j. enl. Soc. slh. Afr. [992 Vol. 55. No. [, pp.

2[-31

Parasitism of Florida Wax Scale, Ceroplastes floridensis Comstock, on Citrus in Israel

by

YAEL ARGOV
The Israel Cohen Institute for Biological Control, 27 Keren Kayemet St., Rehovot 76345, Israel

BERT SCHNEIDER
Makhteshim Chemical Works, P.O.Box 60, Beer-Sheva 84100, Israel and

DAVID ROSEN
The Hebrew University, Faculty of Agriculture, P.O.Box 12, Rehovot 76100, Israel Population censuses of the Florida wax scale, Ceroplasles jioridensis Comstock (Homoptera: Coccidae), and parasites attacking it were made over a 4-year period between 1983 and Ig87 in 2 citrus groves in Israel. Two annual generations of the scale were produced in both groves. The most abundant parasite was Telrasljehus uroplastae Girault (Hymenoptera: Eulophidae). Peak numbers of parasites were synchronized with peak numbers of hosts susceptible to parasitism. Parasites had a significant effect on the host population in one grove, as determined by life-table analysis. The key stage mortalities occurred at the first and second larval instars and the young female stage. Additional parasites were imported and released during the study; one was not recovered, and the recovery rate for others was very low. Two species were recovered in the study plots and one in home gardens.

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INTRODUCTION
The Israel Cohen Institute for Biological Control at Rehovot, Israel, initiated a project in 1982 to bring the Florida wax scale (FWS), Ceroptastesfioridemis Comstock (Homoptera: Coccidae), under biological control by natural enemies. The major activities included: importing and releasing exotic natural enemies (Argov & Rossler 1988); carrying out population censuses of FWS; and developing a mass production method for culturing FWS in the insectary (Argov et at. IgB7). The major indigenous parasite attacking FWS populations in Israel is Tetrasfichus ceroplastae Girault (Hymenoptera: Eulophidae) (Rosen 1967; Ben-Dov 1972; POOoler et al. 1986; Schneider et al. IgB8). This species, eight additional parasites and the

22

j. ent. SOC. sth. Afr. Vol. 55, NO.1, 1992

predator Chilocorus bipustulatus (L.) (Coleoptera: Coccinellidae) comprise the major biotic mortality factors operating against this pest in Israel. This paper deals with population censuses of FWS in Israel, the effect of parasite populations on this pest of citrus and the recovery rate of released imported parasites.

MATERIALS and METHODS

Description of plots: This study was carried out in two study plots, at Shefayim and Gan Efraim, both in the coastal plain of Israel. The citrus variety planted in Shefayim was Shamouti orange, whereas both Shamouti and Valencia oranges were planted in Gan Efraim. Both groves were ca. 40 years old. The area of each study plot was 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 on June 27, Ig86 during the sampling period with oil plus a nutrient, potassium nitrate. No other insecticides were applied to this grove at least 8 years prior to sampling and during the entire sampling period, with the exception of state-wide Mediterranean fruit fly treatments. These consist of lJL V 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 exception of Mediterranean fruit fly treatments. However, it was located within a larger grove which 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 on each occassion. Each tree was divided in 4 quadrants at the compass directions. Four twigs per quadrant were randomly sampled. The sampling universe consisted of twigs at the tree's periphery and up to a height of 1.5 2 m from the ground. Each twig was ca. 20 em in length, with a variable number ofleaves. Samples were taken to the laboratory for 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 and cause 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, three additional periods in the scale's development are defined on the basis of wax morphology and reproductive state: young female (Yfl, pre-ovipositional female (POf) and ovipositional female (Of). Males are not known. Five stage categories of the FWS were defined for the purposes of this study as: I L l + L2, 2 L3, 3 Yf, 4 - POf, 5 Of. L 1 and L2 were sampled as one stage category because these ins tars are not attacked by parasites. Parasitism was determined by turning over scales and observing the presence of a characteristially darkened ventrum. A visible change in color is detectable when the parasite has reached the later stages of development. Percent parasitism was calculated on the basis of hosts susceptible to parasitism in each sample. To identify the species composition of parasites in these samples, all scales in stage categories susceptible to parasitism (L3 - Of) were incubated in doth-covered plastic cups at ca. 26C for one month. Life tables: Life tables were constructed by the procedure described by Schneider et al. (1987). Briefly, the procedure consists of the following steps: (I) separating scale generations, (2) producing survival curves with a non-increasing sequence 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 Israel

3-cycle moving averages (Sokal & Bryant 1967). This method is based on the idea that during a given time interval each individual has three possible fates: remaining in the same stage (s), progressing to the next stage (p), or dying (d). An assumption of this method is that mortality is proportionally the same in all stage categories at each sampling occasion. This assumption, although not entirely true, does not distort the results because the great majority of scales at anyone sampling occasion are at one or two stage categories. The number of scales entering each stage is calculated by summing Pi where i is the stage category. Example
Time interval Stage category

1000 2 3 4

P2
300

P3

kdi

200
300

500
200

237 237
a

262 34 29 6

100
45

70
kPi
537

50

In the above example, 1000 scales entered the first stage category, 537 entered the second stage category and 296 entered the third stage category.

