Content uploaded by Riadh Moulaï
Author content
All content in this area was uploaded by Riadh Moulaï on Mar 01, 2020
Content may be subject to copyright.
Content uploaded by Riadh Moulaï
Author content
All content in this area was uploaded by Riadh Moulaï on Feb 29, 2020
Content may be subject to copyright.
Zoology and Ecology, 2019, Volume 29, Number 2
Print ISSN: 2165-8005
Online ISSN: 2165-8013
DIVERSITY AND ECOLOGY OF DIURNAL LEPIDOPTERA IN
BELEZMA NATIONAL PARK (AURÈS, ALGERIA)
Sonia Berkanea*, Abdelhak Rahmanib, Bachir Arib and Riadh Moulaïa
Laboratoire de zoologie appliquée et d’écophysiologie animale, Faculté des sciences de la nature et de la vie,
Université de Bejaia-06000 Bejaia, Algérie B. P.: 359 Amizour, Bejaia, Algeria
*Corresponding author. Email: soniaberkane2000@hotmail.com
Abstract. To establish a list of existing diurnal Lepidoptera in the Belezma National Park (Aurès,
Algeria) and produce a rst report on the health of its forest environments using these species as
bio-indicators, 192 surveys were carried out between March 2010 and February 2011. This sampling
comprised four stations among different habitats; three forests (cedar, oak, pine) and a wasteland.
This allowed us to identify 896 individuals, representing 30 species: 29 Rhopalocera (Nymphali-
dae, Pieridae, Lycaenidae and Hesperiidae) and only 1 species of diurnal Heterocera belonging to
the family Arctiidae. The wasteland proved to be the richest station with 18 species and also the
most diversied and balanced station (H′ = 3.49 bits; E = 0.84). It is followed by cedar forest (17
species; H′ = 3.16 bits; E = 0.77) and oak forest (12 species; H′ = 2.58 bits; E = 0.72). Finally, the
pine forest (9 species; H′ = 2.56 bits; E = 0.81) was the least diversied station. Correspondence
Analysis of the most characteristic butteries at each station revealed that despite continual efforts
of park services to safeguard forest formations, especially cedar forests, butteries still suffer from
population depletion.
INTRODUCTION
Butteries are among the most popular and familiar of
insects encountered (Chinery and Cuisin 1994). Because
of their specic link with their host plants and habitats,
they are recognized as excellent bio-indicators of the
health status of natural environments (Tarrier and De-
lacre 2008; Faure 2007; Manil et al. 2007).
A recent systematic and ecological catalogue of butter-
ies has been established for Algeria (Tennent 1996).
It was followed by an inventory on butteries living in
the most interesting habitats in the north-eastern region,
particularly wetlands (Samraoui 1998). More recently,
work on the diversity and abundance of buttery species
has been carried out in agricultural plots in the north-
central part of the country (Remini and Moulaï 2015).
However, there is a need to enrich these inventories by
expanding the prospecting areas to other regions of the
country in order to cover as much territory as possible
in the long. Butteries can be considered to be a means
of monitoring the quality of protected area management
in Algeria. As such, they can be a good way to monitor
the efforts of reforestation in Algeria’s forests.
The Aurès region, and particularly the Belezma National
Park (BNP), is a remarkable and promising area to ex-
plore. The BNP represents a biogeographical region at the
crossroads of sub-humid and arid northern Mediterranean
inuences. It is also the site of the last remains of Cedrus
atlantica forests facing the great Sahara Desert. This
park acts as a biological reservoir for species dispersal
and migration, regulates natural balances and produces
economic and social resources (Sahli 2004).
The objective of this study was to compile the rst
inventory on diurnal Lepidoptera in this area and to
increase knowledge about their diversity and ecology.
Bio-indicator butteries can provide us with informa-
tion on the current state of general species richness in
forest environments. This study lasted 12 months, from
March 2010 to February 2011. It involved four stations,
one each in mixed cedar forest, oak forest, wasteland
and pine forest.
MATERIALS AND METHODS
Study sites
Geographical location
The Belezma National Park is in the eastern part of
northern Algeria (latitude 35° North and on either side
at longitude 6° East). It is in the mountainous massif
of Belezma, which is at the western end of the Aurès
Mountains, about 7 km northwest of the town of Batna.
It covers an area of 26,250 ha. It is a series of small
massifs trapped between the Hodna Mountains in the
west and the Aurès Mountains in the south-east, while
in the north-west and south-west it overlooks the Mer-
ouana plains and the Batna valley. Administratively,
this territory overlaps eight municipalities belonging
https://doi.org/10.35513/21658005.2019.2.11
Keywords:
Algeria; diurnal Lepidop-
tera; diversity; ecology;
Belezma National Park
Article history
Received: 15 April 2019;
accepted 10 October 2019
144 Berkane S., Rahmani A., Ari B., Moulaï R.
to the wilaya of Batna: Merouana, Seriana, Oued El
Ma, Hidoussa, Djerma, Fesdis, Oued Chaaba and Batna
(Sahli 2004). The BNP was classied as a Biosphere
Reserve by the MAB “Programme on Man and the Bio-
sphere” in 2015 (MAB-Algérie 2016) (Figure 1).
