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Seasonal Variations in the Diet and Food Selection of the Algerian Hedgehog Atelerix algirus

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Abstract

The Algerian hedgehog Atelerix algirus is an insectivorous species. However, the exact composition of its natural diet remains largely undetermined, especially in relation to seasonal variations in food availability. From March to November, we simultaneously analysed the composition of 180 hedgehog faecal samples and food availability in the Soumman Valley, Algeria to assess food selection in this species. The faeces contained 196 different prey species, of which 92% belonged to the class Insecta. The highest prey species diversity was found in the Coleoptera order (100 species recorded) and the highest species occurrence was found in Hymenoptera (65% of the prey items, mainly represented by the harvester ant Messor barbarus, a crop-ravaging species). This study shows that the Algerian hedgehog is mainly a generalist species with a diet that is strongly linked to food availability. However, seasonal variations were observed in prey selection, and a notable shift in food preference was observed during autumn. The exact nature of these changes in feeding behaviour remains to be investigated, notably in relation to changes in energy requirements of this species before hibernation, in terms of quantity and/or quality.
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African Zoology
ISSN: 1562-7020 (Print) 2224-073X (Online) Journal homepage: http://www.tandfonline.com/loi/tafz20
Seasonal variations in the diet and food selection
of the Algerian hedgehog Atelerix algirus
Chafika Mouhoub-Sayah, Hafsa Djoudad-Kadji, Florian Kletty, André Malan,
Jean-Patrice Robin, Michel Saboureau & Caroline Habold
To cite this article: Chafika Mouhoub-Sayah, Hafsa Djoudad-Kadji, Florian Kletty, André Malan,
Jean-Patrice Robin, Michel Saboureau & Caroline Habold (2018) Seasonal variations in the diet
and food selection of the Algerian hedgehog Atelerix algirus, African Zoology, 53:1, 1-10, DOI:
10.1080/15627020.2017.1419072
To link to this article: https://doi.org/10.1080/15627020.2017.1419072
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Published online: 22 Mar 2018.
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African Zoology 2018, 53(1): 1–10
Printed in South Africa — All rights reserved
Copyright © Zoological Society
of Southern Africa
AFRICAN ZOOLOGY
ISSN 1562-7020 EISSN 2224-073X
https://doi.org/10.1080/15627020.2017.1419072
African Zoology is co-published by NISC (Pty) Ltd and Informa UK Limited (trading as Taylor & Francis Group)
Agricultural intensification has occurred in recent decades
across most of the world, causing a major decline in
biodiversity (Macdonald et al. 2007). This decline has been
described in farmland birds and invertebrates (Donald et al.
2001; Stoate et al. 2001), and more recently in mammals
(Macdonald et al. 2007).
The Algerian hedgehog Atelerix algirus is a small mammal
living in agricultural areas of North Africa. The IUCN
considers the status of this species to be Least Concern.
However, in general, hedgehogs are declining in northern
Africa, but population trends are not known for the Algerian
hedgehog (Amori et al. 2008). It is necessary to understand
the biology of this species and its role in the ecosystem,
especially within the food web. The diet of the Algerian
hedgehog is composed of many phytophagous insects, other
invertebrate species and some vertebrates (e.g. Doumandji
and Doumandji 1992; Sayah 1996). Its strongly seasonal
lifecycle enables it to face environmental constraints: the
Algerian hedgehog hibernates in winter, reproduces in spring
and builds up energy reserves for the following hibernation
period during summer and autumn (Mouhoub-Sayah et al.
2008). Doumandji and Doumandji (1992) suggest possible
seasonal variations in its diet. Such variations could be
explained by specific energy requirements at certain key
points of its life cycle and/or by variations in prey availability.
However, neither prey availability nor seasonal variations
have been assessed in previous studies of the Algerian
hedgehog diet.
This study examines the diet of the Algerian hedgehog
to better understand its place in the ecosystem. This was
achieved by making a precise analysis of the different diet
components, identifying possible seasonal variations and
assessing links between diet and prey availability in order to
establish if the Algerian hedgehog is completely generalist
or if specialisation occurs for certain types of prey.
Materials and methods
Study site
The Algerian hedgehog is widespread in North Africa,
with a distribution ranging from the Atlas Mountains to the
Mediterranean coast (Sahraoui-Brahim 1984) and covering
all of northern Algeria (Sellami et al. 1989). The study was
conducted in the Soummam Valley region, which begins
on the south-western side of the Djurdjura mountains
in Algeria (36°21′ N, 3°53′ E) and ends 120 km further
east on the Mediterranean coast near Béjaïa (36°45′ N,
5°20′ E). This valley contains mainly cultivated plots located
Seasonal variations in the diet and food selection of the Algerian hedgehog
Atelerix algirus
Chafika Mouhoub-Sayah1, Hafsa Djoudad-Kadji1, Florian Kletty2, André Malan3, Jean-Patrice Robin2, Michel Saboureau3
and Caroline Habold2*
1 Laboratoire de Zoologie Appliquée et d’Ecophysiologie Animale, Faculté des Sciences de la Nature et de la Vie, Université
de Bejaïa, Bejaïa, Algeria
2 Université de Strasbourg, CNRS, IPHC, UMR 7178, Strasbourg, France
3 Institut des Neurosciences Cellulaires et Intégratives, Département de Neurobiologie des Rythmes, CNRS UPR-3212,
Université de Strasbourg, Strasbourg, France
* Corresponding author, email: caroline.habold@iphc.cnrs.fr
The Algerian hedgehog Atelerix algirus is an insectivorous species. However, the exact composition of its natural