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Effect of parasites on host populations: The method used to determine the effect 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 of parasitized hosts (N ph ) on a generational basis. Nh values are based on the number of scales 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 described by Southwood (1978). This method involves determining the area under the curve described by Nph vs. cumulative degree-days for the parasite T. ceroplastae for each FWS generation. Daily minimum and maximum temparatures in the study plots were obtained from nearby meteorological stations. Degree-days were calculated by employing the Degday program written by Higley et al. (1986). The developmental threshold for T. ceroplastae, 7C, was obtained from Ben-Dov (1970). The area thus calculated was divided by the developmental constant for this parasite species, 460 degree-days (Ben-Dov 1970), in order to determine the number of parasites acting during that generation (N ph )' The effect of parasites is expressed as the k-value due to parastism (k p ) where:
(N h ) In(Nh-N ph )

Field release and recovery of imported parasites: }'our species of parasites were 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 the Israel Cohen Institute on FWS; and one species from Florida, USA: Metaphycus emptor (Howard) (Hymenoptera: Encyrtidae), obtained from FWS.

J.

ent. Soc. stk. Afr. Vol. 55, No.

I, 1992

RESULTS and DISCUSSION

Phenology: At the study grove in Gan Efraim, two annual generations of the
FWS were produced, in the spring and fall (Fig. I). This is consistent with findings in previous studies (Bodenheimer 1951; Podoler et al. Ig86; Schneider et al. Ig88). Population densities of the stages susceptible to parasitism were exceptionally high in the fall generations of 1983 and 1986. The number of scales in these stages was greater than 6 per twig, and sooty mold was a problem during these periods. The parasite population density during the falI of Ig86 was low. A possible explanation for the reduction in % parasitism during this season could be that chemical treatments were made in the surrounding grove with broad-spectrum insecticides in June and September, Ig85. Percentage of parasitism in this grove also had two annual peaks which lagged behind the susceptible scale population peaks (Fig. I). The dominant parasite was T. ceroplastae,

::r::
0

3
....... available ..... parasitized

~ ~

<

90

IJ:l

1
2

Reproduced by Sabinet Gateway under licence granted by the Publisher (dated 2009).

~ ~
(f.l

::3
(f.l

.--.

< + 0 ~

.....

" ',
II II

>
" " "
"

, ,
\
I,

"I
"

.--. 70~
60 ..... 0 50
E-t 40 ....... (f.l

'-"

"'"'
0
~

0 ......

tlO

.
,, ,
! ,

'" ' "" I' " ,, " , 'I , , "

I I

"

;S .......
<

E-t

:::E 0 Z Z

IJ:l

, ,, ,

30 20
10

0...

" " " t

:::E

< ~

0 6

..

,
...............LJ

~o
12

12

12 1985 1986

17

6 1987

1983

1984

DATE

(months)

Fig.

I.

Phenology of the Florida wax scale, Ceroplastes j/lJridensis, and its parasites on citrus (Gan Efraim).

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

which was recorded on a greater number of sampling occasions and at greater numbers than other indigenous parasites. Of the 46 sampling occasions in this grove, T. ceroplastae was recorded 27 times, Microterys .flavus (Howard) I I times, Metaphycus jlavus (Howard) 3 times 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 in this grove (Fig. 2). A possible explanation for the difference between the two groves is that no broad-spectrum insecticides were applied during the entire sampling period within this grove and in its near vicinity. No damage resulting from sooty mold was observed during the entire study period, except in the winter of 1985, when an unusually high host population was recorded. The % parasitism recorded during this period was inexplicably low. The dominant parasite in this grove was T. ceroplastae, followed by the

::c
Z
~ p::)

u <:

3
.--.. available
"
"

.... parasitized

90
" " " "

Reproduced by Sabinet Gateway under licence granted by the Publisher (dated 2009).

ji:l

r
~
"
" "

80
,-...

0...

rn

2
,-... .......

" " I'

70~

ji:l

<: + U r::: rn ......... s

J:;r..,

....:I

'" , " , , I'

1.
I, I, I, I ,

0
Iil
~
p::)

.-

t:lll 0

" "

"

' ,,
I
I

', '

"
, "I I

" "

1\

" "

Z 60 ...... 0

50 N <:
Eo-< 40 ...... rn

Eo-<

......

