Advances in

n Environmental Biology, 10(10) October 2016, Pages: 20-28

AENSI Journals

Advances
ces in Environmental Biology
ISSN-1995-0756

EISSN-1998-1066

Journal home page: http://www.aensiweb.com/AEB/

Importance of embryonic antagonists in regulating

populations
of
processionary
Thaumetopoeapityocampa (Denis & Schiffermuller,
1775) Schiff in some Algerian cedar forests.
1Mounir

Kherroubi, 1Fazia Mouhouche,

Mouhouche 2Chakali Gahdab

Laboratory of Phytopharmacology,, Zoology agricultural and forest department, High School of Agronomy, Hassan Badi, El Harrach,
Algiers, Algeria
2
Laboratory of Entomology, Zoology agricultural and forest department, High School of Agronomy, Hassan Badi, El Harrach, Algiers,
Algeria
Address For Correspondence:
Mounir Kherroubi, Laboratory of Phytopharmacology, Zoology agricultural and forest department, High School of Agronomy,
Hassan Badi, El Harrach, Algiers, Algeria
E-mail: kherroubi.m@hotmail.fr
This work is licensed under the Creative Commons Attribution International License (CC BY).
http://creativecommons.org/licenses/by/4.0/

Received 28 August 2016; Accepted 18 October 2016; Available online 22 October 2016

ABSTRACT
The purpose of this study is to propose alternative solutions based on the use of antagonists biologic, in order to fight against
aga
the
pinprocessionary, Taumetopoeapityocampa (Denis and Schiffermller). That is considered as a defoliator because of the damage to the
silvicultural and health problems in the Algerian forests or wooded areas open to the public. To meet this objective, we have we conducted
outings for harvesting the
he eggs mass of pine processionary. This operation was performed in a random manner in pure cedar forests of three
station : Chrea,, Theniet El Had and Chelia. The prepared biological material is monitored daily in the laboratory to monitor the emergence
of antagonists over time. A diversity of four parasitoids in control populations of the pine processionary moth was
identified:Baryscapusservadeii,
Baryscapusservadeii, Ooencyrtuspityocampae and Trichogrammaembryophagum encountered in three cedar forests (Chrea,
(
Chelia and Theniet El-Had).
Had). The fourth species is typical of Anastatusbifasciatus pundits cedar forest Theniet El had. From all the Eggs
mass analyzed, the frequency rate of occurrence of the species Baryscapusservadeii stood at 29.31% for the station Chrea, 4.54% and 25%
for Chelia and Theniet El Had respectively. For Ooencyrtuspityocampae,, it is about 10.34% for the punters harvested site Chrea, 2.27% for
laying harvested Chelia and 6.25% for biological material Theniet El-had.
El
The attendance rate of Trichogrammaembryophagum
Trichogrammaembryoph
remains
very low, with only 3.44% in Chrea and 6.25% in Chelia. This species remains absent in the site Theniet El had. The different rates of
parasitism of a site to another depending on the species and in relation to the form of egg mass, cylindrical
cylindrical or plat. in conclusion, , the
Baryscapus servadeii remains more active than the rest of the parasitoids identified. Based on these results, it is desirable to provide this
parasitoid farms, that showed performance on several cases in biological control.

KEYWORDS: Cedar, Egg mass, Moth processionary, parasitoids.

INTRODUCTION
Mediterranean forests cover a geographical area of about 81 million hectares (FAO, 2010). Algerian forest
occupies 4.7 million hectares distributed in the northern part of the country (DGF, 2007).
2007) it is consists of a
mixture of tree species, mainly the Aleppo pine, maritime pine, stone pine, cork oak, holm oak and Atlas cedar.
These biotic communities are currently threatened by various species of defoliators and borers(Imbaultet
borers
al.,
2013; Rossi et al., 2016).
). The most spectacular defoliation caused by the processionary of softwood and
hardwood(Rousseletetal., 2015). Adults in this group of social insectshave a very limited lifetime. The larvae,