diet remains largely undetermined, especially in relation to seasonal variations in food availability. From March
to November, we simultaneously analysed the composition of 180 hedgehog faecal samples and food availabil-
ity in the Soumman Valley, Algeria to assess food selection in this species. The faeces contained 196 different
prey species, of which 92% belonged to the class Insecta. The highest prey species diversity was found in the
Coleoptera order (100 species recorded) and the highest species occurrence was found in Hymenoptera (65% of the
prey items, mainly represented by the harvester ant Messor barbarus, a crop-ravaging species). This study shows
that the Algerian hedgehog is mainly a generalist species with a diet that is strongly linked to food availability.
However, seasonal variations were observed in prey selection, and a notable shift in food preference was observed
during autumn. The exact nature of these changes in feeding behaviour remains to be investigated, notably in
relation to changes in energy requirements of this species before hibernation, in terms of quantity and/or quality.
Keywords: agricultural area, dietary preference, ecosystem, feeding behaviour, food niche, insectivore
Online supplementary material: Supplementary information for this article is available at https://doi.org/10.1080/15627020.2017.1419072
Introduction
Published online 22 Mar 2018
Mouhoub-Sayah, Djoudad-Kadji, Kletty, Malan, Robin, Saboureau and Habold
2
alongside urban centres and scattered hamlets. Vegetation
is typical of the Mediterranean region, primarily made up
of farmland (fruit and vegetable crops, such as potato,
tomato, melon and watermelon) separated by hedges
and trees (cork oak Quercus suber, holm oak Quercus
ilex, Aleppo pine Pinus halepensis, poplar Populus spp.
and olive Olea europaea). The climate is Mediterranean,
with hot, dry summers and cool, rainy winters (mean
temperature and rainfall for Béjaïa, Algeria for July–
September from 1974 to 2008 is 24.5 °C and 21.8 mm,
and for January–March from 1974 to 2008 is 12.5 °C and
90.6 mm). The location and timing of our data collection
was planned using the study by Mouhoub-Sayah et al.
(2009) of the spatio-temporal distribution of this species
in this area. Data were obtained for cropland, grassland,
woodland stream and forest edge habitats, the four charac-
teristic habitats of the Soummam Valley. Samples were
collected at four specific areas, referred to hereafter as
stations, i.e. one station per habitat.
Sample collection and analysis
The diet of the Algerian hedgehog
Faecal samples were collected from March to November
2004, the period of activity for this species. Faecal pellets
were rarely found from December to February, when
the animal is hibernating (Mouhoub-Sayah et al. 2008).
A total of 305 samples were collected, of which 180 (five
faecal samples per habitat per month) were randomly
selected for analysis. Samples were collected on the
second and the fourth week of each month along four
500-m-long transects at each station. To determine the
composition of faeces, faecal samples were soaked in 2%
formaldehyde solution, broken up and filtered through a
sieve (1 mm mesh) to retain the rigid cuticles of arthropods.
The aqueous solution and any particles that had passed
through the sieve were collected in a beaker and stored
at ambient temperature for the subsequent determina-
tion of the presence of earthworm setae (Mouches 1981).
Prey species were identified with identification guides
(Bernard 1968; Reichholf-Riehm 1984; Du Chatenet 1986;
Chinery 1988; Zahradník and Severa 1988; Tolman and
Lewington 1999; Passera 2008), and by referring to the
large arthropod collections at the insectarium of the Ecole
Nationale Supérieure Agronomique Entomology laboratory
(El Harrach, Algeria), and the Laboratoire de Zoologie
Appliquée et d’Écophysiologie Animale (Béjaïa, Algeria).
The analysis relied on specific undigested elements for
each taxon, according to identification keys. To avoid
overestimating the number of individuals in each prey
species, the counting relied either on unique body elements
(e.g. the thorax for Hymenotera) or on characteristic
elements (e.g. setae in Oligochaeta).
Food availability
During the same study period, we made a monthly
inventory of the food items available in each of the four
habitats. A sweep net was used to capture Orthoptera,
Diptera and Lepidoptera individuals (Benkhelil 1991). Ten
sweeps were carried out at five different locations in each
of the four stations. Pitfall traps were used to catch crawling
arthropods such as Coleoptera or Myriapoda, and also any
flying insects that landed on the trap (Benkhelil 1991). In
each station, 10 pitfall traps were placed in a line at 10 m
intervals and collected 48 h later. These methods permitted
the qualitative and quantitative sampling of invertebrates
that may make up the staple diet of the Algerian hedgehog.
The collected invertebrates were then identified, using the
means cited above.
Data analysis
Sample data were separated into sets for spring (collected
in April, May and June), summer (July, August and
September), autumn (October and November) and winter
(March) for the assessment of seasonal diet and prey
availability. Total species richness (S) was defined by
the number of species found in the different taxa during
the whole year. Percentages represent the proportion of
animals (prey or available animals found in the season/
month) for the concerned taxon.
Analyses were conducted using Statistica 5.5 (StatSoft,
Tulsa, OK, USA, 1999), Sigma Stat 3.5 (Jandel Scientific
Software, San Rafael, CA, USA, 2005) and R 3.3.2
software (R Core Team 2016). Results were analysed using
ecological indices of composition and structure. Shannon–
Weaver’s diversity index was calculated as
1
2
1
log
s
ii
i
H pp
=
=−⋅
2
11
11
n
iij ik
ij
nn
ik
ii
ij ik
jk
Cnn
NN
ρρ
=
ρ +ρ
∑∑
−−
1
n
i
jij
Nn
=
=
1
n
i
kik
Nn
=
=
jj
Sa= ρ
1.96
Lower 95% confidence limit sin 2
xY