Climate and bioclimate
Bioclimatic analysis was carried out using meteoro-
logical data from the Ain Skhouna reference station
(35°44′20′′N 06°21′95′′E). It shows that the park area
belongs to the lower semi-arid bioclimatic level, char-
acterized by very severe climatic conditions, especially
during the summer season. This is due to the increase
in temperature values and drought caused by the wind
blowing from the south (Sirocco). This area is char-
acterized by a cool and rainy winter and a hot and dry
summer. The average annual temperature is 14 °C with
a maximum of 25.5 °C and a minimum of 5.1 °C. The
average annual rainfall is 300 mm (Arbouche et al. 2012;
Houamel 2012; Litim 2012).
Geographic distribution of the sites
The cedar forest (Figure 1 – Station A) (35° 34′ 39.62′′N
6°02′ 46.33′′E): The cedar forests in the park are essen-
tially made up of Cedrus atlantica. It is in Belezma that
the largest areas of cedar forest in the country are found
(1589.9 ha in 2014). Station A is part of cedar forest that
covers an area of about 300 ha. It is mainly located in
Jebels Tuggurt and Boumerzoug. The most dominant plant
species in this station are: C. atlantica, Juniperus oxyced-
rus, Quercus ilex, Fraxinus xanthoxyloides, Asphodelus
microcarpus and Calycotome spinosa. The oak forest
(Figure 1 – Station B) (35°34′43.16′′N 6°04′29.93′′E):
Belezma oak forests are matorrals with Quercus ilex as-
sociated either with J. oxycedrus, J. phoenicea or Olea
europaea. Station B is a matorral oak forest that covers
almost the entire mountainous area. The most dominant
plant species in this station are: Quercus ilex, J. oxyc-
edrus, C. spinosa, Stipa tenacissima and Ampelodesma
mauritanica. The wasteland (Figure 1 – Station C)
(35°37′21.03′′N 6°14′17.64′′E): The wastelands are in
different parts of the park. Station C consists mainly of
perennial herbaceous plants. The most dominant plant spe-
cies in this station are: Retama raetam, Sinapis arvensis,
Lavandula stoechas and Thymus vulgaris.
The pine forest (Figure 1 – Station D) (35°40′45.14′′N
6°15′45.96′′E): The pine forests of the park include
the Aleppo pine in its natural and wooded state. Sta-
tion D is the result of reforestation during the 1960s.
It is composed of young trees, is improving, and does
not show any major deterioration. The most dominant
plant species in this station are: Pinus halepensis,
J. phoenicea, Rosmarinus ofcinalis, C. spinosa and
L. stoechas (Smaihi and Kalla 2017; P. N. B. 2010 by
P. N. B. 2006; Sahli 2004).
Figure 1. Geographical location of the Belezma National Park and the study stations (Sahli 2004, modied).
145Diversity and ecology of diurnal Lepidoptera in Belezma National Park (Aurès, Algeria)
Methodology
The census of diurnal Lepidoptera at BNP stations was
carried out by regular counting of images from transect
surveys conducted between March 2010 and February
2011. This method was implemented by the English
with their “Buttery Monitoring Scheme” (Moore 1975;
Pollard and Yates 1993). The surveys were carried out
by 2 observers throughout the series. They observed the
images at the rear limit of a virtual box of 5 m on each
side, advancing for 1.5 km/1 h at least once a week.
Certain weather conditions were constraining: never
below 13°C, minimum sunshine period of 60% for tem-
perature between 13°C and 17°C, without any sunshine
constraint of sunshine above 17°C, and wind strength
having to be less than 40 km/h (Carriere 2013; Demerges
and Bachelard 2002; Ouin et al. 2000). All butteries
were identied and counted, either by direct observation
of the species where feasible or by capturing individu-
als, so that they could be released on site. Identication
guides were used when necessary: Guide des papillons
d’Europe et d’Afrique du Nord (Tolman and Lewington
1999), The Butteries of Morocco, Algeria and Tunisia
(Tennent 1996) and Guide des papillons nocturnes de
France (Robineau 2007). For the purposes of identica-
tion in the park, collection of a single voucher specimen
of each species was required.
Data analysis
The data collected were processed using the follow-
ing indicators: species richness (S), which is the total
number of all species encountered in the course of N ob-
servations; average richness (Sm), which is the average
number of species encountered during every counting
event: Sm = Ʃ Ni/R (Ni: number of species in survey
i, R: total number of surveys) (Ramade 1984); relative
abundance as a percentage of individuals of a given
species in relation to the total number of individuals,
which is expressed by the following formula: F (%) =
(ni/N)*100 (ni: number of individuals of a species I, N:
total individuals of all species combined); frequency of
occurrence: Fo (%) = P/R * 100 (P: number of records
containing the species studied); species are: ubiquitous
if Fo = 100%, constant if 75% ≤ Fo < 100%, regular if
50% ≤ Fo < 75%, accessory if 25% ≤ Fo < 50%, acci-
dental if 5% ≤ Fo < 25%, rare if Fo < 5% (Dajoz 1971;
Faurie et al. 2003); Shannon-Weaver Diversity Index:
H′ (bits) = -∑ qi log2 qi, where qi = ni/ N; Equitability
Index: E = H′/ H′max, where H′: observed diversity,
H′max: maximum diversity; H′max = log2S, where S
is species richness (Ramade 1984; Dajoz 1985; Pielou
1969); and nally, the Sörensen Index: Cs = (2J/a +
b)*100 (a: number of species present at site A, b: number
of species present at site B, and J: number of species
common to the two sites A and B (Maguran 1988).
