Observation of Arthropod Populations during Outbreak of Olive - Iresa

Observation of Arthropod Populations during Outbreak of
Olive Psyllid Euphyllura olivina in Tunisian Olive Groves
Naceur Gharbi, Institut de l’Olivier, Rue Hédi Karray, 2080 Ariana, Université de
Sfax, Tunisia, Ali Dibo, and Mohieddine Ksantini, Institut de l’Olivier, P.O. Box.
1087, 3000 Sfax, Université de Sfax, Tunisia
__________________________________________________________________________
ABSTRACT
Gharbi, N., Dibo, A., and Ksantini, M. 2012. Observation of arthropod populations during
outbreak of olive psyllid Euphyllura olivina in Tunisian olive groves. Tunisian Journal of Plant
Protection 7: 27-34.
This study aims to investigate the Arthropod communities in pullulating period of Euphyllura olivina
(Homoptera: Psyllidae) which is recognized as a serious problem pest of olive trees in Tunisia. The
field trials were achieved in two successive years, i.e. 2009 and 2010, in two organic olive orchards
situated in the regions of Taous and Chaal (Sfax, Southern East of Tunisia). The assessment of
abundance of different groups of Arthropods showed that phytophagous and natural enemies were
much more abundant in 2010 than in 2009 in Taous and Chaal groves. More than 94% of all herbivores
were E. olivina. The most abundant natural enemies on olive trees was the indigenous bug Anthocoris
nemoralis (Heteroptera: Anthocoridae) with an average population frequency of 49% of the total
natural enemies found, followed by Psyllaephagus euphyllurae (Hymenoptera: Encyrtidae) (26%),
lacewings (20%), Syrphid predators (3%), and other generalist predators (2%).
Keywords: Biodiversity, Euphyllura olivina, natural enemies, olive tree
__________________________________________________________________________
Olive culture is considered to be of
great ecological, economic, dietary and
social importance in Mediterranean
countries. In Tunisia, olive plantations
counts about 66 million trees and cover
about one third of the arable land area
(cultivated area 1.7 million ha).
The olive grove is an
agroecosystem that supports a wide range
of diverse and functionally important
groups of Arthropods (13, 17, 18). The
canopy arthropod community has
Corresponding author: Naceur Gharbi
Email: gharbi.naceur@yahoo.fr
Accepted for publication 28 June 2012
a complex structure that includes
functional groups with phytophagous,
predator, parasitoid and detritivore
species (17, 18, 20).
The olive psyllid Euphyllura
olivina (Homoptera: Psyllidae) is a
serious pest in Tunisia. High psyllid
populations can affect the vegetative
development, the fertility and the
reproduction of the olive tree (1, 9, 10,
12). During the beginning of early spring
season, olive trees produce new shoots
that continue to elongate throughout most
of the spring. Outbreaks of olive psyllid
populations may be associated with new
shoot production, weather conditions (4)
and with insecticide use which destroys
the psyllid natural enemies (5, 12).
Tunisian Journal of Plant Protection 27 Vol. 7, No. 1, 2012

The olive psyllid is commonly
consumed by several species of generalist
predators (Anthocoridae, Chrysopidae,
Aranae, Coccinellidae, and Miridae) and
many parasitoids (Psyllaephagus
euphyllurae, Alloxista sp., Elasmus sp…).
These natural enemies successfully
control psyllid in some cases (4).
At present, intensive pesticide use
is being held responsible for irreversible
damage to biodiversity, and numerous
alternatives are being investigated in
order to control crop pests (7, 16).
The aim of this study was the
monitoring of the group of Arthropods in
olive groves in the pullulating period of
E. olivina.
MATERIALS AND METHODS
Orchards. The study areas were
located in two olive groves near Sfax
(Southern East of Tunisia): Taous and
Chaal groves with different agricultural
systems. The predominant cultivar is
Chemlali. Both olive groves have been
conducted according to organic growing
guidelines. All olive trees were well
tended, but no pesticide sprays were
applied against pests or diseases, and soil
was ploughed superficially with a
scarifier two to four times a year to
control weeds.
In Taous grove, the planting
density is of 7 m × 7 m, the olive trees are
about 10 years old and the field was
irrigated. Chaal grove was planted in
extensive (pluvial) mode with trees about
70 years old spaced 24 m × 24 m apart.
The two biotopes are characterized by a
typical continental climate, cold winters
(5.8°C in January) and very hot summers
(32.2°C in August).