= −


1.96
Upper 95% confidence limit sin 2
xY

= +


2
rp
Dr p rp
=+−
where pi = ni
/N expresses the probability of encountering
the species i among the total number of species S, n is the
number of individuals in the different taxa and N represents
the total number of individuals across all collected species.
Equitability, or evenness, was calculated on the basis of
E = H/Hmax
where H is the Shannon–Weaver index as defined above
and Hmax is the theoretical maximum diversity with the
given sample size. Equitability varies between 0 and 1. A
value close to 0 occurs when almost all individuals belong
to a single species, whereas a value close to 1, indicating
complete equitability, occurs when each species is
represented by the same number of individuals (Ramade
1984). Morisita’s original index was chosen to compute
niche overlap between seasons as the most appropriate
and accurate calculation method when comparing counts
(Smith and Zaret 1982). It was calculated as described by
Krebs (2009), using the following formula :
1
2
11
11
n
iij ik
ij
nn
ik
ii
ij ik
jk
C
nn
NN
ρρ
=
ρ +ρ
∑∑
−−
1
n
i
jij
Nn
=
=
1
n
i
kik
Nn
=
=
jj
Sa= ρ
1.96
Lower 95% confidence limit sin 2
xY

= −


1.96
Upper 95% confidence limit sin 2
xY

= +


2
rp
Dr p rp
=+−
where C is Morisita’s index of niche overlap between
seasons j and k; ρij and ρik are the proportion of prey i in the
total prey for season j and k, respectively; nij and nik are the
number of prey i for season j and k, respectively; and Nj
and Nk are the total number of prey during season j and k,
respectively, i.e.,
1
2
1
log
s
ii
i
H pp
=
=−⋅
2
11
11
n
iij ik
ij
nn
ik
ii
ij ik
jk
Cnn
NN
ρρ
=
ρ +ρ
∑∑
−−
1
n
i
jij
Nn
=
=
1
n
i
kik
Nn
=
=
jj
Sa= ρ
1.96
Lower 95% confidence limit sin 2
xY

= −


1.96
Upper 95% confidence limit sin 2
xY

= +


2
rp
Dr p rp
=+−
and
1
2
1
log
s
ii
i
H pp
=
=−⋅
2
11
11
n
iij ik
ij
nn
ik
ii
ij ik
jk
Cnn
NN
ρρ
=
ρ +ρ
∑∑
−−
1
n
i
jij
Nn
=
=
1
n
i
kik
Nn
=
=
jj
Sa= ρ
1.96
Lower 95% confidence limit sin 2
xY

= −


1.96
Upper 95% confidence limit sin 2
xY

= +


2
rp
Dr p rp
=+−
.
African Zoology 2018, 53(1): 1–10 3
A Morisita’s index value of 1 indicates 100% overlap
between two niches, while a value of 0 shows there is
no overlap. Smith’s measure was used to assess niche
breadth (Smith 1982), using the formula
1
2
1
log
s
ii
i
H pp
=
=−⋅
2
11
11
n
iij ik
ij
nn
ik
ii
ij ik
jk
Cnn
NN
ρρ
=
ρ +ρ
∑∑
−−
1
n
i
jij
Nn
=
=
1
n
i
kik
Nn
=
=
jj
Sa
= ρ
1.96
Lower 95% confidence limit sin 2
xY

= −


1.96
Upper 95% confidence limit sin 2
xY

= +


2
rp
Dr p rp
=+−
where S is Smith’s measure of niche breadth, ρi is the
frequency of prey j in the diet and aj is the frequency of
prey j available in the environment. This measure ranges
from 0 (minimal) to 1 (maximal); it takes prey availability
into account and does not give greater weight to abundant
or rare prey, which occurs when using Hurlbert’s measure
or percentage similarity methods (Krebs 2009). An
approximate 95% confidence interval was obtained using
arcsine transformation as follows (Krebs 2009):
1
2
11
11
n
iij ik
ij
nn
ik
ii
ij ik
jk
Cnn
NN
ρρ
=
ρ +ρ
∑∑
−−
1
n
i
jij
Nn
=
=
1
n
i
kik
Nn
=
=
jj
Sa= ρ
1.96
Lower 95% confidence limit sin
2
xY

= −


1.96
Upper 95% confidence limit sin 2
xY

= +


2
rp
Dr p rp
=+−
1
2
1
log
s
ii
i
H pp
=
=−⋅
2
11
11
n
iij ik
ij
nn
ik
ii
ij ik
jk
Cnn
NN
ρρ
=
ρ +ρ
∑∑
−−
1
n
i
jij
Nn
=
=
1
n
i
kik
Nn
=
=
jj
Sa= ρ
1.96
Lower 95% confidence limit sin 2
xY

= −


1.96
Upper 95% confidence limit sin
2
xY

= +


2
rp
Dr p rp
=+−
where x = Arcsin(S) and Y is the total number of faecal
samples.
For food preference, Jacobs’ index was calculated as
1
2
1
log
s
ii
i
H pp
=
=−⋅
2
11
11
n
iij ik
ij
nn
ik
ii
ij ik
jk
Cnn
NN
ρρ
=
ρ +ρ
∑∑
−−
1
n
i
jij
Nn
=
=
1
n
i
kik
Nn
=
=
jj
Sa= ρ
1.96
Lower 95% confidence limit sin 2
xY

