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DIVERSITY OF APHIDS AND THEIR NATURAL ENEMIES IN THE CITRUS

(CITRUS SINENSIS) ORCHARD OF LAKHDARIA, BOUIRA-ALGERIA

Article  in  Munis Entomology and Zoology Journal · January 2022

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DIVERSITY OF APHIDS AND THEIR NATURAL ENEMIES IN

THE CITRUS (CITRUS SINENSIS) ORCHARD OF LAKHDARIA,
BOUIRA- ALGERIA

Kamila Gacem*, Farid Mezerdi* and Nia Billal**

* Laboratory Promotion of Innovation in Agriculture in Arid Regions, Department of
Agronomic Science, University of Biskra, ALGERIA. E-mails: kamila.gacem@univ-
biskra.dz, gacem.kamila.pv@gmail.com, f.mezerdi@univ-biskra.dz, mezerdif@yahoo.fr,
ORCID IDs: 0000-0002-0800-110X and 0000-0002-4388-2520
** Scientific and technical research in arid regions (CRSTRA), Biskra, ALGERIA. E-mail:
nia.billal@crstra.dz, bilalniadz@gmail.com, ORCID ID: 0000-0003-0047-9261

[Gacem, K., Mezerdi, F. & Billal, N. 2022. Diversity of aphids and their natural
enemies in the citrus (Citrus sinensis) orchard of Lakhdaria, Bouira- Algeria. Munis
Entomology & Zoology, 17 (1): 573-582]

ABSTRACT: The diversity of the aphid fauna and their natural enemies present on the
experimental orchard of Lakhdaria at Bouira. Weekly monitoring of the population
dynamics of aphids was carried out between March and May 2019. The results obtained first
made it possible to highlight a qualitative richness of 4 species of aphids subservient to
citrus in this region (Aphis spiraecola, Aphis gossypii, Myzus persicae, and Toxoptera
aurantii), the species A. spiraecola is the most dominant. Three predators counted:
Coccinella algerica, Harmonia axyridis, and Episyrphus balteatus. Aphidius colemani and
the only parasitoid species harvested in this study.

KEY WORDS: Population dynamics, aphid, natural enemies, citrus, Lakhdaria

Citrus occupies an essential social and economic role in Algeria, where citrus
trees cover an area of 416 hectares or 21.55% of the total arboricultural In the area
of Bouira, the citrus production arrived at 43710,50 Qx; in contrast, Lakhdaria
occupied 258 ha, their show came at 25695 Qx in 2018 (D.S.A., 2019).
Citrus has been utilized in more medicinal preparations than most other
plants and finds its use to remedy scores of ailments ranging from a toothache,
diarrhea, constipation, insomnia, and vomiting(Lebbal & Laamari, 2015).
The importance of the aphid as a pest is related to several factors; it attacks
the orchards in the spring. It is a polyphagous species that evolve on different
fruit species during the development of buds and young shoots, such as citrus,
apricot, peach, and pomegranate (Helyer, Cattlin, & Brown, 2014).
Latter was fundamental data in interpreting the mechanisms of variation of
abundance and temporal distribution of the pest and their natural enemies in its
natural habitat to understand the impact of the host plant factor, temperature,
and hygrometry on the development of aphids. Thus, this knowledge was a way to
consider effective control strategies at the right time, improve yields and protect
tree productions, especially before the maturity of the fruits, to make them
suitable for consumption and acceptable for marketing (Rand & Louda, 2006).
The purpose of this study was to elaborate on the biodiversity and distribution
of aphids fauna on citrus and the effect of their natural enemies combined with
climatic factors on the population dynamics of these species. Such information
was essential in discovering new and potentially valuable biological control agents
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and choosing appropriate species and biotypes for the integrated pest
management program (Dedryver, Le Ralec, & Fabre, 2010).

MATERIALS AND METHODS

Experimental orchard
This study was carried out in Lakhdaria, whose geographical coordinates were
36°33’35’’ North latitude and 3°36’17’’ East longitude. Altitude: 131 m.
The experiment was conducted from March to May 2019 in a citrus orchard.
This study aimed to identify the species of aphids and their natural enemies
present in the citrus orchard and observe the efficiency of capturing different
sampling methods—the samples were taken by visual analysis, yellow traps.
The flight phase in aphids plays a significant role in the dispersion of species,
in the search for host plants, and the transmission of viral diseases.
To control all these phenomena was necessary to proceed to a sampling of the
aerial environment by capturing the winged aphids which move freely (Rabasse,
1976).
The citrus orchard was selected, on average 0.5 ha, and there were 80 trees,
with an average age of approximately eight years. We collected Data concerning
the aphid's natural enemies from citrus trees with yellow traps. And identified
species.