Observations. The survey of the
fluctuation of psyllid population and
beneficial insects was monitored weekly
by sampling from the beginning of
February till the end of May over a period
of 2009 and 2010. Two sampling
techniques were applied in the current
study: beating sheet and branch sampling.
Beating sheet. Ten trees at about
the same stage of growth were randomly
selected in each biotope and five branches
per tree were sampled. All captured
individuals were identified under
binocular at the order, family or species
level and the total number of each taxon
was recorded.
Branch sampling. Five trees per
site were randomly sampled, five twigs
(10-15 cm in length) were cut per tree,
covered in plastic bags and taken to the
laboratory where they were examined
under binocular and the current stages of
psyllids (eggs and juveniles) and
parasitoids or predators were counted.
Psyllid stages observed in sample
were expressed in linear density (4, 5)
that represents the total number of psyllid
stages on length of examined twigs
(number of stages/m).
For the assessment of the
fecundity of E. olivina, females were
sampled weekly and examined in the
laboratory for the presence of mature
eggs, after opening their abdomen.
Data analysis. Data were analyzed
with ANOVA using LSD test (SPSS
version 17). If necessary data were
transformed using the Log-transformation
for normal distribution and homogeneity
of variances.
RESULTS
Beating sheet results. The
assessments of abundance of the different
groups of arthropods in the regions of
Taous and Chaal from February till end of
May over two years, a total of 60117
insects were captured, among which
51493 were herbivores and 8684 were
natural enemies. Phytophagous and
Tunisian Journal of Plant Protection 28 Vol. 7, No. 1, 2012

natural enemies were much more
abundant in 2010 than in 2009 survey in
Taous and Chaal groves. More than 94%
of all herbivores were E. olivina (a total
of 48490 individuals; sex ratio:
male/female = 0.88/1). High population
densities of psyllid occurred between the
beginning of March till the end of May
with two peaks; the first peak in the
middle of March and the second one at
the end of April. Other herbivores were
olive moth, Prays oleae (Lepidoptera:
Yponomeutidae) (4%) and Liothrips
oleae (Thysanoptera: Phlaeothripidae) (<
2%).
The most abundant natural
enemies on olive trees was Anthocoris
nemoralis (Heteroptera: Anthocoridae)
with an average population frequency of
49%, of the total of natural enemies
found, followed by Psyllaephagus
euphyllurae (Hymenoptera: Encyrtidae)
(26%), green and brown lacewings
(Neuroptera: Chrysopidae) (20%),
Syrphid predators (Diptera: Syrphidae)
(3%) and other generalist predators (2%).
Mean numbers of E. olivina were
significantly different between Taous and
Chaal groves (Table 1). In contrast, there
were significant location effects on the
mean numbers of A. nemoralis and P.
euphyllurae from February till end of
May samplings in both years (2009 and
2010). In all cases, Taous grove had
higher densities of these insects than
Chaal grove. The effect of location by
year interaction on the linear densities of
E. olivina was not significant (F3, 19 =
1.097, P = 0.31). However, the locationyear
interactions have no effects on the
abundance of P. euphyllurae and A.
nemoralis. Both P. euphyllurae and A.
nemoralis were more abundant in Taous
than Chaal grove in each of collection
periods.
Mean numbers of Chrysopid and
Syrphid predators were not significantly
different between Taous and Chaal
groves. However, during both years, the
mean numbers of Chrysopid and Syrphid
predators were higher in Taous than in
Chaal.
In two orchards, every year, some
predator species such as Chrysoperla
carnea (Neuroptera: Chrysopidae) were
present at low number before the growth
of phytophagous populations. Overall,
predator populations started to increase in
numbers from March to mid May,
especially for A. nemoralis. Furthermore,
P. euphyllurae was observed especially in
the period between mid April and mid
May, and it was not frequently observed
at the last period of observations
(beginning of May), because the psyllid
nymphs were absent in this period (Fig.
1).
Branch sampling results. The
total number of collected E. olivina
nymphs was 84623 and a total of 119309
psyllid eggs were sampled. The structure
of psyllid population was composed by
68% young instars (L1, L2 and L3) and
32% old instars (L4 and L5). The total
number of immature mortality was 1287,
with 65% of them consumed by natural
enemies.