= −


1.96
Upper 95% confidence limit sin 2
xY

= +


2
rp
Dr p rp
=+−
where r is the proportion of a resource in the diet and p
is the proportion of the resource available in the habitat.
Values range from −1 (absolute prey avoidance) to 1
(absolute prey preference) (Krebs 2009; Kauhala and
Auttila 2010). If little data are available concerning prey in
the diet and availability for one taxon, the resulting Jacob’s
index does not represent real preference or avoidance of
the prey. We therefore only calculated Jacob’s indices for
data showing more than one prey individual in the diet and
in prey availability per field session and per habitat, i.e.
above a threshold of eight individuals (in the diet and in
prey availability) belonging to the given taxon per month.
A Kruskal–Wallis test was also performed to test the
significance of the difference (p < 0.05) in mean diet
between stations, and a global linearised model (GLM)
from gamma family, with the season and the taxon as fixed
factors, was used to look for a difference in the diet between
seasons. Normality was tested using a chi-square test, and
homoscedasticity was tested with a Fisher–Snedecor test.
Results
Composition of the Algerian hedgehog’s diet
Analysis of Algerian hedgehog faeces did not reveal any
significant difference in the distribution of prey between
the four sites (Kruskal–Wallis test: N = 16, H(3) = 0.45,
p = 0.930; Table 1). The highest variations in invertebrates
between habitats were found for Oligochatea, with a
negligible variation ranging from 1.9% to 4.2%. Occurrence
was very low for all vertebrates, with a maximum of two
individuals per class per habitat, so using frequency
differences were meaningless. For all prey, the inter-habitat
differences observed in the frequencies of any given taxon
were insignificant compared with inter-taxa differences.
We therefore pooled the values of the four sites for further
comparisons. The majority of the results presented here do
not represent vertebrates, because they were extremely
scarce in the diet and their availability as a source of food
was not evaluated.
Insects were the dominant class of prey (91.8%) and
made up the bulk of the diet of the Algerian hedgehog
(Table 2). They were followed by annelids (Oligochaeta:
earthworms) with much lower rates (3.2%) and
crustaceans, gastropods, myriapods and arachnids, which
all showed very low rates (between 0.9% and 2.0%) and a
richness that did not exceed nine species (Table 2).
Given that insects were amply represented in hedgehog
faeces with 12 752 of the 13 899 items, we further investi-
gated their occurrence at the order level. Hymenoptera
and Coleoptera were the most commonly found orders,
followed by Lepidoptera (Table 2). It should be noted that
all Lepidoptera prey were consumed as larvae.
During the study, 196 prey species were identified in
the faeces, of which 168 were insects (Table 2). Among
Table 1: Prey of the Algerian hedgehog Atelerix algirus in four different habitats of the Soummam Valley, Algeria. Proportion of prey from
different classes (percentage of the number of prey in the given habitat), number of prey, richness (number of species) and diversity (with
Shannon–Weaver index and equitability) of prey species found in hedgehog faeces
Class Cropland Grassland Woodland stream Forest edge
Insecta 93.50 92.55 90.14 90.43
Oligochaeta 1.89 2.62 4.64 4.16
Crustacea 1.59 1.99 2.16 2.27
Gastropoda 1.14 1.12 1.41 0.80
Myriapoda 0.89 0.72 0.86 1.36
Arachnida 0.94 0.87 0.76 0.91
Reptilia 0.02 0.06 0.00 0.05
Aves 0.02 0.06 0.00 0.03
Mammalia 0.00 0.00 0.03 0.00
Number of prey 4 028 3 209 2 910 3 752
Richness (S) 182 175 167 159
Shannon–Weaver diversity index 3.10 2.95 3.05 3.19
Equitability 0.45 0.43 0.46 0.50
Mouhoub-Sayah, Djoudad-Kadji, Kletty, Malan, Robin, Saboureau and Habold
4
insects, the highest total richness (S) was observed
in Coleoptera (100 species), Orthoptera (26 species),
Hymenoptera (19 species) and Heteroptera (13 species).
The Formicidae family was predominant in Hymenoptera,
the order with the highest number of consumed individuals.
A total of 14 Formicidae species were recorded, of which
the Harvester ant Messor barbarus was the most abundant
(46.5% of the items), followed by Camponotus sp. (5.4%)
and Crematogaster scutellaris (2.2%). Twenty-six families
belonging to the Coleoptera order were identified, mainly
Cetoniidae, Tenebrionidae and Silphidae (3.6%, 2.1%
and 1.9% of the items, respectively). The most common
Coleoptera species consumed by the hedgehog were
Silpha granulata (Silphidae, 1.8%) and Aethiessa sp.
(Cetoniidae, 1.4%).
Seasonal variations in the diet of the Algerian
hedgehog
Shannon–Weaver (H′) and equitability (E) indices showed
that diversity in the hedgehogs’ diet was greatest in May
and generally decreased from spring to autumn (Figure 1).
The equitability index reflects a balanced consumption
of different prey species in spring (E close to 1), whereas
some species seem to be more frequently consumed than
others during summer and autumn (E closer to 0; Figure 1).
The Algerian hedgehog’s diet was significantly affected by
seasons (Figure 2a; GLM F = 3.47, p < 0.001). In summer,
the diet of the Algerian hedgehog consisted mainly of
Hymenoptera at the rate of 85.7%, whereas markedly less of
these insects were consumed throughout autumn and winter
(Table 2, Figure 2a). Coleoptera, the second most consumed
prey of hedgehogs, were eaten throughout the year, but
were consumed at higher rates in winter and spring, as
also observed for Orthoptera and Dermaptera. Heteroptera,
Gastropoda, Crustacea and Myriapoda appeared mostly in
the winter faecal samples, whereas a high occurrence of
Lepidoptera and Oligochaeta was observed in the diet of
hedgehogs during autumn (Table 2, Figure 2a).
Analysis of niche overlap of the diet showed that
hedgehogs’ diet in autumn was different from other seasons,
because overlap values with winter, spring and summer
were quite low (Figure 3a). The monthly analysis showed
that this difference resulted from a peculiarity in the diet in
November, because the overlaps of this month with other
