Journal of Phytopathology and Pest Management 7(1): 43-53, 2020
pISSN:2356-8577 eISSN: 2356-6507
Journal homepage: http://ppmj.net/
Corresponding author:
Aly A. Abd-Ella,
E-mail: aly.abdella@aun.edu.eg
43
Copyright © 2020
Population fluctuations of oystershell scale insect,
Lepidosaphes ulmi
(L.) (Homoptera: Diaspididae) on
certain olive varieties and the factors affecting its
population
Aly A. Abd-Ella
1*
, Yehia A. Abdel-Rahman
2
, Gaber H. Abou-Elhagag
1
, Ayman S. Gaber
2
1
Plant Protection Department, Faculty of Agriculture, Assiut University, 71526 Assiut, Egypt
2
Plant Protection Department, Faculty of Agriculture, Al-Azhar University, Assiut, Egypt
Abstract
Keywords: Lepidosaphes ulmi, population fluctuation, Aphytis spp., weather factors, olive varieties.
44
1. Introduction
The olive (
Olea europaea
L.), a long-
lived evergreen, is one of the most
economically horticultural crops in Egypt
and worldwide. Most olive growing
countries are localized in the
Mediterranean basin which has more than
90% of the world’s cultivated olive trees.
Olive trees are subjected to attack by
several insect pests that had a harmful
effect on the quality and quantity of the
olive yield. Oystershell scale,
Lepidosaphes ulmi
(L.) (Homoptera:
Diaspididae) is one of the most important
insect pests that causes severe damages to
olive trees (Milek & Simala, 2012;
Argyriou & Kourmadas, 1981).
L. ulmi
is
a polyphagous species and having more
than 150 hosts. It feeds on various fruit
and forest trees, shrubs and ornamental
plants, including olive trees ( Milek et al.,
2017; Alford, 2014; Milek & Simala,
2012; Mansour et al., 2011; Dminic et al.,
2010; Katsoyannos & Stathas, 1995). It is
a cosmopolitan species capable of living
in different climatic regions. It infests
numerous plant species from different
families and is spread all over the
Mediterranean basin (Ferris, 1937).
L.
ulmi
infestation causes discoloration of
the leaf and premature deterioration of
the leaf; the infested fruit is unsightly,
spotted and discolored, and may drop
prematurely. This scale insect can kill
branches and young trees, and if left
unchecked, mature plants will seriously
weaken and stunt (Gill, 1997). Even light
infestations can cause great economic
losses because of a zero tolerance policy
for exported fruits (Helsen et al., 1996).
The hymenopterous parasitoid
Aphytis
spp. was recorded as a natural enemy of
L. ulmi
(Stathas et al., 2005; Erol &
Yaşar, 1999; Boulancer, 1965). Ozgokce
et al. (2016) found that one of the main
causes of
L. ulmi
mortality in apple trees
was parasitization with the aphelinide,
Aphytis mytilaspidis
(Le Baron), which
mainly attacks the egg stage, but can also
be found in adult females. Where, the
percentage parasitism ranged between 22
and 36 % during the egg stage. The
objectives of this study are to identify the
seasonal changes in the population of
oystershell scale,
L. ulmi
on different
olive varieties in Assiut Governorate,
Egypt to survey
L. ulmi
parasitoids on
olives, to evaluate the rate of natural
mortality of
L. ulmi
that caused by
parasitoids, and to assess the effect of
certain weather factors on the population
fluctuation of
L. ulmi
and its associated
parasitoids.
2. Materials and methods
Two seasons of study were conducted on
three olive varieties, Picual, Coratina and
Chemlali to determine the population
density and fluctuation of
L. ulmi
on
olive trees and its associated natural
enemies as well effect of weather factors
on the population of
L. ulmi
and its
associated parasitoids. These
experimental trials were conducted at the
Faculty of Agriculture Experimental
Farm, Assiut University, Assiut, Egypt
during 2017-2018 and 2018-2019
seasons. This farm is a rather mosaic
agro-ecosystem characterized by isolated
areas of olive.