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Advances in Environmental Biology, 10(10) October 2016, Pages: 20-28

known for their gregarious lifestyle,their greed (Fraval, 2007) and their stinging properties pose many health
problems even for humans and animals. With the known climate change, the infestations of this defoliator take a
wider dimension recorded in her range and accentuated by the decline of her natural enemies (Van Dyck, 2012;
Roques et al., 2015).Extending the range of host species plays a very important role in the movements of the
insect (Battistiet al., 2015). The temperature remains the determining factor in its distribution and the health of
forest stands. Currently, infestations of this insect affect insouthern Europe and northern Africa (FAO, 2010).
The population of the pine processionary moth can be controlled by the intervention of various auxiliaries
including embryonic parasitoids that play an important role in limiting populations of culmination phase. These
parasitoids, belonging to the order Hymenoptera and are mainly part of the family Chalcididae using the eggs
processionary as a host for their development (Morel, 2008). This parasitism mechanism is important in
biological control to reduce the ecological niche of the processionary in cold areas of the European continent
and altitude ecosystems of Mediterranean areas (Demolin, 1987). Several studies on the importance and use of
these eggs parasitoids for biological control, have been led by; Suty (2010), kherroubi (2012),
Jactel(2014),Battisti (2015), Guyot(2015).
The choice of subject was conducted following the importance of growthprocessionarypopulations and the
practice of the use of the eggs parasitoids proves of a great interest for the regulation of
theprocessionarypopulationsin zones sub-wet and semi-arid of Algeria.
MATERIALS AND METHODS
2.1. Harvest and preparation of the eggs mass:
During the summer of 2014, we conducted outings for harvesting the eggs mass of pine processionary. This
operation was performed in a random manner in pure cedar forests in the early dates of adult flights. The eggs
mass of varying lots were taken from selected sites. A staff of 78 eggs mass was harvested in the resorts of
Chrea (3626'4.15"N, 253'20.29"E) and Chelia (3518'8.48"N, 637'4.17"E). The third lot represented by 56
eggs mass were harvested in Cedar of Theniet ElHad (3551'19.64"N, 20'7.33"E). The biological material was
gathered by the accessibility and height of man. The eggs mass collected are stored individually in tubes of
10cm in length and 1 cm in diameter plugged with cotton for ensure the ventilation. Each tube is fitted with a
label bearing the number of the Ponte.
2.2. Control of biological material in the laboratory:
The prepared biological material is monitored daily in the laboratory to monitor the emergence over time.
hatching caterpillars and Parasitoidsare noted in control cards. Meanwhile, daily temperatures are recorded
using a thermometer to record the variability of outbreaks related with temperatures.
2.3. Enumeration of emergences:
With the emergence, theparasitoids are identified with Professors Chakali G.and Doumandji S. All
parasitoids are counted to derive information on theparasitism rate on each species in the surveyed stations.
2.4. Methods of data analysis:
Frequency distribution and the analysis of variance. The statistical analysis of the parasitism rates was
conducted on Excel Stat 9.
RESULT AND DISCUSSION
3.1. Parasitic diversity of eggs of the processionary:
Four parasite Hymenopteraoophages belonging to Chalcidoidae have emerged from the biological material
controlled; the identificationwas made by Professor ChakaliGahdab and confirmed by Professor
DoumandjiSalaheddine. The species, Ooencyrtuspityocampae, Baryscapusservadeiiand Trichogrammaem
bryophagum have been noted in the three stations explored. The fourth species isAnastatusbifasciatuswas
obtained only from two eggs mass fromthe Cedar Forest ofTheniet El-Had.
3.2. Analyses Frequency of the parasitoidspresence:
It is important to emphasize that an egg laying maybe parasitized, by one, two or three species
simultaneously. All combinations are noted in our experimentation.
Case of the Cedar Forest of Chrea:
On 70 Eggs mass placed under observation, 12 have not been parasitized, either a calculated rate of 83% of
the eggs mass have given at least a parasite.Similarly, Kherroubi (2012) showed a parasitism rate of 58% in the