months were all relatively small (Supplementary Figure S1).
Food availability in the habitat of the Algerian hedgehog
On an annual basis, the highest food availability was
found in Insecta (88.0% of the items collected), followed
by Crustacea, Oligochaeta, Arachnida, Gastropoda and
Myriapoda (Table 3). Among insects, the most frequently
captured species belonged to Hymenoptera and Coleoptera,
with other orders representing less than 5% of prey.
Table 2: Annual and seasonal distribution of prey in the faeces of the Algerian hedgehog Atelerix algirus. Annual number of individuals (n),
annual richness (S), and annual and seasonal relative abundance (%) of prey groups (classes and insect orders)
Class/Order Annual Seasonal (%)
n S % Winter Spring Summer Autumn
Arachnida 122 7 0.88 0.21 0.93 1.28 0.25
Crustacea 276 2 1.99 8.11 2 0.3 3.1
Gastropoda 153 9 1.1 4.83 1.85 0.65
Insecta 12 752 168 91.75 77 92.38 98.01 83.64
Blattoptera 46 2 0.33 0.72 0.21 0.48 0.11
Coleoptera 1 673 100 12.04 15.5 19.98 6.8 7.39
Dermaptera 559 2 4.02 10.27 5.36 1.7 4.04
Diptera 19 3 0.14 0.35
Heteroptera 156 13 1.12 3.49 1.77 0.56 0.29
Hymenoptera 9 057 19 65.16 40.25 60.58 85.71 41.78
Lepidoptera 863 3 6.21 1.13 0.32 0.46 29.27
Orthoptera 379 26 2.73 5.65 4.16 1.95 0.76
Myriapoda 135 6 0.97 4.41 1.33 0.37 0.32
Oligochaeta 451 1 3.24 5.24 1.39 – 12.04
Aves 2 1 0.03 0.04
Mammalia 1 1 0.01 0.02
Reptilia 7 1 0.04 0.21 0.06 0.04
TOTAL number 13 899 196 974 4 754 5 397 2 774
Figure 1: Monthly diversity of prey species found in the diet of the
Algerian hedgehog Atelerix algirus, represented by the Shannon–
Weaver index and equitability measure
1
2
3
4
0.25
0.50
0.75
1.00
March
April
May
June
July
August
September
October
November
Shannon−Weaver
MONTH
SHANNON–WEAVER INDEX
EQUITABILITY
Equitability
African Zoology 2018, 53(1): 1–10 5
Seasonal variations in food availability were observed
(Table 3, Figure 2b). In summer and autumn, Hymenoptera
were the most available prey. In winter and spring, this
order was still the most strongly represented, but was found
at lower frequencies, whereas an increase was recorded in
the presence of Coleoptera and Orthoptera. Other insect
species remained at low and constant levels throughout the
year. Oligocheta were almost nonexistent during summer,
but their availability was higher during spring and autumn,
with the highest levels being recorded during winter. The
overlap of food availability between seasons was generally
large, ranging from 0.891 for spring–summer to 0.990 for
summer–autumn (Figure 3b).
Food preferences of the Algerian hedgehog throughout
the year
Hedgehogs’ diet and food availability were closely linked
throughout the year because the measure of annual niche
breadth was high (Figure 4). The season analyses also
showed high breadth measures, but links between diet
and food availability were weaker in autumn than summer
because confidence intervals of these seasons were
significantly different, whereas winter and spring showed
intermediate indices (Figure 4).
At the taxon level, hedgehogs preferred certain types of
prey, as shown by Jacobs’ preference indices. Dermaptera
were generally preferred, whereas Arachnida and Diptera
were avoided and Coleoptera were neither particularly
preferred nor avoided (Figure 5). In addition, seasonal
variations in prey type preference were also observed.
Hedgehogs preferred Hymenoptera in spring and summer,
but avoided eating them in winter and autumn. The
preference for Insecta was high in summer, but was not
observed in winter and autumn. The highest Jacobs’
preference index was found for Lepidoptera in autumn
(0.81), but these insects were not selected in winter and
summer and were strongly avoided in spring (−0.87). The
same pattern was observed for Oligocheta, although no
Arachnida
Crustacea
Gasteropoda
Myriapoda
Oligochaeta
Blattoptera
Coleoptera
Dermaptera
Diptera
Heteroptera
Hymenoptera
Lepidoptera
Orthoptera
Podurata
Thysanourata
Winter
Spring
Summer
Autumn
10
20
30
40
50
60
70
80
10
20
30
40
50
60
70
(a)
(b)
FREQUENCY IN FAECES (%)
FREQUENCY IN HABITAT (%)
CLASS/ORDER
Figure 2: Seasonal variation in the frequencies of the different prey groups (classes, and orders for insects) found in the faeces (a) and
habitat (b) of the Algerian hedgehog Atelerix algirus in the Soummam Valley, Algeria
Mouhoub-Sayah, Djoudad-Kadji, Kletty, Malan, Robin, Saboureau and Habold
6
data were available for the summer period. Hedgehogs
consumed Crustacea in autumn and especially in winter,
but avoided this class of prey in summer. The monthly
analysis of prey preference indicated that a strong decrease
in preference for Dermaptera and Coleoptera occurred over
October and November (Supplementary Figure S2). This
decrease was not highlighted in the seasonal analysis,
where October and November were included in the autumn
data set. Likewise, monthly changes were also observed
in preference levels for Dermaptera, where the preference
index was high from March to May, null from June to August,
then returned to high levels in September and October
before falling in November (Supplementary Figure S2).
Discussion
This study identified 196 different species in the Algerian
hedgehog’s diet. These were almost exclusively
invertebrates and mostly insects, with Hymenoptera
constituting the majority of the diet. Prey taxa were not
equally represented within the diet, and variations occurred
between seasons. This can be explained by variations in
food availability, because there is a concordance between
prey availability and prey in the diet. However, our data
also reveal the selection of certain prey by the Algerian
hedgehog, which varies its prey selection throughout
the year. As an example, Hymenoptera seemed to be
particularly sought after in spring and summer but not in
autumn, when hedgehogs preferred other groups such as
Lepidoptera or Oligochaeta.
Diet of the Algerian hedgehog – comparison with other
hedgehog species and between ecosystems
This study of Algerian hedgehogs’ diet in four different
habitats of the Soummam Valley in Algeria showed
very high prey richness compared with the European
hedgehog’s diet (Erinaceus europaeus; S = 77; Yalden