Collect leaves by hand

We chose five trees at random. Verify the presence of insects; regular samples
consisted of 50 leaves of citrus were randomly collected in a transparent bag and
transferred to the laboratory for counting aphid species and their natural
enemies. Samples are taken weekly. The insects were collected using forceps,
brushes, and test tubes and then packed in plastic containers previously
identified.

Yellow traps
We placed ten circular yellow plastic traps between the leaves and branches of
the trees at an average height of 1 m above the soil to cover the entire orchard for
our study, the traps containing 0.50 liters of water and 2 mL of neutral detergent
to break the surface tension.
We renewed and replaced the soapy water in the traps every week after each
collected species were removed with a fine brush and then put in micro-tubes
containing 70% alcohol. The date, location of collection, and host plant were
noted.
We obtained insects and transferred them to plastic containers for counted
and identification in the laboratory.

Equations
Total richness (S), centesimal frequency, and constancy were the ecological
indices of composition used.

The total richness (S)

The total number of species in the stand considered in a given ecosystem
(Ramade, 1994).
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Relative abundance or centesimal frequency (%)

The percentage of individuals of a species concerning the total number of
individuals (Dajoz, 1985).
It expressed the formula:
ni: Number of individuals of a species.
N: Total number of individuals.

Ecological indices of composition

Index study of species diversity, we calculated four descriptors to characterize
the diversity: indices of Shannon-Weiner H', Simpson’s. The Pielou’s and
Simpson’s indices were used to calculate the evenness of aphids (Shayesteh,
Ranji & Ziaee, 2015) and their natural enemies.

Shannon-Wiener indices H':

Pi: the proportion of ith species among all collected samples.
S: the total number of species in the community.

Simpson’s diversity indices: according to (Shayesteh et al., 2015), It

expressed the formula:

1-D: Simpson’s index.

ni: number of individuals of particular species.
N: total number of individuals in all collected species.
The probability that any two randomly selected species from the sample will
be different (0= low diversity, 1= high diversity)

Pielou’s evenness:
S: the total richness of species in the community
H’: Shanon’s diversity index (Shayesteh et al., 2015).

Simpson’s equitability (evenness):

RESULTS AND DISCUSSION

Identification of aphid population and their natural enemies

We identified four species of aphids belonging to the Aphididae family,
including (Aphis spiraecola, Aphis gossypii, Myzus persicae, and Toxoptera
aurantii. Also, four predators counted two species of coccinellids identified,
including Coccinella algerica, Harmonia axyridis, and species Episyrphus
balteatus (Diptera: Syrphidae). And the only parasitoid species Aphidius
colemani harvested in this study (Figs. 01, 02, 03).
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Figure 01. Aphis spiraecola green citrus aphid, winged and apterous.

Figure 02. Ventral and dorsal face of Coccinella algerica.

Figure 03. Ventral and dorsal face of Episyrphus balteatus.

Aphid population
Relative abundance (%)
The experimental study of aphids' population dynamics was conducted
between March and May 2019 in Lakhdaria in citrus trees. It recorded four
aphidian species, which were by order of predominance.
Figure 04 shows the number and the frequency of occurrence of aphid species
in 2019. Aphis spiraecola was the most abundant aphid species in the citrus
orchard (Fig. 04).

Figure 04. Relative abundance (%) of aphid species found in the citrus orchard.
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Aphis spiraecola observed during the study period was the most dominant,
with 94,78% individuals, followed by Aphis gossypii with 2,19%, Myzus persicae
with 2,04%, and Toxoptera aurantii with 0,99% individuals in capacity.
Myzus persicae is considered an occasional pest of fruit trees, specifically
peach (Ben Halima & Ben Hamouda, 2005). Its presence in citrus with 2,04% was
related to the existence of peach orchard. The other species were considered
accidental species, which explains their weak presence on citrus.
We note that the species richness of the plant cover in the citrus orchards
offers a diversity of host plants, which justifies the large number of aphid species
inventoried. The total absence of phytosanitary products can also explain the high
abundance of aphids; the massive use of pesticides has a significant negative
effect on several levels (Fig. 05).

Figure 05. Evolution of the fluctuations of the different aphid species installed on the citrus
orchard.