2.1 Survey and population fluctuations
of oystershell scale insect and its
associated natural enemies inhabiting
olive trees
2.1.1 Experimental layout and
population fluctuations of the scale
insect pest
The experimental area was divided into
three lines for three varieties, Picual,
45
Coratina and Chemlali. Each tree divided
into three levels (bottom, middle and top
level). From each tree level, Half-
monthly samples of 10 leaves were taken
at random and were kept in a
polyethylene bag, then were transferred
to the laboratory for examination. The
numbers of
L. ulmi
(nymphs and adults)
were counted on both sides (upper and
lower surfaces) of leaves under a
stereomicroscope for each inspection
date.
2.1.2 Population fluctuations of
oystershell scale insect parasitoids
Even as the
L. ulmi
numbers were
recorded on the leaves; the parasitized
oystershell scale insects were counted
too. The scales, which have a minute hole
because of the parasitoid emergence,
were considered as parasitized ones.
Also, samples of the three scale insect
emerged parasitoid adults were kept in
vials containing 75% ethyl alcohol for
identification according to (Abou-
Elhagag, 2004). The percentage of
L.
ulmi
parasitism was calculated during
2018/2019 season based on the following
formula:




2.2 Effect of three weather factors on
population fluctuations of oystershell
scale insect and associated parasitoids
inhabiting olive trees
2.2.1 Meteorological data
The daily records of the day maximum
temperature, minimum temperature and
the daily mean relative humidity were
obtained from the meteorological station
located close to the experimental area at
the University of Assiut Experimental
Farm
during 2017-2018 and 2018-2019
seasons.
2.3 Statistical analysis
Data were analyzed as a one-way
ANOVA and were presented as means
SEM (Standard Error of Mean).
Correlation coefficient values (r) were
first estimated by SPSS software ver. 16.
The counted populations of the pest or
the parasitoids were considered as the
dependent variate (Y), while the reading
of corresponding weather factors
represented the independent variate (X).
Figures and statistical analysis were done
using GraphPad Prism version 5.0.0 for
Windows, GraphPad Software, San
Diego, California USA,
www.graphpad.com.
3. Results and Discussion
3.1 Population density and fluctuation
of oystershell scale insect,
L. ulmi
Data presented in Figures 1 and 2 shows
the mean monthly population count of
oystershell scale insect,
L. ulmi
(nymph
and adult stages) on olive varieties
picual, coratina and chemlali leaves
during 2017-2018 and 2018-2019
seasons. During 2017-2018 season, the
pest population started with an average
number of 7.0 insects / 10 leaves on
April (Max. temp. 33.2 °C, Min. temp.
14.4 °C and RH 25%) and progressively
increased throughout January (10.28),
February (13.72) and March (15.56)
insect/ 10 leaves on picual variety.
Whereas on coratina variety, the
population started with an average
number of 5.06 insect/ 10 leaves on April
46
and progressively increased throughout
January (5.72), February (4.67) and
March (8.28 insect/ 10 leaves). While on
chemlali variety, the pest population
started during the season with a
population level around 8.0 insect/ 10
leaves during April, December, January,
and February then increased during
March to be 11.67 insect/ 10 leaves
(Figure 1).
Figure 1: Population fluctuations of the oystershell scale insect, L. ulmi on the
leaves of certain olive varieties and some prevailing weather factors during 2017-
2018 season.
During 2018-2019 season, the population
of oystershell scale insect,
L. ulmi
started
with high monthly mean in April (12.78
insect/ 10 leaves) and in June with an
average of 14.61
insect/ 10 leaves for
picual variety.