0.916 0.928
0.715
0.793
0.753
0.787
0.984
0.891
0.99
0.967
0.929 0.93
FOOD AVAILABILITY OVERLAP
Winter−spring
Spring−summer
Summer−autumn
Autumn−winter
Winter−summer
Spring−autumn
0.7
0.8
0.9
0.7
0.8
0.9
INTER−SEASON COMPARISON
DIETARY OVERLAP
(a)
(b)
Figure 3: Overlap between seasons for the diet of the Algerian
hedgehog Atelerix algirus (a) and for food availability (b), computed
using Morisita’s original index. Wide overlaps indicate that the
niches of the two seasons compared are similar
Table 3: Distribution of the different invertebrate classes and insect orders collected in the agricultural areas of the Soummam Valley,
Algeria, from March to November (annual: number of individuals collected [n], percentage of the annual total) and according to seasons
(percentage of the seasonal total)
Class/Order Annual Seasonal (%)
n% Winter Spring Summer Autumn
Arachnida 224 2.74 2.98 2.49 3.20 1.98
Crustacea 321 3.93 1.65 2.65 6.07 1.91
Gastropoda 86 1.05 3.64 1.90 0.17 0.68
Insecta 7 179 87.95 79.83 87.07 89.49 89.02
Blattoptera 20 0.25 0.00 0.00 0.56 0.00
Coleoptera 746 9.14 11.24 15.22 5.08 7.63
Dermaptera 100 1.23 1.65 1.03 0.98 1.98
Diptera 208 2.55 1.65 4.82 1.66 1.16
Heteroptera 210 2.57 2.15 4.78 1.85 0.68
Hymenoptera 5 210 63.82 53.72 47.87 74.84 68.78
Lepidoptera 220 2.70 2.48 4.39 0.93 4.16
Orthoptera 341 4.18 6.94 6.28 2.11 4.43
Podurata 39 0.48 0.00 0.55 0.62 0.20
Thysanourata 85 1.04 0.00 2.13 0.87 0.00
Myriapoda 68 0.83 1.82 0.87 0.79 0.48
Oligochaeta 285 3.49 10.08 5.02 0.28 5.93
Total number 8 163 605 2 530 3 561 1 467
African Zoology 2018, 53(1): 1–10 7
1976) and is also high compared with values found in
populations of the same species living in other locations
(59 < S < 167; e.g. Doumandji and Doumandji 1992;
Metref 1994). As observed previously (e.g. Doumandji
and Doumandji 1992), the vast majority of prey were
insects and Oligochaeta. Some other classes, such as
crustaceans, gastropods, myriapods and arachnids, were
also frequently encountered, whereas reptiles, birds and
mammals were relatively rare.
Among insects, the most consumed prey of the Algerian
hedgehog in the Soummam Valley was Hymenoptera,
representing approximately two-thirds of the items
consumed during the active period (from March to
November). This proportion can even exceed 75% in
habitats that are particularly rich in Hymenoptera (Doumandji
and Doumandji 1992; Sayah 1996). Hymenoptera represent
over 80% of the diet of the desert hedgehog Paraechinus
aethiopicus (Rahmani 1999). In contrast, consumption of
Hymenoptera by the Algerian hedgehog was very low at high
altitudes (about 2%; Bendjoudi 1995). The predominance of
Hymenoptera in the diet of hedgehogs could be explained
by the prevalence of this order in different habitats,
because Hymenoptera are diverse and abundant in many
locations around the world (Gibb et al. 2017). It could also
be explained by the strong social behaviour observed in the
Formicidae family (Schultz 2000). As shown in the present
study, the main prey species of the Algerian hedgehog is
the Harvester ant Messor barbarous. This ant species can
severely damage crops, decreasing the total cereal harvest
by up to 10% (Bernard 1968). By consuming insects and
especially harvester ants, the Algerian hedgehog may
play a role in controlling pest species in agricultural areas,
as claimed by local farmers (CM-S pers. obs.), but further
studies are needed.
The second most frequently consumed prey of the
Algerian hedgehog in the Soummam Valley were
Coleoptera (this study: 12%; Talmat 2002). Similar to other
studies (Agrane 2001; Baouane 2005), the highest richness
in prey species was observed in this order (100 species),
whereas only 19 Hymenoptera species were identified.
Coleoptera species belonged mainly to the Cetoniidae,
Tenebrionidae, Silphidae and Scarabaeidae families, which
were also the most frequently found families in our traps.
In other regions of Algeria, remains of other families were
found more frequently in hedgehog faeces (Carabidae:
Doumandji and Doumandji 1992; Staphylinidae and
Curculionidae: Agrane 2001). The European hedgehog
also consumes varying proportions of Coleoptera species
0.933
0.923
0.962
0.899
0.97
SEASON
Winter Spring Summer Autumn Ye ar
0.850
0.900
0.950
SMITH'S INDEX
0.925
0.975
0.875
SEASON
Winter Spring Summer Autumn
−1.0
−0.5
0.0
0.5
1.0
−1.0
−0.5
0.0
0.5
1.0
JACOBS' PREFERENCE INDEX
Arachnida
Crustacea
Gasteropoda
Insecta
Myriapoda
Oligochaeta
Blattoptera
Coleoptera
Dermaptera
Diptera
Heteroptera
Hymenoptera
Lepidoptera
Orthoptera
Podurata
Thysanourata
(a)
(b)
Figure 4: Dietary niche breadth of the Algerian hedgehog Atelerix
algirus indicated by Smith’s index, and 95% confidence intervals,
for seasons and for the whole year. Smith’s index takes food
availability into account in the niche breadth measure. High niche
breadth indicates that the diet is closely linked to food availability
Figure 5: Variation in dietary preference of the Algerian hedgehog
Atelerix algirus over seasons for prey classes (a) and insect orders
(b), computed with Jacobs’ index. Values close to 1 indicate a
strong preference for the prey, those close to −1 indicate a strong
avoidance, and those close to 0 indicate an absence of preference
or avoidance
Mouhoub-Sayah, Djoudad-Kadji, Kletty, Malan, Robin, Saboureau and Habold
8
from the Carabidae and Scarabaeidae families in Europe
(Yalden 1976; Castaing 1982).
The use of faecal analysis methods to evaluate the
diet of a predator provides non-invasive and relatively
easy sampling techniques that allow large sample sizes
(Cavallini and Volpi 1995; Zabala and Zuberogoitia
2003). The most challenging aspect of this method is the
difficulty of assessing how much of the diet each type of
prey represents (Reynolds and Aebischer 1991; Klare et
al. 2011). This is less problematic when studying Algerian
hedgehogs because their diet is mostly composed of
invertebrates, whose cuticle remains partially undigested,
allowing specific body parts to be counted. The present
study evaluates the significance of a prey group for the
Algerian hedgehog by evaluating the frequency of prey