To explore differences in buttery species diversity
in different stations, based on specic abundances, a
Correspondence Analysis (CA) was carried out using
the Past software, version 3.20 (Hammer et al. 2001).
For greater readability, only the abbreviations of the
species names appear.
RESULTS
During the study period, 30 species were recorded at
BNP level, including 29 Rhopalocera and 1 diurnal
Heterocera. Rhopalocera were represented by four
families: Nymphalidae, Pieridae, Lycaenidae and
Hesperiidae. There were 13, 9, 6 species from the rst
three families and only 1 species from the last one.
However, we only encountered one species of diurnal
Heterocera belonging to the family Arctiidae. 3 species
were recorded at all the stations studied: Colias croceus,
Glaucopsyche melanops and Pieris rapae. However,
17 species were found at only one of the stations:
Melitaea aetherie, Nymphalis polychloros, Pararge
aegeria, Polyommatus icarus, Pyrgus armoricanus and
Vanessa cardui in the cedar forest; Callophrys avis and
Melanargia occitanica in the oak forest; Coenonympha
pamphilus and Melanargia ines in the pine forest; and
Anthocharis belia, Chelis maculosa, Euchloe ausonia,
Euchloe belemia, Euchloe charlonia, Maniola jurtina
and Pontia daplidice in the wasteland. The number of
individuals recorded per station varied between 100 and
379. Argynnis pondora recorded the highest number at
cedar forest and oak forest, with 80 and 60 individu-
als, respectively. Colias croceus recorded its highest
numbers at the wasteland and pine forest, with 52 and
33 individuals, respectively. Among the species listed,
we noted the presence of 3 species protected by Alge-
rian law, namely: C. croceus, Polyommatus icarus and
Melanargia galathea (Table1).
Pieris rapae recorded its highest frequencies of occur-
rence (100%) as a ubiquitous species in the cedar and oak
forests. Pontia daplidice recorded its highest frequency
of occurrence in the pine forest as a ubiquitous species
with 100%. Then, Pieris rapae was constant at the level
of wasteland with 75%. On the other hand, it was absent
in the pine forest. C. croceus was constant at three sta-
tions (oak forest, wasteland and pine forest) with 75%
and regular with 50% in the cedar forest. G. melanops
and Pieris brassicae were regular in the wasteland as
Lycaena phlaeas in the oak forest, with 50% of frequency
of occurrence for each one of them (Figure 2).
Pontia daplidice recorded its highest relative abundance
in the pine forest with 48.75%. Pieris rapae recorded
its most important relative abundance in three stations:
cedar forest, oak forest and wasteland with, respectively:
46.38%, 47.68% and 35.05%. C. croceus also recorded
146 Berkane S., Rahmani A., Ari B., Moulaï R.
Table 1. Inventory and numbers of diurnal Lepidoptera species recorded in the four stations of the Belezma National Park
(March 2010 – February 2011) (name in bold: protected species in Algeria).
Species Code Cedar forest Oak forest Wasteland Pine forest
Anthocharis belia (Linnaeus, 1767) A.be 0 0 3 0
Argynnis pandora (Denis et Schiffermüller, 1775) A.pa 80 60 0 15
Callophrys avis (Chapman, 1909) C.av 0 1 0 0
Chelis maculosa (Gerning, 1780) C.ma 0 0 2 0
Coenonympha pamphilus (Linnaeus, 1758) C.pa 0 0 0 5
Colias croceus (Geoffroy in Fourcroy, 1785) C.cr 40 20 52 33
Euchloe ausonia (Hübner, 1803) E.au 0 0 14 0
Euchloe belemia (Esper, 1800) E.be 0 0 12 0
Euchloe charlonia (Donzel, 1842) E.ch 0 0 2 0
Glaucopsyche melanops (Boisduval, 1828) G.me 24 1 12 2
Gonepteryx cleopatra (Linnaeus, 1767) G.cl 9 5 40
Hipparchia algiricus (Oberthür, 1876) H.al 65 57 7 0
Hipparchia ellena (Oberthür, 1893) H.el 77 44 2 0
Lampides boeticus (Linnaeus, 1767) L.bo 3 0 2 0
Lasiommata megera (Linnaeus, 1767) L.me 4003
Lycaena phlaeas (Linnaeus, 1761) L.ph 0 2 8 5
Maniola jurtina (Linnaeus, 1758) M.ju 0 0 40
Melanargia galathea (Linnaeus, 1758) M.ga 6 0 40
Melanargia ines (Hoffmannsegg, 1804) M.in 0 0 0 3
Melanargia occitanica (Esper, 1789) M.oc 0 5 0 0
Melitaea aetherie (Hübner, 1826) M.ae 1 0 0 0
Nymphalis polychloros (Linnaeus, 1758) N.po 3 0 0 0
Pararge aegeria (Linnaeus, 1758) P.ae 14 100
Pieris brassicae (Linnaeus, 1758) P.br 3 1 16 0
Pieris rapae (Linnaeus, 1758) P.ra 43 29 34 29
Polyommatus icarus (Rottemburg, 1775) P.ic 2 0 0 0
Pontia daplidice (Linnaeus, 1908) P.da 0 0 70
Pyrgus armoricanus (Oberthür, 1910) P.ar 4000
Tomares ballus (Fabricius, 1787) T.ba 0 1 6 5
Vanessa cardui (Linnaeus, 1758) V.ca 1 0 0 0
Figure 2. Diagram of frequencies of occurrence of diurnal Lepidoptera species observed by stations in the Belezma National
Park.
high relative abundance in the pine forest and wasteland
with, respectively: 30.2% and 25.63% (Figure 3).