Thereafter, the population
decreased slightly during December,
January, and February and in March
reached its lowest level, where it was
5.78, 3.37, 4.78, and 3.84 insect/ 10
leaves, respectively. In coratina variety,
the maximum population recorded
during May, June, July and November;
the population ranged from 7.11 to 7.39
insects / 10 leaves, whereas the lowest
population recorded during December
47
(3.39 insect/ 10 leaves), January (2.84
insect/ 10 leaves), February (4.45 insect/
10 leaves), and March (3.84 insect/ 10
leaves). The population of the pest was
on the chemlali variety started on April
with an average of 6.73 insect/ 10 leaves
and reached the highest number during
May (8.52 insect/ 10 leaves), June (9.06
insect/ 10 leaves), July (9.12 insect/ 10
leaves), August (9.67 insect/ 10 leaves)
and September (8.05 insect/ 10 leaves),
whereas the lowest population recorded
on December (4.39), January (3.56),
February (4.33) and March (4.11 insect/
10 leaves) (Figure 2). Data of both
seasons clearly indicated that, the pest
population was reached its peak during
the period from April to September. The
highest average of oystershell scale
insect,
L. ulmi
population was recorded
on picual variety (7.81 and 8.96 insect/
10 leaves) compared to the other
varieties coratina (4.72 and 5.01 insect/
10 leaves) and chemlali (6.88 and 6.73
insect/ 10 leaves) during 2017-2018 and
2018-2019 seasons, respectively.
Cavalloro (1984) stated that, oystershell
scale insect,
L. ulmi
population are lost
during winter owing to the harvest or to
the falling of olives.
Figure 2: Population fluctuations of the oystershell scale insect, L. ulmi on the leaves of
certain olive varieties and some prevailing weather factors during 2018-2019 season.
48
3.2 Factors affecting the oystershell
scale insect,
L. ulmi
, population
3.2.1 The parasitoids,
Aphytis
spp.
Survey of
L. ulmi
parasitoids resulted in
two species of parasitoids,
Aphytis
chrysomphali
(Mercet) and
Aphytis
disppidis
(Howared) (Hymenoptera:
Aphelinidae) in the Faculty of
Agriculture Experimental Farm, Assiut
University, Egypt. Seasonal variation of
the percentage of parasitism by
Aphytis
spp. in the oystershell scale insect,
L.
ulmi
on three olive varieties picual,
coratina and chemlali during 2018-2019
season showed in Figure (3 A and B).
Data presented in Figure (3 A and B)
indicated that, the average percentage of
parasitism was relatively high during
April, May, June, July, August and
September with an average of 4.79, 5.29,
4.74, 7.10, 6.52 and 5.76 % on picual
variety, respectively. Meanwhile, the
lowest average percentage of parasitism
was recorded on October, November,
December, January and March with an
average of 0.50, 3.45, 3.85, 1.47 and
2.44%.
Figure 3: Population fluctuations of the oystershell scale insect, L. ulmi and monthly average parasitism
by Aphytis spp. on olive varieties picual, coratina and chemlali and some prevailing weather factors
during 2018-2019 season.
49
On coratina variety, the average
percentage of parasitism was relatively
high during April, May, September,
December, and January with an average
of 4.01, 5.20, 4.22, 6.98 and 7.92 %, and
the lowest record was on June, July,
August, October and November with an
average of 2.46, 1.98, 1.35, 3.93 and
2.01%, respectively. While, on chemlali
variety, the highest average percentage of
parasitism was recorded during May,
June, July, August December, February,
and March with an average of 7.84, 4.80,
8.60, 4.74, 8.60, 5.28 and 6.53 %,
respectively. Statistical analysis of the
data indicates that, no significant
differences among the averages of the
annual percentages of the parasitism
within the three varieties (4.86 %, 4.22 %
and 3.89 % on chemlali, picual and
coratina varieties, respectively) during
2018-2019 season (Fig. 3 D). These
results showed that, the population of the
parasitoids,
Aphytis sp.
was
approximately synchronized with the pest
population. The lowest percentage of
parasitism was recorded on the pest
might be owing to the lowest population
numbers of the pest and the weather
factors. It is known that, most
Aphytis
species are facultative gregarious. The
degree of gregariousness depends on host
size but there are some differences
between species (Luck et al., 1982). In
Egypt,
Abd-Rabou (1997) and Abou-
Elhagag (2004)
studied the role of
Aphytis sp.
in regulating the olive scale
insects. Statistical analysis of the data in
Table (1) indicates that, the correlation
between the monthly average parasitism
by
Aphytis
spp. and the weather factors
(max. and min. temperatures) were
highly significant positive on picual
variety (r= 0.550 and 0.561), whereas,
the relative humidity showed highly
significant negative correlation (r = -
0.349
).