occurrence in the diet. However, other methods such
as volumetrics can also be used, and could provide
complementary information about the hedgehog’s diet
(Ciucci et al. 1996; Zabala and Zuberogoitia 2003).
Seasonal diet variations and link with food availability
During the year of the study, measures of equitability and
dietary overlaps revealed a progressive change in the diet
composition of Algerian hedgehogs from winter to summer,
followed by a shift in autumn, with a marked change
in November.
The Algerian hedgehog appeared to be primarily a
generalist (sensu Revilla and Palomares 2002). Other
predatory mammals living in similar habitats are also
generalist with seasonal variations and a predominance
of certain prey in their diet (European hedgehog: Brockie
1959, Jones et al. 2005; European badger: Roper 1994).
The high number of prey species (196 in the present
study) in the Algerian hedgehog’s diet indicates that this
species has many trophic connexions with other species
of the ecosystem. This and its mainly generalist feeding
behaviour suggest that it should be able to alter its diet
according to prey availability and adapt to changes
in its habitat.
Food selection
Despite its mainly generalist behaviour, the Algerian
hedgehog selects certain prey species, as shown by differ-
ences in seasonal overlap between food availability and
consumption, and Jacobs’ indices distant from 0. Such
prey selection has also already been observed in captive
European hedgehogs (Dimelow 1963) and in wild common
shrew Sorex araneus, two species that rely little on prey
availability (Churchfield 1982). In our study, the variation
observed across seasons did not result from stochastic
variations, but rather came from coherent changes
from one month to the next, i.e. not confused points but
interpretable patterns of the curves. A real shift appeared
in the diet in autumn, and specifically in November,
with Algerian hedgehogs relying progressively less on
Hymenoptera, the most available food, but more on other
prey such as Lepidoptera, Oligochaeta or Crustacea.
Similar results were found in European hedgehogs, which
consumed more Lepidoptera larvae prior to hibernation
in New Zealand (Brockie 1959). Given that food quality
may be more important for animals than food abundance
(Begon et al. 2005), the shift observed in the diet and
the selection of prey before hibernation suggests specific
nutritional requirements during this period to accumulate
body reserves for hibernation. Hibernation is a succession
of bouts of multi-day torpor interspersed with periods of
euthermia. During torpor, hibernating mammals reduce
their metabolism and body temperature and many physio-
logical functions cease (Heldmaier et al. 2004; Ruf and
Geiser 2014). Even if energy requirements during hiberna-
tion are low, hibernators fast throughout this period and
rely on large fat stores (Geiser 1990; Florant et al. 1993;
Geiser et al. 1994). We could not assess the quality of the
prey consumed by the hedgehogs in the present study.
However, we know that Oligochaeta provide high levels
of energy (CM-S unpublished data), and that Lumbricidae
are also particularly rich in proteins (Sabine 1983;
Granval et al. 1988).
Conclusion
In view of the wide variety of prey it consumed, we
considered the Algerian hedgehog to be a generalist
species. However, this species selected certain prey, and
this selection varied throughout the year. Although further
studies are required to confirm our hypothesis, this prey
selection is particularly evident before hibernation, and
suggests that the Algerian hedgehog may depend on
the presence of particularly nutritionally rich prey during
this period. In this case, the protection of the habitat and
thus populations of specific prey species are necessary
to ensure its survival. This mammal species is indeed
subjected to various anthropic pressures, such as road
mortalities (Mouhoub-Sayah et al. 2009), poaching and
the destruction of its habitat. All of these threats could
ultimately lead to its decline, as already observed for other
mammalian species living in ecosystems with a strong
human impact (Tissier et al. 2016).
Acknowledgement — We are grateful to the two anonymous
reviewers for their comments, especially advice on specific data
analysis, which greatly improved the manuscript.
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Received 15 July 2016, revised 11 December 2017, accepted 15 December 2017
Associate Editor: Nico Avenant
... No hay datos disponibles sobre el tamaño poblacional ni la tendencia demográfica de esta especie (Amori et al., 2008;Mouhoub-Sayah et al. 2018). En España, se considera abundante en las Islas Baleares y Ceuta y poco abundante en la península ibérica (Alcover, 2007). ...
... Apenas hay datos íbero-baleares o canarios sobre la dieta en España. Información más detallada hay sobre la dieta de la especie en el norte de África, donde el consumo de hormigas (Hymenoptera) es mayoritario, aunque hay algunas variaciones estacionales (Doumandji y Doumandji 1992;Sayah, 1996;Ouarab y Doumandji, 2010;Djennoune et al. 2018;Mouhoub-Sayah et al., 2018). ...
... La comparación entre disponibilidad de presas y dieta mostró que ambas estaban ligadas en verano, pero menos en otoño. Las hormigas fueron preferidas en primavera y verano, pero en otoño mostró preferencia por lepidópteros y oligoquetos (Mouhoub-Sayah et al., 2018). ...
... By selectively harvesting seeds, ants can depress common plant species, thereby increasing community diversity (e.g., Nicolai and Boeken 2012). Harvester ants have a variety of direct trophic interactions with other animals including preying on other arthropods (e.g., Whitford 1978, Whitford andJackson 2007), being preyed upon by insectivores (e.g., McIntyre 2003, Hojati et al. 2014, Sullivan et al. 2014, Mouhoub-Sayah et al. 2018) and stinging to defend nests against seed-eating vertebrates (Wiernasz et al. 2014). Below we summarize the ecological effects of harvester ants to highlight the various roles they play within their ecosystems. ...