,
\
~

30 20

::;,
Z Z

0...
10 0

<:

<:

ji:l

, , , ,
I

"
1983

12 1984

12 1985

12 1986

12 5 1987

DATE (months)

Fig.

2.

Phenology of the Florida wax scale, Ceroplastes ftoridensis, and its parasites on citrus (Shefayim).

J.

ent. Soc. 5th. Afr. Vol. 55, No.1, 1992

other indigenous species. Of the 47 samples taken in this grove, T. ceroplastae was recorded 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 presented in Table I. The graphical presentation of phenology (Figs 1,2) is consistent with life table 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 populations during these seasons (Table I). The Lg population is indicative of the number of hosts susceptible 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 in Shefayim (Fig. 2) are also apparent in the Lg populations during these generations (Table I). This consistency between raw data presented in the graphs and processed data 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 I srad. LI-L2 L3 Gan Efraim 273 1 45 8 189 993 338 334 901 Shefayim Yf 1988 32 4 96 700 27 6 227 645
POf

Of 92 4 45 119 3.5 [9 206

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fall 1983 spring 1984 fall 1984 spring 1985 fall 1985 spring 1986 fall 1986

5 216 [ 076 27 2 1 743 2242 I 176 128 3

411 20 57 29[ [58 79 573

spring 1983 fall 1983 spring 1984 fall 1984 spring 1985 fall 1985 spring 1986

3740 357 1116 143 997 I 123 6028

358 21 ! 12 5 [3 2 349 944 103

293 194 94 114 301 860 773

65 73 18 55 175 62 9 19

19 4' 9 33 27 34 0 8

Two aspects of population dynamics which are not evident from analysis of raw data and can be analysed in life tables are density-dependent mortality and key-factor mortality. Density-dependent mortality: The presence of density-dependent mortality was determined by employing the test for density dependence as described by Varley et al. (1973). This test is carried out by regressing log Ni on log N i+ I where N is the number of individuals and i is the stage category. Significant density dependence is verified when the regression coefficient, b, is significant (P<O.05) and when b ofiog Ni on log N,+ I and log N i+ 1 on log Ni are on the same side and significantly different from 1 (unity). No significant density dependence was found in either grove. This finding is consistent with results of a previous study (Schneider et al. 1987).

Argov el al.: Parasitism oj Florida Wax Scale in Israel

27

Key-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 this study is based on the graphical method described by Varley et at. (1973) and the regression method described by Podoler & Rogers (1975). Varley's method involves graphing k; values (defmed as log N; log N j + d vs. the generation and determining which kj value most closely resembles the total generation mortality K, (where K=k l +k z+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 the largest regression coefficient is the key factor (Table 2). The stage categories in which key-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 results obtained in previous work (Schneider et al. 1987; Oliver & Chapin 1981).
TABLE 2. Key-factor analysis hased 011 Podoler & Rogers' method. Regression cociIicicnts

stan-

dard errors or k. vs. K. Gan Erraim 0,23 -0,05 0,52 0,30 0,20

0,14 0.04
0.16 0,08 0,08

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0,41 0,04 0,47 0,08

o,r 7

0,09 0,11 0,13

0,10
0,1 I

The ellect of parasites on FWS populations in these two groves was determined according to the method described earlier and expressed as kp values (Table 3). Mortality due to parasitism (k p) was generally greater in Shefayim then in Gan Efraim (Table 3). However, key-factor analysis based on Podoler & Rogers' method (Table 2) indicates that tll<' action of parasites as a factor is similar in both groves.

TABLE 3. The number of TeiraslichuJ ceroplastae acting on F\VS populations, N ph ' in two groves in Israel and their kp values.

Gan Efrairn spring 1983 fall 198:1 spring 1984 fall 198.4 spring 1985 fall 1985 spring 1986 fall 1986 297 13 2 87

Shefayim 0,77 oA3 0,5 2

0,1 I

1460

30 4
67 73
liZ

62
22

033 0,47 0,19 0,03 0,17 0,09

O,OI

30
~L)

112
-80 .)

0,07 0,05 0,32

28

J.
2

ent. Soc. sth. Afr. Vol. 55, No.

I,

1992

::.::
0

.!i;

...
0

.!i;

&.

l;

Reproduced by Sabinet Gateway under licence granted by the Publisher (dated 2009).

.,
0

..
I

:i
0

F83

884

F84

S85

F85

S86

F86

Generation (Gan Efraim)

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

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

3

29

::.:: 2

.!>:

.
0

.!>:

..
0

.!>:

'!:.

Reproduced by Sabinet Gateway under licence granted by the Publisher (dated 2009).