Significantly, there were more
eggs and immatures of E. olivina in
Taous than Chaal during the sampling
period. Also, mean proportion of intact
immature was statistically similar in
Taous than Chaal from March to mid
May (Table 2). However, Taous had
higher proportion of immatures
parasitized than Chaal. Likewise, mean
proportion of immatures consumed was
higher in Taous than Chaal during the
sampling period.
Tunisian Journal of Plant Protection 29 Vol. 7, No. 1, 2012

Table 1. Phytophagous and predaceous insects occurring on olive trees colonized by Euphyllura olivina in
Taous and Chaal groves during two years 2009 and 2010 (Sampling period: February - May)
Insect species Mean number (± SE) of insects a Statistical values
Sampling year Taous Chaal F P
2009
Phytophagous
Euphyllura olivina
Prays oleae
Liothrips oleae
Predaceous
Anthocoris nemoralis
Psyllaephagus euphyllurae
Chrysopid predators
Syrphid predators
2010
Phytophagous
Euphyllura olivina
Prays oleae
Liothrips oleae
Predaceous
Anthocoris nemoralis
Psyllaephagus euphyllurae
Chrysopid predators
Syrphid predators
134.27 ± 42.09 a
3.71 ± 0.41 a
1.50 ± 0.61 a
5.56 ± 1.86 a
3.06 ± 0.85 a
2.44 ± 0.69
0.30 ± 0.18
171.21 ± 65.29 a
2.62 ± 0.84
2.06 ± 0.43 a
7.93 ± 1.02 a
3.93 ± 0.87 a
2.64 ± 0.66
0.38 ± 0.04
83.26 ± 24.67 b
1.82 ± 0.35 b
0.94 ± 0.11 b
3.05 ± 1.12 b
1.78 ± 0.55 b
2.06 ± 0.47
0.23 ± 0.08
92.29 ± 31.30 b
2.28 ± 0.63
0.72 ± 0.07 b
4.18 ± 0.82 b
2.18 ± 0.54 b
2.53 ± 0.59
0.37 ± 0.02
F1,31 = 5.91
F1,31 = 8.67
F1,31 = 4.25
F1,31 = 12.253
F1,31 = 6.321
F1,31 = 3.662
F1,31 = 2.698
F1,31 = 23.051
F1,31 = 0.543
F1,31 = 21.066
F1,31 = 24.514
F1,31 = 6.124
F1,31 = 9.546
F1,31 = 0.776
0.0410
0.0331
0.0110
0.0421
0.0341
0.0708
0.0927
0.0013
0.8761
0.0012
0.0134
0.0112
0.0638
0.3847
a Data show mean number (± SE) of insects per tree. Means followed by the same letter within a line are not
significantly different according to LSD test at P < 0.05.
Table 2. Mean number of immature stage of Euphyllura olivina on olive trees in Taous and Chaal groves during
two years 2009-2010 (Sampling period: February-May)
Sampling year
Mean linear density (± SE)
of E. olivina
Mean proportions (± SE) of Nymphs a
Grove site
2009
Eggs Nymphs Intact Parasitized Consumed
Taous 93.997 ± 28.951 a 52.875 ± 11.517 a 0.810 ± 0.052 a 0.054 ± 0.016 a 0.136 ± 0.038 a
Chaal 59.752 ± 22.814 b 28.806 ± 11.506 b 0.935 ± 0.014 b 0.021 ± 0.006 b 0.043 ± 0.011 b
F1,31 3.923
17.013
26.032
17.470
26.728
P 0.036
0.003
0.00927
0.00308
0.00085
2010
Taous 146.961 ± 34.184 a 67.373 ± 18.419 a 0.616 ± 0.102 a 0.078 ± 0.014 a 0.306 ± 0.089 a
Chaal 76.984 ± 31.526 b 32.579 ± 17.291 b 0.856 ± 0.024 b 0.049 ± 0.013 b 0.095 ± 0.018 b
F1,31 29.358
26.401
25.875
11.691
26.363
P 0.00923
0.00817
0.00945
0.00909
0.00089
a
Means followed by the same letter within a line are not significantly different according to LSD test at P < 0.05.
Tunisian Journal of Plant Protection 30 Vol. 7, No. 1, 2012

Fig. 1. Linear densities of the different stages of Euphyllura olivina in Taous and Chaal groves during 2009
and 2010 (Sampling period: February-May).