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region Chrea, at this subject, Arkam (2011) notes the importance of parasitoids on eggs mass of processionary
vary a biotope to another and from a year to another. It is important to emphasize that the percentage represents
the eggs mass who have suffered a parasitism. In the biological material examined, it existed of eggs mass that
are heavilyattacked, other moderately attacked and the last category is represented by eggs mass weakly
attacked. The combinations of the presence of the three parasitoids are noted on the biological material consider
born with a dominance of the species,Baryscapusservadeii, representing a rate 29,31% of the global workforce.
The frequency of the presence of B.servadeiiand T. embryophagumamountsto 20.68%. Other combinations of
presence is limited between 3.44 and 10.34% however only variant O. pityocampae with T.embryophagumhas
not been noted.Schmidt et al. (1997) at his study about the parasitodes of processionary had noted a
parasitismrate of 21,4% byBaryscapusservadeiiandOoencyrtuspityocampae.The extremities of the eggs mass
are the most sought by the parasitoids identified. On the basis of these results, it is important to emphasize that
the parasitoids, O.pityocampa and T.embryophagum seem to recognize to not to return in specific competition.
These antagonists appear to recognize the parasitized.
Case of the Cedar Forest of Chelia:
On a batch of 50 eggs mass, sixeggs mass only do not contain parasitodes. Unlike the previous site of
Chrea, we note a low rate 4.54% of parasitism by Baryscapusservadeii. The presence of the three parasitoids
sets represented the highest percentage, either 40, 90% of the total workforce. The Combination of
Baryscapusservadeii with Trichogrammaembryophagum occupies a frequency of 15.90% and the combination
of B.servadeii and O.pityocampaeoccupies 13.63%. The presence of T.embryophagum with 6.81% allows to
draw a first idea on the performance and the ability to parasitize the eggs mass in this site despite the protection
of eggs mass per the scales. This ability opens up prospects for research for its use on a large scale. It should be
noted that theT. embryophagum is the most common species with frequency of the presence of 6.81 % in the
Cedar Forest of Chelia. The species B. servadeii occupies the second rank. The third species O. pityocampae
is limited to 2.27%.
Case of the Cedar Forest of ThenietEl-Had:
On a batch of 37 eggs mass placed under observation, five have not given of emergence of parasitodes. The
rate of parasitism is 86.48% of the presence of a parasite at least in the biological material taken into
consideration. Among the antagonists the more frequent that have emerged is Baryscapusservadeii occupies a
percentage of 25%. As noted earlier the combination of the three parasitoids simultaneously occupies the greater
frequency, is 31.25%. As the region of Chrea the absence of combination between the two Oophages, O.
Pityocampae and T. embryophagum is remarkable. However the presence of T. embyophagum with
Baryscapusservadeii is noted. The frequency of the presence of T. embryophagum alone is zero. Contrary to
the region of Chelia, the species remains the most representative. The presence of three parasitoid sets still the
highest percentage 31.25%. It is important to point out the presence of a fourth species. Anastatusbifasciatus a
workforce of 4 individuals has emerged only of two eggs mass harvested from this site.
3.3. Chronology ofemergences of active species according to the regions:
3.3.1. Emergence of Baryscapusservadeii:
Case of the Cedar Forest of Chrea:
The cumulative curve of emergences of this embryonic parasitoid on a population of 58 eggs mass is
represented by the figure 1. according to biological material from the Cedar Forest of Chrea, the first Emerging
Baryscapusservadeii have been noted in the first week of the month of July 2014. The emergences were
staggered on 36 days. The date of timing, corresponding to 50 % of the emergence of the population is carried
out at 12 July 2014.
Case of the Cedar Forest of Chelia:
The cumulative curve of emergences of this embryonic parasitoid on a number of 78 eggs mass is
illustrated by Figure 2. According to the graph above, we note that the species Baryscapusservadeii emerged
with a low number with respect to the station of Chrea. The emergencesare carried out in the second week of
the month of July 2014 and are spaced out during 14 days. There comparing with the data collected on the
previous population of Chrea. It is apparent that the emergences are more late and more limited in the time to
Chelia. The date of the shimming (50% of the emergence) was registered on 15 July 2014.
Case of the Cedar Forest of Theniet El-had:
The cumulative curve of emergences of this embryonic parasitoid on a number of 56 eggs mass is
represented by the figure 3. The first emerging Baryscapusservadeii in the region of Theniet El-Had have been
noted from the third week of the month of August 2014 with a very low number. It is from the 3 October that the
population is manifested significantly. It is possible that a few individuals are released before the late harvest of