.,
.!>:

..
I

:i

1-

0 S83 F83 S84 F84 S85 F85 S86

Generation (Shefayim)
Fig. 4. Key-factor mortality analysis based On Varley's method (see text) in Shefayim.

30
TABLE

j. ent. Soc. 5th. Afr. Vol. 55, No.1, 1992

4. Release and recovery of four imported parasites against the Florida wax scale on citrus in Israel.
M. clauseni
AI. speciosus
;\,1. eruptor

C. hawaiiensis

Shefayim Date of first release Date of last release

12.10.83

# parasites # releases # recoveries

160

90

27

Gao Efraim Date of first release Date of last release # parasites # releases # recoveries
28.1 L83 12.10.83 12.10.83

23-4- 87 27.'l3

23-4- 87 38 37 0

29
2

33

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Field release and recovery of introduced parasites. The release and recovery of imported parasites is presented in Table 4. Recovery was recorded for only two of the four species in both groves, at a very low 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 places emphasis on the effect of parasites on its populations. Findings in this study regarding the lack of density-dependent mortality and the presence of key stage mortalities in 1.1-L2, Yf and PDf are consistent with previous studies. The eHect of parasites in this work was generally greater than in a previous study carried out in Israel (Schneider el al. 1988). The reason for wide fluctuations in % parasitism and their effect on host populations as measured by kp values from grove to grove and season to season are not known. However, broad-spectrum insecticides applied even in the near vicinity may have an adverse effect on parasite activity, as implied in this study. Imported exotic parasite species reared and released during this study did not become established. However, in view of the absence of density-dependent mortality in this system, the search for additional parasites and conservation of existing parasites are believed to be important to the eventual success of bringing the FWS under biological control. ACKNOWLEDGEMENTS The authors are grateful to Dr. H. Kajita, Kyushu University, Fukuoka,Japan and Dr. Ru Nguyen, Division of Plant Industry, Gainesville, Florida, for collecting and sending shipments of Ceroplastes parasites. We gratefully acknowledge Mrs. M. Tsamry and Mrs. W. Domareiski, The Israel Cohen Institute for Biological Control, Rehovot, for

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 during the study.
REFERENCES
ARGOV, Y., H. PODOLER, O. BAR-SHALOM & D. ROSEN. 1987. Mass rearing of the Florida wax scale, Ceroplastes jloridensis, for production of natural enemies. Phytoparasitica 15: 277- 287. ARGOV, Y. & Y. ROSSLER. 1988. Introduction of beneficial insects into Israel for the control of insect pests. Phytoparasitiea 16: 303-315. BEN-DOV, Y. 1972. Tetrastiehus ceroplastat (Girault) (Hymenoptera: Eulophidae), a parasite of the Florida wax scale, Ceroplastts foridensis (Homoptera: Coccidae) on citrus in Israel. Journal oj the Entomological Socie!>, oj Southern 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 calculating degree-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-II7 OLIVER, A.D. & J.B. CHAPIN. IgSl. Seasonal history and population dynamics of Florida wax scale, Ceroplastes foridensis Comstock (Homoptera: Coccidae), on Dahoon holly in Louisiana. Proceedings oj the Louisiana Academy oj Science 44: 29-36. PODOLER, H., Y. DREISHPOUN & D. ROSEN. 1981. Population dynamics of the Florida wax scale, Ceroplastes foridensis (Homoptera: Coccidae) on citrus in Israel. 1- A partial life table. Acta Oecologica/Oecologia Applicata lI: 81-91. PODOLER, H. & D. ROGERS. 1975. A new method for the identification of key factors from life-table data. Journal oj Animal Ecology 44: 85-114. ROSEN, D. 1967. The hymenopterous parasites of soft scales on citrus in Israel. Beitrage zur Entomologie 17: 251-279. SCHNEIDER, B., H. PODOLER & D. ROSEN. 1987. Population dynamics of the Florida wax scale, Ceroplastesforidensis (Homoptera: Coccidae) on citrus in Israel. 4.- Abundance. Acta Oecologica/Oecologia Applicata 8: 217-228. SCHNEIDER, B., H. PODOLER & D. ROSEN. IgS8. Population dynamics of the Florida wax scale, Ceroplastes foriJensis (Homoptera: Coccidae) on citrus in Israel. 5.- Effect of the parasite, Tetrastiehus eeroplastae (Girault). Acta Oecologica/Oecologia Applicata 9: 75-83. SOKAL, RR. & E.H. BRYANT. 1967. Computing a budget from sequentially sacrificed replicated cultures. Researches on Pupulation Ecolog)' 91 10- 11. SOUTHWOOD, T.R.E. 1978. Ecological MeiltoJs, witlt partiCl/lar nJtrnlCI to the study oj insect populations. 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.

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Accepted 9July

1991