After one year of prospecting, the total species rich-
ness varied between 9 and 18 species. The wasteland
proved to be the richest station with 18 species. It was
followed by cedar forest (17 species) and oak forest (12
species). The pine forest was the least rich station with
only 9 species.
The average richness expressed in the average number of
species per survey followed the same order. The highest
147Diversity and ecology of diurnal Lepidoptera in Belezma National Park (Aurès, Algeria)
values were recorded at the wasteland and cedar forest
with, respectively, 4.23 and 3.5 species per survey.
They were followed by oak forest and pine forest with,
respectively, 2.5 and 2.06 species per survey.
When calculating the Shannon-Weaver Diversity Index
and Equitability Index applied to the four stations, the
most diversied station was the wasteland with a value
of 3.49 bits. It was followed by cedar forest (3.16 bits)
and oak forest (2.58 bits). Finally, the pine forest proved
to be the least diversied station with a value of 2.56 bits.
The wasteland was also the most balanced station with
a fairness value of 0.84. Then came the pine forest with
0.81 and the cedar forest with 0.77. The least balanced
station was the oak forest, with 0.72 (Table 2).
According to the Sörensen similarity coefcient, the
cedar and oak forest stations were the most similar with
62% in common. Then came the oak forest, which had a
similarity of 60% with the wasteland and 57% with the
pine forest. Next were the cedar forest and wasteland
stations, which were 55% similar. Finally, with similar
percentages, the pine forest had a similarity of 38% with
the cedar forest and 37% with the wasteland.
Statistical study
Figure 4 shows that axis 1 represents 64% of the graph’s
inertia and axis 2 represents 26%. Between them, they
have 90% inertia. Some amenities between the environ-
ments and species present are observable. The graph
shows the existence of three groups, distributed on either
side of the two axes.
The group G1 is represented by the wasteland. It is on
the positive side of both axes. It includes the following
species: Euchloe ausonia, E. belemia, E. charlonia,
Pontia daplidice, Anthocharis belia, Chelis maculosa,
Maniola jurtina and Pieris brassicae.
The group G2 represented by the pine forest is on
the positive side of axis 1 and on the negative side of
axis 2. It is characterized by the presence of two species:
Coenonympha pamphilus and Melanargia ines.
The group G3 consists of two stations: the cedar
forest and the oak forest. It is on the positive side of
axis 2 and on the negative side of axis 1. It includes
the following species: Argynnis pandora, Callophrys
avis, Hipparchia algiricus, H. ellena, M. occitanica,
Melitaea aetherie, Nymphalis polychloros, Pararge
aegeria, Polyommatus icarus, Pyrgus armoricanus
and Vanessa cardui.
Finally, some species are found in the middle of the
graphical representation. The cedar forest and waste-
land share the following species: Gonepteryx cleo-
patra, Glaucopsyche melanops, Lampides boeticus and
Melanargia galathea. Between the pine forest and the
wasteland, there are: Lycaena phlaeas and Tomares bal-
lus. Between the oak forest and the pine forest, there is
Lasiommata megera. Finally, between all the stations,
Pieris rapae and Colias croceus are located.
Figure 3. Diagram of relative abundance of diurnal Lepidoptera species observed by stations in the Belezma National
Park.
Table 2. Species richness (S), average richness (Sm), Shannon-
Weaver Diversity Index (H′), Maximum Diversity Index
(H′max), Equitability Index (E), of Rhopaloceran and diurnal
Heteroceran species observed at the stations in the Belezma
National Park during the study period (March 2010 – Febru-
ary 2011).
Types of habitats S Sm H′ (bits) H′max (bits) E
Cedar forest 17 3.5 3.2 4.1 0.8
Oak forest 12 2.5 2.6 3.6 0.7
Wasteland 18 4.2 3.5 4.2 0.8
Pine forest 9 2.1 2. 6 3.2 0.8
148 Berkane S., Rahmani A., Ari B., Moulaï R.
Figure 4. Distribution of diurnal Lepidoptera species among
the study stations at the Belezma National Park, as determined
by Correspondence Analysis (CA).
DISCUSSION
The monitoring of Belezma National Park’s diurnal Lepi-
doptera enabled us to identify 30 species, among which
29 represented Rhopalocera (Nymphalidae, Pieridae,
Lycaenidae, Hesperiidae) and only 1 species of diurnal
Heterocera, belonging to the family Arctiidae. Rhopalocera
represent 24.17% of the total number of species recorded
in Algeria, which counts 120 according to Tennent (1996).
