecategory and 296 entered the third stage category.Effect of parasites on host populations: The method used to determine theeffect of parasites on nvs populations was similar to that described by Schneider et al.(1988). It involved determining the density of susceptible host stages ( ~ h ) and ofparasitized hosts (N ph ) on a generational basis. Nh values are based on the number ofscales entering the L3 stage, since L3 is the first stage that is susceptible to parasitism.Generational Nph values were determined by employing a graphical method describedby Southwood (1978). This method involves determining the area under the curvedescribed by Nph vs. cumulative degree-days for the parasite T. ceroplastae for each FWSgeneration. Daily minimum and maximum temparatures in the study plots wereobtained from nearby meteorological stations. Degree-days were calculated by employing the Degday program written by Higley et al. (1986). The developmental threshold forT. ceroplastae, 7C, was obtained from Ben-Dov (1970). The area thus calculated wasdivided by the developmental constant for this parasite species, 460 degree-days(Ben-Dov 1970), in order to determine the number of parasites acting during thatgeneration (N ph ) ' The effect of parasites is expressed as the k-value due to parastism (kp )where:

(Nh ) In(Nh-Nph )Field release and recovery of imported parasites: }'our species of parasiteswere imported, propagated and released during the course of this study (Argov &Rossler, 1988). Three species from Japan: Coccophagus hawaiiensis Timberlake (Hymenoptera: Aphelinidae), MicToterys clauseni Compere and M. speciosus Ishii (Hymenoptera: Encyrtidael, obtained from Ceroplastes japonicus Green and reared at theIsrael Cohen Institute on FWS; and one species from Florida, USA: Metaphycus emptor(Howard) (Hymenoptera: Encyrtidae), obtained from FWS.


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Argov et at.: Parasitism of Florida Wax Scale in Israelwhich was recorded on a greater number of sampling occasions and at greater numbersthan other indigenous parasites. Of the 46 sampling occasions in this grove, T. ceroplastaewas recorded 27 times, Microterys .flavus (Howard) I I times, Metaphycus jlavus (Howard) 3times and Scutellista cyanea Motschulsky (Hymenoptera: Pteromalidae) 2 times.At Shefayim the FWS produced two annual generations, as in Gan Efraim.However, the apparent effect of parasites on their host population was much greater inthis grove (Fig. 2). A possible explanation for the difference between the two groves isthat no broad-spectrum insecticides were applied during the entire sampling periodwithin this grove and in its near vicinity. No damage resulting from sooty mold wasobserved during the entire study period, except in the winter of 1985, when an unusuallyhigh host population was recorded. The % parasitism recorded during this period wasinexplicably low. The dominant parasite in this grove was T. ceroplastae, followed by the

::c 3u .--.. available . . . . parasitizedZ


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J. ent. Soc. 5th. Afr. Vol. 55, No.1, 1992other indigenous species. Of the 47 samples taken in this grove, T. ceroplastae wasrecorded in 17, Microterys Jlavus in 8, Moranilla californica (Howard) (Hymenoptera:Pteromalidae) in 2 and Metaphycus flavus in 1 sample.Life tables: Life tables of the FWS in Gan Efraim and Shefayim are presentedin Table I . The graphical presentation of phenology (Figs 1,2) is consistent with lifetable presentation. Three peaks of susceptible host population density, in fall 1983,spring 1985 and fall 1986 in Gan Efraim (Fig. I) are also apparent in the Lg populationsduring these seasons (Table I) . The Lg population is indicative of the number of hostssusceptible to parasitism, since it is the first stage which can be attacked by parasites.Two peaks of susceptible host population density in fall 1985 and spring 1986 inShefayim (Fig. 2) are also apparent in the Lg populations during these generations(Table I) . This consistency between raw data presented in the graphs and processeddata presented in life tables, provides confidence in the method ofiife table construction.

TABLE l. Life tables of the Florida wax scale, Ceroplastes jioridensis, in two citrus groves in Israd.