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our biological material. Despite this delay a large number of individuals have emerged and are lagging behind in
their emergence which ran up to the end of the month of 'October. The date of timing, corresponding to 50%
of the emergence of the population is carried out on 12 October 2014. A variability between the dates of
emergences of populations of servadeiiBaryscapus is noted and likely in relationship with thecharacteristics of
the environment particularly the geographic position.
3.3.2. Emergence ofOoencyrtuspityocampae:
Case of the Cedar Forest of Chrea:
Figure 4 illustrates the cumulative curve of emergences of Ooencyrtuspityocampae.As well as the
speciesBaryscapusservadeii. The first emergence of theOoencyrtuspityocampaewas noted from the first week of
the month of July 2014. The first individuals to have emerged on 05 July in contrast to the previous generation
of 2013, for the same region the emergence as were held later to 22 July and are staggered over a period of 25
days. The year 2014 the emergences were staggered on 23 days. About ten days after the observation of the
biological material, 70% of the population have emerged. The date of timing is 13 July 2014.
Case of the Cedar Forest of Chelia:
The cumulative curve of emergences embryonic parasitoid The Ooencyrtuspityocampae establishes from a
workforce of 78 eggs mass is represented by the figure 5. In the site of Chelia the species of
Ooencyrtuspityocampae. Began their emergence from the second week of the month of July with a more
important in relation to the site before. The date of shimming done at 17 July 2014. The timing of emergences
was carried out with 12 days.
Case of the Cedar Forest of Theniet El-Had:
The cumulative curve of collected data is illustrated in Figure 6. The biological material harvested from the
Cedar Forest of Theniet El-Had has highlighted the greatest strength of the parasitoidOoencyrtuspityocampae.
The first outputs of the adults were recorded late in relation of the previous population. This have only from the
fourth week of the month of August 2014 that the first individuals to have emerged. The emergences were
spread out over two months. The date of timing, corresponding to 50% of the emergence of the population is
carried out on 17 October2014.
3.4. Comparative analysis of the rate of parasitism in the three regions according to the species:
To perform a comparison between the rates of parasitism of each species in the different regions according
to the form of eggs mass (cylindrical or in plate). It has counted the number of parasitized eggs according to the
holes in output of each species.
Case of Baryscapusservadeii:
The results obtained are illustrated by the histogram of the figure 7. According to the histogram below, we
note that the rates of parasitism of eggs mass by the Baryscapusservadeii in the two sites Chrea and El-Had
Theniet is very similar for the two forms of eggs mass (cylindrical and plate). The bioclimatic floor and the
altitude of the sites may have an effect on the evolution of these parasitoids. The reduced number of cylindrical
Eggs mass harvested at Chelia does not give reliable results. A study on a greater number of samples gives
more information on the evolution of this parasitoid.
Case of the Ooencyrtuspityocampae:
The results obtained are presented by the histogram of the figure 8. The parasitoidOoencyrtus embryonic
pityocampaeremains more meaning on the cylindrical Eggs mass to Chelia. Has Chrea rates of parasitism
relating to two forms of eggs mass, remain comparable. Has Theniet El-Had a slight difference is noted in favor
of eggs mass in plate.
Case of Trichogrammaembryophagum:
The results obtained are illustrated by the histogram of the figure 9. The Eggs mass harvested in the
three cedars explored have shown that the species Trichogrammaembryophagumchosen more of the eggs mass
in the form of likely plate the species to more preference on these hosts that are better exposed. The Eggs mass
parasitized by T.embyophagum are limited to draw significant information.
3.5. Overall analysis of the rates of parasitism in relationship with the shape of the eggs mass:
The results obtained are illustrated by the histogram of the figure 10. In a general way the parasitoids are
evolving preferentially to ends on the eggs mass in plates. The eggs mass in plates are better exposed and allow
a facility to species to parasitize a maximum of eggs with a movement limited.

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Effective of emergences

1200
1000
800
600
400
200
0
29-Jun 04-Jul

09-Jul

14-Jul

19-Jul

24-Jul

29-Jul 03-Aug 08-Aug 13-Aug

Dates (days)
Fig. 1: Cumulative curve of emergences of Baryscapusservadeii
100

Effective of emergences

90
80
70
60
50
40
30
20
10
0
11-Jul

13-Jul

15-Jul

17-Jul

19-Jul

21-Jul

23-Jul

25-Jul

27-Jul

17-Oct

27-Oct

06-Nov

Dates (days)
Fig. 2: Cumulative curve of emergences ofBaryscapusservadeii
400

Effective of emergences

350
300
250
200
150
100
50
0
18-Aug

28-Aug

07-Sep

17-Sep

27-Sep

07-Oct

Dates (days)
Fig. 3: Cumulative curve of the emergences of Baryscapusservadeii

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70

Effective of emergences

60
50
40
30
20
10
0
29-Jun 04-Jul

09-Jul

14-Jul

19-Jul

24-Jul

29-Jul 03-Aug 08-Aug 13-Aug

Dates (days)
Fig. 4: Cumulative curve of the emergences of the Ooencyrtuspityocampae.
180

Effective of emergences

160
140
120
100
80
60
40
20
0
12-Jul

14-Jul

16-Jul

18-Jul

20-Jul

22-Jul

Dates (days)
Fig. 5: Cumulative curve of emergences of the Ooencyrtuspityocampae

Efective of emergences

600
500
400
300
200
100
0

Dates (days)
Fig. 6: Cumulative curve of the emergencesof the Ooencyrtuspityocampae