Lepidoptera groups that are less specic to their host plants
are richer in species (Weincatner et al. 2006). For this
study, the Nymphalidae (13 species) were at the top of the
ranking. They were followed by Pieridae (9 species), then
Lycaenidae (6 species). Finally, there were the Hesperiidae
and Arctiidae, which each had 1 species.
Some species were omnipresent and in large numbers, as
was the case for ubiquitous species such as Pieris rapae in
the cedar and oak forests and Pontia daplidice in the pine
forest. On the other hand, other species were omnipres-
ent (high occurrence frequencies) but generally not very
abundant (low relative frequencies). This was the case
for Glaucopsyche melanops and Pieris brassicae in the
wasteland and Lycaena phlaeas in the oak forest.
The specic richness of the four stations varied between
9 and 18 species. The wasteland was the most diversied
(18 species) and most balanced (E = 0.8), as this station
has many nectariferous plants: Retama raetam, Sinapis
arvensis, Lavandula stoechas and Thymus vulgaris
(Smaihi and Kalla 2017; P. N. B. 2010; Sahli 2004). This
type of open environment is most valued by butteries
and particularly bio-indicators of open environments
(Faure 2007; Demerges and Bachelard 2002). In some
cases, the rarity or location of a species may correspond
to that of its host plant (Tolman and Lewington 1999). For
example, the presence of Euchloe ausonia in wasteland
can be explained by the presence of Sinapis arvensis
(Tennent 1996). Altitude is also a determining factor
for the presence of certain species. This may explain the
presence of Melitaea aetherie only in the cedar forest
(1300 m). This species has been recorded in the Aurès
region between 1200 and 1800 m altitude (Tolman and
Lewington 1999). However, when tree cover is important,
it affects species that depend on open environments and
warm micro-climates. As trees create a cool microclimate,
forests do not generally represent preferential environ-
ments for daytime species (Chinery and Cuisin 1994).
This may explain a lower number of species observed
in forest stations such as: oak forest (12 species) and
pine forest (9 species). However, the cedar forest (17
species) was rather rich in buttery species. This may
mean that this station represents a more degraded envi-
ronment than the two previous ones. Degradation is due
mainly to anthropogenic action through illegal logging
and overgrazing and a multitude of other factors such
as diseases linked to defoliating insects (lepidoptera) or
certain parasites, one of which is a wood-eating fungus of
the genus Armillaria and another is a wood-boring insect
(Boukerker 2016; P. N. B. 2010 by P. N. B. 2006; Sahli
2004). This results in a decline in cedar to the benet of
other species and the presence of open spaces within the
station itself.
According to the Sörensen similarity coefcient, the
cedar forest and oak forest were the most similar with
62%, noting that these two stations are located in the
geographically close western sector of the park (Fig-
ure 1). Both also suffer from the state of degradation
that affects most Mediterranean woodlands (Sahli 2002;
Quezel et al. 1999). The cedar forest sampled for this
work was accompanied by a oral procession resulting
from extensive degradation (overgrazing, illegal and
abusive cutting). Because of this opening of the popula-
tion, the oral procession is no longer strictly sylvatic,
but strongly inltrated by a lot of species from open en-
vironments. Particularly noteworthy in this cedar forest
was the abundance of the genus Asphodelus, which is
characteristic of livestock resting areas, where the soil is
highly enriched in nitrate by cattle droppings (Boukerker
2016). It is also important to note that forest res, ampli-
ed by human action on these natural Belezma entities
(clearing, cutting and pastoral pressure), considerably
transform the oak landscape into less closed formations
(Smaihi and Kalla 2017).
149Diversity and ecology of diurnal Lepidoptera in Belezma National Park (Aurès, Algeria)
The Correspondence Analysis showed aggregations
between the environments and species present. Two
types of environments: wasteland and pine forest, stood
out and the other two environments: cedar forest and
oak forest, grouped together in a single cluster. The
distribution of species along axis 1 followed a gradient
of habitat openness and along axis 2 in relation to but-
tery species richness.
For all species aggregated at the wasteland level, these
were species linked to an open and owering environment.
This is the case for the Pieridae, which frequent both open
environments and forest borders (Chinery and Cuisin
1994). One of these, for example, was Pontia daplidice,
which is an indigenous migratory buttery in North Africa.
This also applied to Pieris brassicae, a migratory species
that frequents all kinds of environments. In the wasteland
there was the high-altitude buttery Chelis maculosa. Two
specimens were recorded at this station, at an altitude of
nearly 1000 m. Very distinct, the pine forest has only two
species: Coenonympha pamphilus and Melanargia ines.
During this study, these two species were found to be ex-
clusive to this environment. These are species that frequent
herbaceous environments, meadows and wastelands, where
their caterpillars nd the hosts they need, especially grasses
(Tolman and Lewington 1999). Their presence at this sta-
tion was perhaps due to the the present forest being a young
Aleppo pine forest, with low trees and undergrowth rich in
herbaceous plants (Garah et al. 2016; Litim 2012). For the
other two environments, all species were located among
them; however, with specic aggregations at each station.