Tunisian Journal of Plant Protection 31
Vol. 7, No. 1, 2012

DISCUSSION
In this study, the representative
orders in olive orchard were Homoptera,
Lepidoptera, Neuroptera, Thysanoptera
and Coleoptera varying in proportion
between groves and years. These groups
have been reported in the literature as
typically the abundant groups in olive
groves (3, 11, 19). These orders include
key-groups of predators, parasitoids and
phytophagous. Natural enemies play an
important role in the biological control of
olive pests like P. oleae and E. olivina (8,
13, 14, 15).
In Tunisia, the list of natural
enemies of E. olivina is composed by 14
species (11) that were recorded with
different frequencies that varied
according to species belonging to four
families: Anthocoridae, Chrysopidae,
Coccinellidae and Encyrtidae. The first
three families include many predator
species: A. nemoralis, C. carnea and
Coccinella septempunctata (Coleoptera:
Coccinellidae), and the fourth includes
the endoparasitoid P. euphyllurae (4, 11).
The role of herbivore induced volatiles in
the searching behavior of predators like
A. nemoralis and C. carnea under field
conditions was studied (6).
During both years of study, total
abundance of arthropods was higher in
Taous than in Chaal olive grove.
However, this higher abundance is a
result of the high number of Homoptera,
which is due to the presence of the olive
pest E. olivina. Our observations show
clearly that E. olivina is a serious pest of
olive crop. Early attacks, especially in the
spring, cause considerable damage to
flowers and subsequent losses in both
quality and quantity of olive fruits (5).
Throughout the growing season, mid-
February to the end of May, only E.
olivina was constantly present. High
population densities occurred at mid
March to the end of May with two peaks:
the first peak at the mid-March and the
second peak in the second half of April
(Fig. 1).
The largest percentages of mature
females of E. olivina were recorded
during the period between early February
and late April. Generally, the peak of egg
laying occurred in the second week of
March (around 75 to 95% of total females
respectively in 2009 and 2010) and
remained high until mid-April (more than
50% of total females), explaining the
significant increase in its population size
during the spring months (Fig. 1).
In this evaluation, the most
abundant predator found on olive in Sfax
area was A. nemoralis with an average
population frequency varying between 33
and 41% of the total natural enemies
found. Anthocorids are not abundant on
olive early in spring. Its population starts
to increase in numbers by mid-March,
peaking at the end of April, coinciding
with that of E. olivina, and representing
the major part of the predator populations
found on olive tree during the spring.
This indicates the positive relationship
occurring between E. olivina and A.
nemoralis in olive orchards. This
predator, A. nemoralis, can be reared
easily and cheaply and is readily
available. There are many reports
describing the role of this predator in the
biological control of E. olivina
populations (2). However, little is known
on their role in olive orchard and this
needs to be clarified.
The two years of this survey have
provided useful and promising data as a
basis for further research in the effective
sustainable management of P.
euphyllurae, A. nemoralis and C. carnea
populations, which constitute the most
important group of natural enemies of
insect pests recorded in olive orchards.
Tunisian Journal of Plant Protection 32 Vol. 7, No. 1, 2012

__________________________________________________________________________
RESUME
Gharbi N., Dibo A. et Ksantini M. 2012. Observation des populations d’arthropodes durant la
période de pullulation du psylle de l’olivier dans les oliveraies tunisiennes. Tunisian Journal of
Plant Protection 7: 27-34.
Ce travail vise l’étude de la communauté des arthropodes durant la période de pullulation d'Euphyllura
olivina (Homoptera: Psyllidae), un ravageur majeur des oliviers en Tunisie. Le suivi s’est étendu sur
deux années successives 2009 et 2010, dans deux oliveraies biologiques localisées dans les régions de
Taous et Chaal (Sfax, Sud-Est de la Tunisie). L’évaluation de l’abondance des différents groupes
d’arthropodes montrent que les phytophages et les auxiliaires étaient plus abondants en 2010 qu’en
2009 dans les oliveraies Taous et Chaal. Plus que 94% de la totalité des phytophages collectés est
composée d’E. olivina. L’ennemi naturel le plus rencontré est la punaise prédatrice Anthocoris
nemoralis (Heteroptera: Anthocoridae) avec une population moyenne de 49% de la totalité des
auxiliaires collectés, suivi de Psyllaephagus euphyllurae (Hymenoptera: Encyrtidae) (26%), des
chrysopes (20%), des syrphes (3%) et d’autres prédateurs généralistes (2%).