LI-L2 L3 Yf POf OfGan Efraimfall 1983 5 216 2731 1988 411 92spring 1984 [ 076 458 32 4 20 4fall 1984 27 2 189 96 57 45spring 1985 1 743 993 700 29[ 119fall 1985 2242 338 276 [58 3.5spring 1986 I 176 334 227 79 [9fall 1986 1283 901 645 573 206

Shefayimspring 1983 3740 358 293 65 19fall 1983 357 21 ! 194 73 4'spring 1984 1116 125 94 18 9fall 1984 143 [32 114 55 33spring 1985 997 349 301 175 27fall 1985 I 123 944 860 62 9 340spring 1986 6028 I 103 773 19 8

Two aspects ofpopulation dynamics which are not evident from analysis of rawdata and can be analysed in life tables are density-dependent mortality and key-factormortality.Density-dependent mortality: The presence of density-dependent mortalitywas determined by employing the test for density dependence as described by Varley etal. (1973). This test is carried out by regressing log Ni on log Ni+ I where N is the numberof individuals and i is the stage category. Significant density dependence is verified whenthe regression coefficient, b, is significant (P


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Argov el al.: Parasitism oj Florida Wax Scale in Israel 27Key-factor analysis and the effect of parasites on their host populations:Key-factor analysis was introduced by Morris (1957) and developed by Varley &

Gradwell (1960), Podoler & Rogers (1975) and Manly (1977). Key-factor analysis in thisstudy is based on the graphical method described by Varley et at. (1973) and theregression method described by Podoler & Rogers (1975). Varley's method involvesgraphing k; values (defmed as log N; log N j + d vs. the generation and determiningwhich kj value most closely resembles the total generation mortality K, (whereK=k l +kz+k,+k 4 ) in direction and magnitude from generation to generation (Figs 3,4).Podoler & Rogers' method is based on regression ofk; vs. K. The k; which produces thelargest regression coefficient is the key factor (Table 2). The stage categories in whichkey-factor mortality occurred were LI-L2 and Yf This is most evident in Shefayim (Fig.4 and Table 2). Key-factor mortality in Gan Efraim occurred also in the preovipositional stage (Fig. 4 and Table 2). These results are consistent with resultsobtained in previous work (Schneider et al. 1987; Oliver & Chapin 1981).

TABLE 2. Key-factor analysis hased 011 Podoler & Rogers' method. Regression cociIicicnts standard errors or k. vs. K.

0,23 0,14-0,05 0.040,52 0.160,30 0,080,20 0,08

Gan Erraim0,41 0,090,04 0,110,47 0,130,08 0,10o,r 7 0,1 I

The ellect of parasites on FWS populations in these two groves was determinedaccording to the method described earlier and expressed as kp values (Table 3).Mortality due to parasitism (kp) was generally greater in Shefayim then in GanEfraim (Table 3). However, key-factor analysis based on Podoler & Rogers' method

(Table 2) indicates that tll


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J. ent. Soc. sth. Afr. Vol. 55, No. I , 1992

F83 884 F84 S85 F85 S86 F86Generation (Gan Efraim)

Fig. 3. Key-factor mortality analysis based on Varley's method (see text) in Gan Efraim.


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30 j . ent. Soc. 5th. Afr. Vol. 55, No.1, 1992TABLE 4. Release and recovery of four imported parasites against the Florida wax scale on citrus in

Israel.

Date of first releaseDate of last release# parasites# releases# recoveries

Date of first releaseDate of last release# parasites# releases# recoveries

M. clauseni AI. speciosus ;\,1. eruptor

3 16027

28.1 L8323-4-8727.'l329

2

Shefayim12.10.83

Gao Efraim12.10.83

23-4-8738 370338

C. hawaiiensis

90

12.10.83

Field release and recovery of introduced parasites. The release andrecovery of imported parasites is presented in Table 4.Recovery was recorded for only two of the four species in both groves, at a verylow rate. Recovery for M. clauseni was recorded on citrus in home gardens.COKCLUSIONS

This study deals with population dynamics of the Florida wax scale and placesemphasis on the effect of parasites on its populations. Findings in this study regardingthe lack of density-dependent mortality and the presence of key stage mortalities in1.1-L2, Yf and PDf are consistent with previous studies. The eHect of parasites in thiswork was generally greater than in a previous study carried out in Israel (Schneider elal. 1988). The reason for wide fluctuations in % parasitism and their effect on hostpopulations as measured by kp values from grove to grove and season to season are notknown. However, broad-spectrum insecticides applied even in the near vicinity mayhave an adverse effect on parasite activity, as implied in this study. Imported exoticparasite species reared and released during this study did not become established.However, in view of the absence of density-dependent mortality in this system, thesearch for additional parasites and conservation of existing parasites are believed to beimportant to the eventual success of bringing the FWS under biological control.