These two environments are characterized, rst, by their
locations – they happen to be located in the same sector
of the park (western sector) (Figure 1) and, secondly, by
their degraded condition, which has caused them to become
open environments (Smaihi and Kalla 2017). The cedar
forest shelters: Melitaea aetherie, Nymphalis polychloros,
Pararge aegeria and Hipparchia ellena. All these species
are fond of light woods. Then, Pyrgus armoricanus and
H. algiricus follow. They both frequent rocky escarpments
and owery grasslands. This observation shows the alarm-
ing situation of this station, which is suffering from decline
(Bentouati 2008). The decline in the park’s cedar forests
is said to be due as much to the attacks of a wood-boring
insect discovered in 1982 (Thaumetopoea bonjeani) and
its weakening by a succession of dry years spread over the
decade 1992–2002, as to man and his herds (Kherchouche
et al. 2013; Sahli 2004). Finally, there is also the presence
of Vanessa cardui and Polyommatus icarus. These two
butteries inhabit a wide variety of habitats (Tolman and
Lewington 1999). The oak forest sampled for this work
(1320 m above sea level) appears with a procession as-
sociated with high altitude environments, but with two
more characteristic species: Melanargia occitanica, which
resides in the scrubland and along the edge of the forests,
and Argynnis pandora, which frequents all types of wooded
areas. Finally, the oak forest houses Callophrys avis, which
is adapted to many ecological and climatic environments.
This species is common within brush, in clearings and in
shaded rocky areas (Tolman and Lewington 1999). Our
observations revealed that the degradation of sulphur in
this station was of a smaller scale than that of the cedar
forest, because the oak forest of the BNP was experienc-
ing renewal and regeneration and, above all, reforestation
successes (Smaihi and Kalla 2017). Finally, some species
were indifferent to a particular environment, which means
that they were in the middle of the graphical representa-
tion. Cedar forest and wastelands share species that prefer
open spaces or low-density woods. This was the case for
the following butteries: Gonepteryx cleopatra, which
ies in open scrubland, often rocky and near light woods;
Glaucopsyche melanops, which frequents scrubland
and light woods; Lampides boeticus, whose habitat is
varied: wastelands, crops, pleasure gardens; and nally,
M. galathea, which resides in all types of shrubland (Tol-
man and Lewington 1999). Between the pine forest and
the wasteland, there were: Lycaena phlaeas, a lepidopteran
that likes wasteland, and Tomares ballus, which likes dry
open meadows and rocky places (Tolman and Lewington
1999). In addition, between the oak grove and the pine
forest, there is Lasiommata megera, which frequents
scrubland and rocky areas (Tolman and Lewington 1999).
Finally, for all the habitats there is Pieris rapae, which ies
to almost everywhere its host plants grow. This species
prefers temporary meadows and wastelands. Finally, there
is Colias croceus, a native of the temperate regions around
the Mediterranean, which prefers owering fallow lands
(Tolman and Lewington 1999).
CONCLUSION
The monitoring of diurnal Lepidoptera in the Belezma
National Park enabled us to count 896 individuals,
representing 30 species: 29 Rhopalocera (Nymphali-
dae, Pieridae, Lycaenidae, Hesperiidae) and 1 diurnal
Heterocera (Arctiidae). The Rhopalfauna of the BNP is
interesting from a diversity point of view. It represents
24.17% of the Algerian rhopalfauna, which has 120
species according to Tennent (1996).
The species encountered during this study were for the
most part those that are frequent and widespread in
Algeria (Tolman and Lewington 1999). Three species
were identied at all the stations studied: Colias croceus,
Glaucopsyche melanops, and Pieris rapae. Others, on
the contrary, were found only on one of the 4 sites: Meli-
taea aetherie, Nymphalis polychloros, Pararge aegeria,
Polyommatus icarus, Pyrgus armoricanus, and Vanessa
cardui were observed only in the cedar forest; Callophrys
opinion and Melanargia occitanica were only found in
the oak forest; Coenonympha pamphilus and Melanargia
150 Berkane S., Rahmani A., Ari B., Moulaï R.
ines only in the pine forest; and nally Anthocharis belia,
Chelis maculosa, Euchloe ausonia, E. belemia, E. char-
lonia, Maniola jurtina and Pontia daplidice only in the
wasteland. Among the 30 species listed, we noted the
presence of 3 species protected by Algerian law, namely:
Colias croceus, Polyommatus icarus and Melanargia
galathea. These species deserve attention, particularly
for the preservation of useful species and the orientation
of research on species considered rare or threatened.
The primary objective of this work, namely, to establish
a rst list of the diurnal Lepidoptera fauna of the park,
has been achieved – even if this list remains open and the
number of Lepidoptera is likely to change signicantly
in unsurveyed environments.
Secondly, the observation revealed by this inventory is
that despite the efforts of the park services to safeguard
existing forest formations (P. N. B. 2005; Laabed 2001),
these remain insufcient. Indeed, the Correspondence
Analysis carried out on the diurnal Lepidoptera and their
presence in the four sampled stations made it possible
to identify certain groups according to a gradient of
openness of the environments. It appears that the forest
stations of this inventory were populated with butteries
which are bio-indicators of open environments. These
stations therefore will always suffer from a depletion
of tree populations.
We therefore recommend monitoring forest stands that
are conserved using bio-indicator butteries in order to
have more data on their evolution over time, in order to
validate or refute the methods used to restore and maintain
them. We propose this monitoring method because diurnal
Lepidoptera monitoring can give much faster results than
those provided by vegetation monitoring (Faure 2007).