The trapping of aphids allowed us to capture 2010 individuals, the results

obtained us first to highlight a qualitative richness of 4 species of aphids infested
with citrus in this region, Aphis spiraecola with 21 individuals on 14 March, and
their population reached 394 species on 25 April or two weeks later.
On 28 March 2019, the installation of Myzus persicae. A similar trend in the
rest of the species expressed biotic factors such as high temperature, and
continuous rainfall can also reduce aphid populations.
The appearance of Aphis gossypii and Toxoptera aurantii in the orchard with
low numbers during April and May.
We observed a rapid increase in the number of individuals of Aphis spiraecola
until it reached 394 individuals on 25 April. The numbers progressively decreased
until they almost disappeared from citrus trees at the end of May.

Ecological indices of aphid species in the citrus orchard

The highest Shanon's (H') diversity index of aphids was obtained on 25
April (0,399), followed by 02 May (0,347) with equitability indices of 0,288
and 0,250, respectively.
The highest Simpson's index is 0,170. It was also calculated on 25 April
(Table 01).
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Table 01. Diversity indices of aphid’s community at different time intervals in the citrus
orchard of Lakhdaria.

H: Shanon’s Index, E.H.: Shannon's equitability, 1-D: Simpson’s index, E.D.: Simpson’s
equitability.

Natural enemies of aphids

Coccinella algerica was more abundant compared to the other species. In
parallel to the monitoring of aphid populations in the citrus orchard, we were
interested in the natural enemies of aphids and, more particularly.
The predators were polyphagous insects, which feed on nectar or pollen, in
addition to aphids. Among the most used in biological control were the families
of Coccinellidae.
Two species represent the family Coccinellidae: Coccinela algerica and
Harmonia axyridis; the family Syrphidae is represented by a single species
Episyrphus balteatus.
The results indicate that ladybugs dominate in a citrus orchard. The species
Coccinela algerica comes first. The ladybug Harmonia axyridis was found in
the citrus orchard but with low numbers.
We revealed only one primary parasitoid species, Aphidius colemani
belonging to the order Hymenoptera, family Braconidae in citrus orchards.

Relative abundance (%)

The Coccinellidae represent the vast majority, Coccinella algerica
dominates on citrus with 65,31%, and then Harmonia axyridis represents
4,08%. Then comes the Syrphidae family represented by the species
Episyrphus balteatus but at low abundance 3,06%, the parasitoid Aphidius
colemani was found in citrus orchards with 27,55% (Fig. 06).
The activity of natural enemies on citrus started at the beginning of April
when we captured four species of Coccinela algerica, one species of Harmonia
axyridis, and one individual of Episyrphus balteatus. The maximum activity of
natural enemies recorded on 18 April with the capture of 31 individuals of
Coccinela algerica and two Harmonia axyridis.
The results of fluctuations of different predators identified in citrus orchards
are shown in the (Fig. 07).
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Figure 06. Relative abundance (%) of the natural enemies of aphids found in the citrus
orchard.

Figure 07. Fluctuations of different natural enemies of aphid species in the citrus orchard.

Natural enemies were living organisms that were useful to agriculture

because of their regulatory actions on pests. The traps installed in the citrus
orchard allowed the systematic collection of a large number of predators
insects. Indeed, three species of the predators were found from 04 April to 23
May 2019.
The presence of natural enemies is linked to climatic conditions, the
availability of food (aphids), and the species richness of the flora.
(Benoufella-Kitous, 2005), report the presence of these aphid predators in
the region of Tizi Ouzou. The presence of C. algerica species was also reported
by (Guettala, 2009) during his study on apple aphids in the Batna region.
In this study, we found natural enemies represent the group frequently
observed. Show that ladybugs are recognized as excellent predators of aphids
during all stages of their life. Ladybugs were the essential entomophagous
group in regulating aphid populations by reporting the same species
(Saharaoui, Benzara & Doumandji-Mitiche, 2001). These results agreed with
the results of (Coutin, 2007) who notes that ladybugs constitute an
entomophagous group likely to play an essential role in reducing aphid
populations. Next comes the appearance of E. balteatus.
Parasitoids need a host for their development; Hymenoptera includes most
of the parasitoids of aphids.
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This species was reported for the first time in Algeria by (Laamari,
Jousselin, & d'Acier, 2009). They have also been written in the natural and
cultivated environments of eastern Algeria.
In our study, the presence of parasitoids was significant in reducing aphid
populations due to the influence of different factors such as the availability of
food and favorable climatic conditions (temperature and air humidity).
(Langer, Boivin, & Hance, 2004) demonstrated that moderate temperatures
associated with humidity levels between 25 % and 90 % favored the activity of
parasitoid Hymenoptera.