24-Jul

26-Jul

28-Jul

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Rates of parasitisme

12
10
8
6
4
2
0
Chrea Plate
Chrea
clutche
Cylindrical
clutches

Chelia Plate
Chelia
clutche
Cylindrical
clutches

Theniet ElHad Plate

clutche

Theniet ElHad
Cylindrical
clutches

Fig. 7: Rates of parasitism by Baryscapusservadeii in the three stations in relationship with the type of Eggs
mass (cylindrical and plate)
4

Rates of parasitisme

3.5
3
2.5
2
1.5
1
0.5
0
Chrea
Plate
clutche

Chrea
Cylindrical
clutches

Chelia
Plate
clutche

Chelia Theniet El- Theniet ElCylindrical Had Plate

Had
clutches
clutche Cylindrical
clutches

Rates of parasitisme

Fig. 8: Rates of parasitism by Ooencyrtuspityocampaein the three stations in relationship with the type of Eggs
mass (cylindrical and plate)
5
4.5
4
3.5
3
2.5
2
1.5
1
0.5
0
Chrea
Plate
clutche

Chrea
Cylindrical
clutches

Chelia
Plate
clutche

Chelia Theniet El- Theniet ElCylindrical Had Plate

Had
clutches
clutche Cylindrical
clutches

Fig. 9: Rates of parasitism by Trichogrammaembryophagum in the three stations in relationship with the type of
Eggs mass (cylindrical and plate)

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20

Rates of parasitisme

18
16
14
12
10
8
6
4
2
0
Chrea
Plate
clutche

Chrea
Cylindrical
clutches

Chelia
Plate
clutche

Chelia Theniet El- Theniet ElCylindrical Had Plate

Had
clutches
clutche Cylindrical
clutches

Fig. 10: Rates of parasitism overall in the three stations in relationship with the type of Eggs mass (cylindrical
and plate)
Conclusion:
A entomological diversity of four embryonic parasitoids has been identified; Baryscapusservadeii,
Ooencyrtuspityocampae and Trichogrammaembryophagumencountered in the three stations studied and
Anastatusbifasciatus, typical to the eggs mass of the Cedar Forest of Theniet El-had. On the whole of eggs mass
analysed the frequency rate of the presence of the species Baryscapusservadeiiamounts to 29, 31% for the
station of Chrea, 4.54% for Chelia and 25% for Theniet El-Had. For the Ooencyrtuspityocampae,itsa order of
10.34% for the eggs mass harvested from site of Chrea, 2.27% for the eggs mass harvested from Chelia and
6.25% for the biological material of the Theniet El-had. The rate of presence of Trichogrammaem br
yophagumremains very low with only 3.44%, either two eggs mass on a workforce of 70 eggs
masscollected from the region of Chrea Atlas cedar and 6.25% in the site of Chelia. This species remains absent
in the site of Theniet El-had. It is desirable to seek more the species on a larger number of samples. The
possibility of simultaneously have one, two or three parasitoids is very frequent on lots of eggs mass harvested
in the three sites with rates very variable depending on the species and the Middle prospected.As the sites
surveyed are not localized in the same floor bioclimatic nor has the same altitude, the rates of different
parasitism from a site to the other depending on the species and in relationship with the form of Ponte
(cylindrical or in plate). The eggs mass have a form in plate are relatively more favorable for all parasitoid
species particularly for the Trichogrammaembryophagum.in conclusion, the Baryscapus servadeii remains more
active than the rest of the parasitoids identified. Based on these results, it is desirable to provide this parasitoid
farms, that showed performance on several cases in biological control.The use of parasitoids in forests requires a
choice of species among the more effective and better adapted. This requires a thorough understanding of the
diversity of indigenous auxiliaries. Among the parasitoids, the polyphagous, Trichogrammaembryophagum is
a species to retain and develop in the framework of fight against possibly several species of insect Lepidoptera.
Its low presence on the eggs mass of the processionary, is explained by the barrier on the protective scales. A
research investigation must be conducted to draw information on its power to parasitize eggs mass protected.
ACKNOWLEDGEMENTS
This study was funded by the Ministry of high education and scientific research, Ecole Nationale
Superieure Agronomique, PhD program, Algeria. Thanks go to Professor DoumandjiSalaheddine, Department
of Zoology agricultural and forest, ENSA Algiers, Algeria for his assistance.
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