On coratina variety, the
correlation was highly significant and
negative between the max. and min.
temperature (r=-0.595 and -0.617) and
highly significant positive correlation
with RH (%) (r=0.334). On chemlali
variety, the correlations between the
monthly average parasitism by
Aphytis
spp and both maximum and minimum
temperatures (r=0.299 and 0.168) were
insignificantly positive and negative with
RH (%) (-0.231).
Table 1: Correlation coefficient between the parasitoid, Aphytis spp. populations and maximum and
minimum temperatures, and relative humidity on certain olive varieties during 2018-2019 seasons.
Varieties
Correlation coefficient values “r”
Maximum Temperature (°C)
Minimum Temperature (°C)
RH (%)
Picual
0.550**
0.561**
-0.349**
Coratina
-0.595**
-0.617**
0.334**
Chemlali
0.299ns
0.168ns
-0.231ns
ns: non-signifiant p >0.05, *p< 0.05, **p<0.01.
Temperature and humidity have strong
effect on
Aphytis
survival. Extreme
temperatures are considered the main
factor of mortality for
Aphytis
in the field
(Rosen & DeBach, 1978). In a laboratory
experiment, Kfir and Luck (1984) found
that the combination of high
temperatures with low humidity
50
negatively affected
Aphytis
adult
survival.
3.2.2. Weather factors
Data in Table (2) showed the simple
correlations between the population of
the oystershell scale insect,
L. ulmi
and
the maximum, minimum temperature,
relative humidity and the monthly
average parasitism by
Aphytis
spp. on
certain olive varieties (picual, coratina
and chemlali) during 2017-2018 and
2018-2019 seasons. During 2017-2018
season, statistical analysis of the data
indicates that the correlation between the
oystershell scale insect,
L. ulmi
population and the maximum (r= -0.488)
and minimum temperatures (r= -0.578)
were highly significant negative
correlation and insignificantly negative
with RH (%) (r= -0.074) on picual
variety. Whereas, on coratina variety the
maximum (r = -0.273) and minimum (r =
-0.393) temperatures, and the relative
humidity (r=-109) showed insignificant
negative correlations. Also, statistical
analysis on chemlali variety showed that
the maximum (r = -0.408) and minimum
(r = -0.506) temperatures showed highly
significant negative correlation, whereas
the relative humidity (r=-0.157) showed
insignificant negative correlation. During
2018-2019 season, the effect of
maximum (r = 0.907) and minimum (r =
0.804) temperatures were highly
significant positive correlation with the
oystershell scale insect,
L. ulmi
population, whereas, the relative
humidity showed highly significant
negative correlation (r = -0.737) on
picual variety. On coratina variety, the
correlation was highly significant
positive correlation between max.
(r=0.574) and min. temperatures (r=
0.587), and highly significant negative
correlation with RH (%) (r= -0.443) and
the population pest. Whereas on variety
chemlali, the max. and min. temperatures
showed highly significant positive
correlation (r= 0.891 and
0.931),meanwhile, the relative humidity
showed highly significant negative
correlation (r = -0.523) with oystershell
scale insect,
L. ulmi
population. The
correlation between the pest and the
parasitoid,
Aphytis
spp. was highly
significant positive on picual (r=0.466),
coratina (r=0.412) and chemlali
(r=0.725) varieties.