Ecological indices of the natural enemies of aphids species in the

citrus orchard
Diversity indices of natural enemies of aphids were higher in May than
April 2019. Simpson’s diversity index on 23 May and 04 April were 1,0 and
0,75, respectively, indicating that the possibility of selecting two different
species of predators was 100% on 23 May and 75% on 04 April (Table 02).

Table 02. Diversity indices of aphid's natural enemies at different time intervals in the
citrus orchard of Lakhdaria during 2019.

Our findings indicated that there was a large population of C. algerica in

the orchard. It seemed the presence of high ladybird species because
pesticides did not spray the orchards. However, the results showed that
ladybird populations were decreased significantly at the end of the sampling
period in May 2019. The population coincided with the migration of
coccinellids to other shelters, especially for summer aestivation. We stated
that coccinellids were more abundant when surrounding landscapes had more
native shrublands and semi-urban areas than those with more annual crops.
Therefore, the orchard composition and heterogeneity affect the design of
coccinellids and the efficacy of these biological control agents.
The abundance, species richness, and diversity increased with increasing
plant diversity and landscape complexity. In our study, the small, simple
structure of the landscapes examined was expected to decrease the richness of
the aphids and their natural enemies. Diversity indices depend not only on
species richness but also on the evenness, or equitability, with which
individuals are distributed among the different species. Simpson's index's
maximum and minimum value for the coccinellids community was 1,0 on 23
May and 0,287 on 18 April 2019. The Simpson's index of aphids in 2019 was
0,101. Suggests that the possibility of selecting two different species of aphids
randomly in the checked orchard in 2019 was 10%. For coccinellids,
Simpson's index was 0,5 for 2019. The low species diversity index (Simpson)
could be due to the uniform distribution of individuals among species.
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CONCLUSION

The main objective of our study was to highlight the population dynamics of
aphids and their natural enemies in the experimental orchard of Lakhdaria.
The results of this work have made it possible to establish the first inventory of
aphids and their natural enemies infested with fruit trees in the region of
Lakhdaria. A total of four species of aphids infested with citrus in this region
Aphis spiraecola (Patch), Aphis gossypii, (Glover), Myzus persicae (Sulzer), and
Toxoptera aurantii (Boyer de Fonscolombe), A. spiraecola was the most
dominant species. The aphid populations increased when the temperature was
optimal in the orchards and the rainfall was low.
Four species of natural enemies are found in the citrus orchard. Tree species
of predators, two ladybugs, represented by the species: Coccinella algerica
(Kovar) and Harmonia axyridis (Pallas), the hoverfly Episyrphus balteatus (De
Geer) (Diptera: Syrphidae), and the first parasitoid found of Aphidius colemani
(Viereck) (Hymenoptera: Braconidae).
Considering the climatic characteristics, the agro-systems practiced in the
region of Lakhdaria, and the biodiversity of its natural environments, it was sure
that other extended surveys in space and time would enrich this list.
In this region, several factors (climatic, biotic, etc.) can favor and intensify the
contamination of these insects.
Our study in the region has shown that control of this species remains
challenging, given the considerable cost of control methods. If the use of ladybugs
can limit the influence of these crop pests, their use has ecological consequences.
The alternative solution, effective and less costly (economically and ecologically),
was the preventive fight through the intervention of agricultural practices (type of
irrigation, fertilization, etc.).
The absence or ineffectiveness of extension for this type of pest in this region
and the lack of information among farmers may leave the field open for rapid and
formidable development of these insects.
In light of the results obtained, it was desirable in the future to propose a
study.
In-depth and detailed on predators and parasitoids that will be an alternative
to chemical control, which is often practiced in the region of Lakhdaria, especially
in fruit farming, still in this directive, the selection of varieties of fruit trees
resistant to aphid attacks was welcome. We did all this experiment only through
scientific research and applications in the field.
In the future, it would be necessary to confirm experimentally the effect of
natural enemies on the growth of aphids to limit phytosanitary problems. It is
recommended to organize days of sensitization and popularisation for the
farmers. On the other hand, it was necessary to extend this survey to other
communes to establish a distribution map of this insect.
A study on the infestation of other fruit trees by the various pests was also
necessary to have more information on the sensitivity and resistance of these
crops in the region of Lakhdaria.

ACKNOWLEDGEMENTS

The authors would like to thank Mr. Chaibi Rachid for his help and provision
of the experimental orchards conducted by the field study.
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