Finally, in order to better protect butteries in the park,
particularly the most vulnerable species, knowledge
of their environments and specic needs must be im-
proved by park services. They will have to consider
the primary importance of studying and safeguarding
these emblematic and benecial insects in their future
development projects.
ACKNOWLEDGEMENTS
We would like to thank the following institutions for their
support: Belezma National Park and the Laboratories of
Ecology and Environment and Applied Zoology and Ani-
mal Ecophysiology, University of Bejaia. We would also
like to express our gratitude to the following people: Mr.
Saïd Rahmani, Director of Belezma National Park, and all
his team both for the permits granted and for their welcome,
in particular: Mr. Gagâ Abdelkrim and Mr. Righi Yassine.
We also express our sincere thanks to the forest rangers of
Belezma for their support and friendship.
References
Arbouche, Y., H. S. Arbouche, F. Arbouche, and R. Ar-
bouche. 2012. Valeur fourragère des espèces prélevées
par Gazella cuvieri Ogilby, 1841 au niveau du djebel
metlili (Algérie). [Feed value of species levied by
Gazella cuvieri Ogilby, 1841 at the djebel metlili
(Algeria)]. Arch. Zootec. 233: 145–148.
Bentouati, A. 2008. La situation du cèdre de l’Atlas dans
les Aurès (Algérie). [The situation of Atlas cedar in the
Aurès (Algeria)]. Forêt méditerranéenne 2: 203–208.
Boukerker, H. 2016. Autoécologie et évaluation de la biodi-
versité dans les Cédraies de Cedrus atlantica Manetti
dans le parc national de Belezma (Batna, Algérie).
[Autoecology and evaluation of the biodiversity in
the Cedar forests of Cedrus atlantica Manetti in the
National park of Belezna (Batna, Algeria)]. Thèse de
Doctorat d’Etat., Université de Biskra (Algérie).
Carriere, M. 2013. Les papillons par la photo. [Butteries
by the photo]. France: Les-Snats.
Chinery, M., and M. Cuisin. 1994. Les papillons d’Europe
(Rhopalocères et Hétérocères diurnes). [The European
butteries (Rhopalocera and diurnal Heterocera)].
Paris: Delachaux et Niestlé.
Dajoz, R. 1971. Précis d’écologie. [ Ecology precise]. Paris:
Dunod.
Dajoz, R. 1985. Précis d’écologie. [ Ecology precise]. Paris:
Bordas.
Demerges, D., and P. Bachelard. 2002. Proposition de mise
en place d’une méthode de suivi des milieux ouverts
par les Rhopalocères et Zygaenidae dans les réserves
naturelles. [Proposal to set up a method for monitoring
open environments with Rhopaloceres and Zygaenidae
in the French natural reserves]. http://www.reserves-
naturelles.org/actualites/sUIVIRHOPALO.pdf.
Faure, E. 2007. Suivie de milieux ouverts dans le parc
naturel régional du luberon par des papillons de jour
(rhopalocères) bioindicateurs. [Monitoring of open
areas in the Regional natural park of Luberon by using
butteries (Rhopalocera) like bioindicators]. Soc. His.
Nat. Alcide-d’Orbigny 8: 86–101.
Faurie, C., C. Ferra, P. Medori, and J. Devaux. 2003. Écolo-
gie – approche scientique et pratique. [Ecology – sci-
entic and practical approach]. Paris: TEC&DOC.
Garah, K., C. Chafai, and A. Bentouati. 2016. Evolution
spatio-temporelle Des écosystèmes forestiers à Pin
d’Alep de l’Aurès Oriental en Algérie. [Spatiotempo-
ral evolution of ecosystems Aleppo Pine forest in the
Aurès Oriental in Algeria]. Lebanese Science Journal
17: 104–116.
Hammer, O., D. A. T. Harper, and P. D. Ryan. 2001. Past: Pale-
ontological Statistics Soft Ware Package for Education and
Data Analysis. Palaeontologia Electronica 4 (1): 9.
Houamel, A. C. 2012. Contribution à l’étude du dépérisse-
ment de la cédraie dans la région de Batna (cas du
151Diversity and ecology of diurnal Lepidoptera in Belezma National Park (Aurès, Algeria)
parc national du Belezma). Diplôme de Magister.,
Université de Tlemcen (Algérie). [Contribution to the
study of cedar decline in the Batna region (case of
Belezma National Park). Magister of Tlemcen Uni-
versity (Algeria)].
Kherchouche, D., M. Kalla, A. Briki, and A. Hamchi. 2013.
La sécheresse et le dépérissement du cèdre de l’Atlas
(Cedrus atlantica Manetti.) dans le massif du Belezma
(Algérie). [Drought and die back of Atlas cedar (Cedrus
atlantica Manetti) in the Belezma mountains (Algeria)].
Sécheresse 24: 129–137.
Laabed, A. 2001. Plan de gestion du Parc National du
Belezma. Rapport multigraphié., Batna (Algérie).
[Management plan for the Belezma National Park.
Multigraphic report]. Batna (Algeria).