Table 2: Correlation coefficient between the parasitoid, Aphytis spp., weather factors (maximum, minimum temperatures,
and relative humidity) and the population of the oystershell scale insect, L. ulmi on certain olive varieties (picual, coratina
and chemlali) during 2017-2018 and 2018-2019 seasons.
Seasons
Correlation coefficient values “r”
Aphytis spp. (%)
Maximum Temperature (°C)
Minimum Temperature (°C)
2017-2018
-
-0.488 **
-0.578 **
-
-0.273ns
-0.393ns
-
-0.408**
-0.506**
2018-2019
0.466**
0.907**
0.804**
0.412**
0.574**
0.587**
0.725**
0.891**
0.931**
ns: non-signifiant p >0.05, *p< 0.05, **p<0.01.
It is clear that the climate and the natural
enemies affects both spatial and temporal
distribution, as well as reproduction and
dissemination of plant pests since
temperature, relative humidity, light and
water are major factors influencing their
51
population, growth and development
(Landa, 2019). Consequently, climate
change is expected to affect the incidence
and severity of pest attacks in olive.
However, it is difficult to predict such
consequences, as they are the results of
complex interactions between the specific
pest, the olive genotype, and the specific
environment (climate, agronomic
practices, etc.). Thus, the life cycle
(survival, reproduction, dispersal,
infection) of a given pest, and their
specific relations with the host can be
affected in very different ways, and
cannot be generalized (Landa, 2019). In
conclusions, the obtained results
indicated that,
L. ulmi
is the most
common scale insects attacks the olive
varieties (Picual, Coratina and Chemlali)
during both seasons. The highest average
of
L. ulmi
population was recorded on
picual variety, while the lowest average
was recorded on coratina variety. Also,
the results stated that picual variety was
more infested by
L. ulmi
than other
varieties. In addition, survey of
L. ulmi
parasitoids resulted in two species of
parasitoids,
A. chrysomphali
and
A.
disppidis
in the Faculty of Agriculture
Experimental Farm, Assiut University,
Egypt. Moreover, the results indicated
that the weather factors affect the
population of
L. ulmi
and its parasitoids.
These results might be helpful in an IPM
program to control the oystershell scale
insect,
L. ulmi
and to settle the best time
for pesticide application on olive
varieties.
Acknowledgements
The authors wish to thank the Plant
Protection Department, Faculty of
Agriculture, Assiut University, Egypt, for
providing a partial funding support for
this study. Also, sincere thanks are
extended to anonymous reviewers who
gave constructive criticisms to the earlier
version of this manuscript.
References
Abd-Rabou S, 1997. Parasitoids attacking the
olive scale insect, Paralatoria oleae
(Colvee) (Homoptera: Coccidea:
Diaspididae) in Egypt, The first
Scientific Conference of Agricultural
Sciences. Faculty of Agriculture, Assiut
University, Assuit, Egypt, pp. 719726.
Abou-Elhagag GH, 2004. Abundance of
olive scale insect, Parlatoria oleae
Clovee (Homoptera: Diaspididae) and its
parasitoids in upper Egypt. Assiut
Journal of Agricultural Science 35: 197
208.
Alford DV, 2014. True bugs. Pests of Fruit
Crops: A Colour Handbook, Second
Edition. CRC Press, 32123.
Argyriou LC, Kourmadas AL, 1981.
Contribution to the timing for the control
of Diaspididae scales of olive trees.
Annales de l'Institut Phytopathologique
Benaki 13: 6572.
Boulancer LW, 1965. Integrated and
Chemical Control of the Oystershell
Scale in Maine. Journal of economic
entomology 58: 672674.
Carrillo LR, Cifuentes CC, Mundaca BN,
1995. Life cycle of Lepidosaphes ulmi
(L.) (Hemiptera: Diaspididae). Revista
Chilena de Entomologia 22: 5-8.
Cavalloro R, 1984. Integrated Pest Control in
Olive Groves: Proceeding of the
CEC/FAO/IOBAC International Joint
Meeting, Pisa, 36 April.