Mots clés: Biodiversité, ennemis naturels, Euphyllura olivina, olivier
__________________________________________________________________________
���ﻣ
ﻼ��ﺑ ﻲ��ﺗ ة��ﻓ لﻼﺧ �ﺟرﻷا تﺎ����ﻣ تﺎﻋ����ﻟ
�ﺻر . 2002 . ﻲ�����ﻗ �ﻳ�ﻟا ﻲ�ﻣو ��ﻳد ﻲ�ﻋو �ﺻﺎﻧ ،ﻲﺑ�ﻐﻟا
. ���ﻧ��ﻟا ن��ﻳ�ﻟا ��ﺗﺎ�ﺑ ﻲﻓ Euphyllura olivina ن��ﻳ�ﻟا
Tunisian Journal of Plant Protection 7: 27-34.
Euphyllura olivina ن��ﻳ�ﻟا ﻼ��ﺑ �ﺛﺎ��ﻟ ���ﻼ�ﻟا ة���ﻟا لﻼﺧ �ﺟرﻷا تﺎ����ﻣ ع��ﺗ �ﺳارد ﻰﻟإ ��ﻌﻟا ا�ه ف�ﻬﻳ
��ﻣﺎﻋ لﻼﺧ �ﺳار�ﻟا ه�ه �ﻳ�ﺟأ . �ﻧ�ﺗ ﻲﻓ ن��ﻳ�ﻟا
رﺎ�ﺷﻷ �ﻳ�ﺟ ����ﻣ ّ�ﻌﺗ ﻲ�ﻟاو ،(Homoptera:
Psyllidae)
ﻲﻗ��ﻟا ب���ﻟا ،�ﻗﺎ�ﺻ)
لﺎﻌ�ﻟاو سووﺎ�ﻟا ْﻲ�����ﺑ �ﻳ�ﻀﻋ/
��ﺟ�ﻟ��ﺑ ن��ﻳز ��ﺗﺎ�ﺑ ﻲﻓ ،2010
و 2009 ���ﻟﺎ��ﻣ
لﻼﺧ �ﻓوأ �ﻧﺎآ ��ﻌ���ﻟا ءا�ﻋﻷاو ��ﺗﺎ��ﻟا تﺎﻓﻵا نأ �ﺟرﻷا تﺎ����ﻣ
�ﻣ �����ﻣ
تﺎﻋﺎ�ﺟ ة�ﻓو �ﻳ��ﺗ
�ﻬ�أ . ( ﻲ�ﻧ��ﻟا
�ﻣ % 94 �ﻣ ��آأ ﺎهد���ﺑ ن��ﻳ�ﻟا ﻼ��ﺑ ���ﻣ
�ﻗو . لﺎﻌ�ﻟاو
سووﺎ�ﻟا ْﻲﻧﺎ��ﺑ ﻲﻓ ،2009
��ﺳ ﻲﻓ ��ﻣ 2010 ��ﺳ
Anthocoris nemoralis (Heteroptera: ﻲﻌ���ﻟا و�ﻌﻟا نﺎآو . ﺎﻬﻌ�ﺟ �ﺗ ﻲ�ﻟا ��ﺷﺎﻌﻟا تﺎﻓﻵا دا�ﻋأ ع���ﻣ
����ﻟا هﻼﺗ ،ﺎﻬﻌ�ﺟ
�ﺗ ﻲ�ﻟا ��ﻌ���ﻟا ءا�ﻋﻷا ع���ﻣ �ﻣ % 49 ـﺑ ر��ﻳ ل�ﻌ�ﺑ ًارﺎ��ﻧا ��آﻷا Anthocoridae)
��ﻓ��ﻟا بﺎﺑ�ﻓ
(% 20)
��ﻟا �ﺳأ �ﺛ (% 26)
Psyllaephagus euphyllurae (Hymenoptera: Encyrtidae)
.(% 2)
�����ﻟا ��ﻏ تﺎﺳ����ﻟا �ﻌﺑ ���ﻌ� ����ﺑو ا��ﺧأو (% 3)
Euphyllura olivina ،ن��ﻳ�ﻟا ة��ﺷ ،ﻲﺟ�ﻟ���ﻟا ع���ﻟا ، ��ﻌ���ﻟا ءا�ﻋﻷا : ��ﺣﺎ��ﻣ تﺎ��آ
__________________________________________________________________________
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Tunisian Journal of Plant Protection 34 Vol. 7, No. 1, 2012