Litim, A. 2012. Biodiversité et Étude Ethnobotanique dans le
Parc National de Belezma (Batna). Diplôme de Master.,
Université de Sétif (Algérie). [Biodiversity and Eth-
nobotanical Study in Belezma National Park (Batna).
Master of Sétif University (Algeria)].
MAB-Algérie. 2016. Rapport du comité national MAB –
Algérie. [Report of the National Committee MAB –
Algeria].
Magurran, A. E. 1988. Ecological Diversity and its Measurement.
New Jersey: Princeton University Press.
Manil, L., P.-Y. Henry, A. Lerch, C. Edelist, K. Ancrenaz,
M. Gaboly, B. Fontaine, R. Lorrilliere, and R. Julliard.
2007. Suivi Temporel des Rhopalocères de France Bilan
2006–2007. [Temporal Monitoring of Rhopalocerans
in France 2006–2007 Assessment]. Paris: MNHN et
ALF.
Moore, N. W. 1975. Buttery transects in a linear habitat,
1964–73. Entomologist’s Gazette 26: 71–78.
Ouin, A., J-M. Paillisson, and J. Lhonore. 2000. Méthodes
de suivi et d’évaluation des populations et peuplements
de papillons de jour. [Methods for monitoring and
evaluating buttery populations and stands]. Insectes
117: 29–31.
Pielou, E. C. 1969. An introduction to Mathematical Ecol-
ogy. New York: Witley-Interscience.
P. N. B. – CF1 2005. Rapport sur le plan de sauvegarde de
la cédraie de la Wilaya de Batna (Algérie). [Report on
the safeguarding plan for the cedar grove of the Wilaya
Batna (Algeria)].
P. N. B. 2010. Plan de gestion du parc national de Belezma
2006–2010. [Belezma National Park Management
Plan 2006–2010]. Jijel (Algeria), as follows (P. N. B.
2006. Plan de gestion du parc national de Belezma
2006–2010. [Belezma National Park Management Plan
2006–2010]. Batna (Algeria).
Pollard, E., and T. J. Yates. 1993. Monitoring Butteries for
Ecology and Conservation. London: Chapman & Hall.
Quézel, P., F. Médail, R. Loisel, and M. Barbero. 1999.
Biodiversité et conservation des essences forestières
du bassin méditerranéen. La Forêt Méditerranéenne.
[Biodiversity and conservation of forest essences in the
Mediterranean basin]. Unasylva 197: 21–28.
Ramade, F. 1984. Elément d’écologie: écologie fondamen-
tale. [ Ecological element: fundamental ecology]. Paris:
McGraw-Hill.
Remini, L., and R. Moulaï. 2015. Diversity and structure
of buttery populations in agro-ecosystems of Mitidja
(Algeria). Zoology and Ecology 25 (4): 355–364.
Robineau, R. 2007. Guide des papillons nocturnes de
France. [Guide to the moths of France]. Paris: Delach-
aux et Niestlé.
Sahli, M. 2002. Le recul des forêts en Méditerranée: le
cas des monts du Belezma (Algérie). Annales volume
V: 65–79. Publication du laboratoire d’Etudes et de
Recherches Maghreb-Méditerranée. Université de
Constantine (Algérie). [The decline of forests in the
Mediterranean: the case of the Belezma Mountains
(Algeria). Publication of the Maghreb-Mediterranean
Studies and Research Laboratory. University of Con-
stantine (Algeria)].
Sahli, M. 2004. Protection de la nature et développement:
cas du Pare national du Belezma (Monts de Batna, Al-
gérie). [Nature protection and development: the case of
the Belezma National Park (Batna Mountains, Algeria)].
New Medit. 4: 38–43.
Sahli, M. 2004. Conservation et développement dans le Parc
National du Belezma (Wilaya de Batna, Algérie). [Con-
servation and development in the Belezma National Park
(Wilaya of Batna, Algeria)]. Revue sciences Humaines
22: 81–91. Université de Constantine, Algérie.
Samraoui, B. 1998. Status and seasonal patterns of adult
Rhopalocera (Lepidoptera) in north-eastern of Algeria.
Nachr. entomol. Ver. Apollo N. F. 19: 285–298.
Smaihi, H., and M. Kalla. 2017. Evolution spatiotemporelle
des formations végétales du parc national de belezma
de la région Est de l’Algérie. [Spatiotemporal evolu-
tion of plant formations in the Belezma National Park
of Eastern Algeria]. Courrier du Savoir 24: 175–184.
Université de Biskra, Algérie.
Tarrier, M. R., and J. Delacre. 2008. Les papillons de jour
du Maroc, guide d’identication et de bio-indication.
[Moroccan butteries, a guide to identication and
bio-indication]. Paris: Biotope, Mèze.
Tennent, W. J. 1996. The Butteries of Morocco, Algeria and
Tunisia. England: Gem Publishing Company.
Tolman, T., and R. Lewington. 1999. Guide des papil-
lons d’Europe et d’Afrique du Nord. [European and
North African Buttery Guide]. Paris: Delâchaux et
Niestlés.
Weincatner, E., N. Wahlberg, and S. Nylin. 2006. Dynam-
ics of host plant use and species diversity in Polygonia
butteries (Nymphalidae). Journal of Evolutionary
Biology 19: 483–491.