52
Dminic I, Milek TM, Bazok R, 2010.
Problems of scale insects (Hemiptera:
Coccoidea) in olive groves of Istrian
county. Glasilo Biljne Zastite 10: 282
291.
Erol T, Yaşar B, 1999. Investigations on
natural enemies, some biological
characteristics and population
fluctuations of Lepidosaphes ulmi (L.)
(Homoptera, Diaspididae) and
Palaeolecanium bituberculatum (Targ.
and Tozz.) (Homoptera, Coccidae)
harmful to apple trees in Van province.
Turkish Journal of Agriculture and
Forestry 23: 151164.
Ferris GF, 1937. Atlas of the scale insects of
North America. USA: Stanford
University Press, California, USA.
Gill RJ, 1997. The scale insects of California.
Part 3: the armored scales (Homoptera:
Coccoidea: Diaspididae). California,
USA: California Department of Food
and Agriculture Technical Series in
Agricultural Biosystematics and Plant
Pathology.
Helsen HHM, Blommers LHM, Trapman
MC, Timing observation and control of
mussel scale Lepidosaphes ulmi. In:
International Conference on Integrated
Fruit Production 422, 1996.
International Society for Horticultural
Science (ISHS), 145149.
Karren JB, Roe AH, Davis R, 2019.
Oystershell (Mussel) Scale
(Lepidosaphes ulmi). Utah State
University Extension and Utah Plant Pest
Diagnostic Laboratory, pp. 1359.
Katsoyannos P, Stathas GJ, 1995. Phenology,
embryonic diapause and importance of
natural enemies of Lepidosaphes ulmi
(L.) (Homoptera: Diaspididae) on olive
trees in Greece. Israel Journal of
Entomology 29: 199206.
Kfir R, Luck RF, 1984. Effects of
temperature and relative humidity on
developmental rate and adult life span of
three Aphytis species (Hym.,
Aphelinidae) parasitising California red
scale. Journal of Applied Entomology
97: 314320.
Landa BB, 2019. EIP-AGRI Focus Group,
Pests and diseases of the olive tree.
Funded by European Commission, pp.
120.
Luck RF, Podoler H, Kfir R, 1982. Host
selection and egg allocation behaviour
by Aphytis melinus and A. lingnanensis:
comparison of two facultatively
gregarious parasitoids. Ecological
Entomology 7: 397408.
Mansour R, Mkaouar R, Lebdi KG, Suma P,
Russo A, 2011. A survey of scale insects
(Hemiptera: Coccoidea) occurring on
olives in Tunisia. Journal of
Entomological and Acarological
Research 43: 315322.
Milek TM, Simala M, 2012. Scale insects
(Hemiptera: Coccoidea) on olive tree
(Olea europaea L.). Glasilo Biljne
Zastite 12: 285297.
Milek TM, Simala M, Bjelis M, Pintar M,
Markotic V, 2017. Updated check list of
scale insects (Hemiptera: Coccoidea) on
olive trees in Croatia with special regard
on Black araucaria scale - Lindingaspis
rossi (Maskell 1891). IOBC/WPRS
Bulletin 121: 9197.
Ozgokce M, Yasar B, Karaka I, 2016. Life
tables of Lepidosaphes ulmi (L.) and
Palaeolecanium bituberculatum
(Targioni Tozzetti)(Hemiptera:
Coccoidea) on apple trees in Van
province, Turkey. Entomologica 33:
53
317322.
Rosen D, DeBach P, 1978. Diaspididae. In:
Clausen CP, ed. Introduced parasites
predators of arthropod pests weeds.: a
world review. Washington, D.C.: US
Department of Agriculture, Handbook,
pp. 78128.
Stathas GJ, Bouras SL, Elipoulos P,
Emmanouel NG, 2005. Control of
diaspidid scales on olive trees by
releasing coccinellid predators.
IOBC/WPRS Bulletin 28: 157166.