... Pogonomyrmex occidentalis (Cresson) is an important prey item for the endangered sage-grouse (Centrocercus urophasianus, Carlisle et al. 2017). Messor and Veromessor are common in the diets of many vertebrate insectivores (e.g., hedgehogs (Atelerix algirus) Mouhoub-Sayah et al. 2018, geckos (Teratoscincus bedriagai) Hojati et al. 2014. Promoting a healthy population of harvester ants is also considered conservation goals for increasing populations of some threatened insectivorous species such as horned lizards (McIntyre 2003, Sullivan et al. 2014. ...
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... As a typical urban adapter, the Algerian hedgehog is an excellent tool for monitoring the health status of ecosystems (Boukheroufa et al., 2015), especially as the species tends to become increasingly urbanized, because of the significant fragmentation of its natural habitats (Boukheroufa, 2017). In Algeria, the Algerian Hedgehog was particularly studies in these last years Boukheroufa et al., 2015;Khaldi et al., 2016;Mouhoub-Sayah et al., 2018;Guerzouetal.,2019;Senaoui et al.,2020). Even if Atelerix algirusis protected by the Algerian low (text appearing on 10 June 2012 in the 35 edition of the Official Journal of the Algerian Republic) in Boukheroufa (2017), the species is increasingly confronted with negative anthropogenic actions (fragmentation of habitats, intensive agriculture, urbanization... ) Madoui et al., 2014., Boukheroufa, 2017Senaoui et al., 2020;Senaoui, 2021). ...
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We conducted this study to identify the preferred habitat of Atelerix algirus in the National Park of El Kala (PNEK), through the analysis of the catches rates of the species combined to an ethno zoological survey carried out among the residents. The study was conducted between January 2010 and December 2011, in five localities of the Park, different by their useful areas (forests and agricultural land) and their degree of urbanization: Raml Souk, El Aioun, Berrihane, El Kala and Bougous. We also surveyed 57 residents of Berrihane locality. Our results identified the locality of Berrihane as the preferred area of life for the species within the PNEK. This area, which has the highest abundance, is rather semi-urban and as much forest as agricultural, meeting the different needs of the species in terms of survival, sustainability and reproduction. This study provided fundamental data on the bio-ecology of this urban adapt species in Mediterranean environments.
... Regarding the pathogens found in this study, the finding of Salmonella sp. in exotic animals of Spain is not unusual, as in 2013 it was found in free-living turtles of Eastern Spain, with a prevalence of 11% (9), although this is the first time this bacterial genus is found in A. algirus. The high prevalence of Salmonella and Campylobacter species in A. algirus may be due to the fact that this hedgehog species is mainly an insectivore, although its diet may vary according to availability and weather conditions (10), and some studies have shown that insects can act as carriers of Salmonella and Campylobacter species (11). The high prevalence of both bacteria found in this study compared to other wildlife species may imply that insects of the Canary Islands are probably carriers of these pathogens and A. algirus feeding habits facilitates their infection. ...
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Atelerix algirus is an invasive species in the Canary Islands (Spain). There are few studies about the zoonotic pathogens this species could be hosting; therefore, this study was focused on analyzing causative agents of diarrhea in humans in feces from hedgehogs. A total of 45 fecal samples obtained in Tenerife (Canary Islands) were analyzed in this study using Biofire FilmArray gastrointestinal panel with an integrated Biofire FilmArray system. Forty-two (93.33%) of the samples presented at least one of the pathogens detected by the panel. The prevalence of four bacteria stands out as for enteropathogenic Escherichia coli (71.11%), Salmonella (66.67%), Clostridioides difficile (33.33%), and Campylobacter sp. (22.22%), all of which were widely distributed along Tenerife. Besides, other pathogens were found, Cryptosporidium sp. and enterotoxigenic E. coli lt/st in 6.66% of the animals, Shigella/enteroinvasive E. coli in 4.44%, and Norovirus GI/GII, Plesiomonas shigelloides, and Vibrio sp. in 2.22%. Of the hedgehogs, 26.66% were hosting just one pathogen, and the others showed coinfection: 24.44% hosted two, 31.11% hosted three, and 11.11% hosted four or more. The close contact with hedgehogs may imply the transmission of not only one causative agent of diarrhea but also multiple agents, since coinfection is highly prevalent. The lack of management measurements for this animal in the Canary Islands, the common habit of adopting hedgehogs from wildlife without veterinary control, and the fact that most of the hedgehogs studied belonged to highly populated areas imply a high risk of transmission of pathogens to humans.
... Atelerix algirus, geographical distribution, North African mammals, Paraechinus aethiopicus, Tunisia F I G U R E 1 Examples of sampling sites representing different habitat types available in Tunisia: (a) Mediterranean evergreen forest, (b) dry forest, (c) agriculture land, (d) pre-Saharan upland steppe, (e) arid mountainous, (f) oasis, (g) Chott desert and (h) Saharan desert studied two Erinaceidae species which occur in Tunisia because there is a need to update the distribution of these small mammals for better protection in the future. Despite some work mainly in Algeria like Chemkhi et al. (2015), Hosni and El-Maghrbi (2014), Sakraoui, Boukheroufa, Sakraoui, and Madoui (2014) and Khaldi et al. (2011) on parasites, Djennoune, Marniche, Amroun, and Boulay (2018), Mouhoub-Sayah et al. (2018) on their feeding and Sayah et al. (2009) on road mortality, no study talks of the biogeography and bioclimatic niche of the North African Erinaceidae species. Hutterer (2015) and Amori et al. (2008) have noted the scarcity of research and the lack of protection measures of these taxa. ...
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