ACKNOWLEDGEMENTSThe authors are grateful to Dr. H. Kajita, Kyushu University, Fukuoka,Japan

and Dr. Ru Nguyen, Division of Plant Industry, Gainesville, Florida, for collecting andsending shipments of Ceroplastes parasites. We gratefully acknowledge Mrs. M. Tsamryand Mrs. W. Domareiski, The Israel Cohen Insti tute for Biological Control, Rehovot, for


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Argov et al.: Parasitism of Florida Wax Scale in Israel

technical assistance. We thank Dr. Y. Rossler, The Israel Cohen Institute, and Dr. S.Steinberg, Faculty of Agriculture, Rehovot, for computer assistance and advice duringthe study.REFERENCES

ARGOV, Y., H. PODOLER, O. BAR-SHALOM & D. ROSEN. 1987. Mass rearing of the Floridawax scale, Ceroplastes jloridensis, for production of natural enemies. Phytoparasitica 15:277-28 7.

ARGOV, Y. & Y. ROSSLER. 1988. Introduction of beneficial insects into Israel for the control ofinsect pests. Phytoparasitiea 16: 303-315.BEN-DOV, Y. 1972. Tetrastiehus ceroplastat (Girault) (Hymenoptera: Eulophidae), a parasite of theFlorida wax scale, Ceroplastts foridensis (Homoptera: Coccidae) on citrus in Israel. Journal

oj the Entomological Socie!>, ojSouthern AJrica 35: 17-34.BODENHEIMER, F.S. 1951. Citrus Entomology in the Middle East. W. Junk, The Hague, 663 pp.HIGLEY, L.G., L.P. PEDIGO & K.R OSTLIE. 1986. DEGDAY: A program for calculatingdegree-days, and assumptions behind the degree day approach. Environmental Entomology

15: 999- 1016.MANLY, B.F.J. 1977. The determination of key factors from life table data. Oecologia (Berl.) 31:

11I-II7OLIVER, A.D. &J.B. CHAPIN. IgSl. Seasonal history and population dynamics of Florida waxscale, Ceroplastes foridensis Comstock (Homoptera: Coccidae), on Dahoon holly in Louisiana. Proceedings oj the Louisiana Academy ojScience 44: 29-36.PODOLER, H., Y. DREISHPOUN & D. ROSEN. 1981. Population dynamics of the Florida waxscale, Ceroplastes foridensis (Homoptera: Coccidae) on citrus in Israel. 1- A part ial life table.Acta Oecologica/Oecologia Applicata l I : 81-91.PODOLER, H. & D. ROGERS. 1975. A new method for the identification of key factors fromlife-table data. Journal ojAnimal Ecology 44: 85-114.ROSEN, D. 1967. The hymenopterous parasites of soft scales on citrus in Israel. Beitrage zurEntomologie 17: 251-279.SCHNEIDER, B., H. PODOLER & D. ROSEN. 1987. Population dynamics of the Florida waxscale, Ceroplastesforidensis (Homoptera: Coccidae) on citrus in Israel. 4.- Abundance. ActaOecologica/Oecologia Applicata 8: 217-228.SCHNEIDER, B., H. PODOLER & D. ROSEN. IgS8. Population dynamics of the Florida waxscale, Ceroplastes foriJensis (Homoptera: Coccidae) on citrus in Israel. 5.- Effect of theparasite, Tetrastiehus eeroplastae (Girault). Acta Oecologica/Oecologia Applicata 9: 75-83.SOKAL, RR. & E.H. BRYANT. 1967. Computing a budget from sequentially sacrificed replicatedcultures. Researches on Pupulation Ecolog)' 91 10- 11.SOUTHWOOD, T.R.E. 1978. Ecological MeiltoJs, witlt partiCl/lar nJtrnlCI to the study oj insectpopulations. John Wiley & Sons, New York, 524 pp.VARLEY, G.C., G.R. GRADWELL & M.D. HASSELL. 1973. JIISfft PopwlQtilJll Ecology, aI/analYtical

approaclt. Blackwell, Oxford, III II pp.Accepted 9July 1991

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