Keywords:

Orchards

Ficus carica

Bark beetles

Hypocryphalus scabricollis

Algeria

Fig tree xylophagous pest’s eects in the Bejaia region (central-north Algeria)

Efectos de la plaga xilófaga de la higuera en la región de Bejaia (Argelia centro-norte)

Efeitos da praga xilófaga da gueira na região de Bejaia (centro-norte da Ar

gélia)

Abdelmadjid Chelli

Aldjia Oudjiane

Rabah Zebsa

Sabah Razi

Fariza Boussad

Soane Boudalia

Rev. Fac. Agron. (LUZ). 2022, 40(2): e234022

ISSN 2477-9407

DOI: https://doi.org/10.47280/RevFacAgron(LUZ).v40.n2.12

Crop Production

Associate editor: Dra. Lilia Urdaneta

University of Zulia, Faculty of Agronomy

Bolivarian Republic of Venezuela

Laboratoire de Zoologie Appliquée et d’Ecophysiologie

Animale, Faculté des Sciences de la Nature et de la Vie,

Université de Bejaia, Algeria.

Institut National de la Recherche Agronomique de Oued

Ghir Bejaia, Algéria.

Laboratoire de Biologie, Eau et Environnement, Faculté des

Sciences de la Nature et de la Vie et Sciences de la Terre et

de l’Univers, Université 8 Mai 1945 Guelma, P.O. Box 4010,

Guelma 24000, Algeria.

Université Mohamed Khider de Biskra (Algéria).

Institut National de la Recherche Agronomique d’Alger

(Algéria).

Received: 26-02-2023

Accepted: 05-05-2023

Published: 10-06-2023

Abstract

In response to alerts from farmers in Bejaia region (central-north Algeria)

about the decline of their g trees, a survey was conducted between 2019 and

2021 in the main localities known for g crops. Hypocryphalus scabricollis

(Eichho) (Coleoptera, Curculionidae: Scolytinae) was identied as the

causal agent of g tree decline in the region. This species is reported for the

rst time in Algeria. Here, a morphological description and main biological

traits of this species are given. Distribution of H. scabricollis in the Bejaia

region is illustred, and an overview of its behaviour, symptoms and damage

caused to the host plant, and their potential impact in commercial g

production is discussed. This work aims to provide a preliminary database to

the scientic community about this xylophagous pest of g trees and to alert

regional and national policy makers to take it seriously and address emerging

bark beetle problems before it is too late.

This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.

Rev. Fac. Agron. (LUZ). 2023, 40(2): e234022. April-June. ISSN 2477-9407.2-6 |

Resumen

En respuesta a las alertas de los agricultores de la región de

Bejaia (centro-norte de Argelia) sobre el declive de sus higueras, se

realizó una encuesta entre 2019 y 2021 en las principales localidades

conocidas por los cultivos de higuera. Hypocryphalus scabricollis

(Eichho) (Coleoptera, Curculionidae: Scolytinae) fue identicado

como el agente causal del declive de la higuera en la región. Esta

especie se reporta por primera vez en Argelia. Aquí se describe la

morfología y principales rasgos biológicos de esta especie. Se

ilustra la distribución de H. scabricollis en la región de Bejaia y se

analiza una descripción general de su comportamiento, síntomas y

daños causados a la planta hospedera, y su impacto potencial en la

producción comercial de higos. Este trabajo tiene como objetivo

proporcionar una base de datos preliminar a la comunidad cientíca

sobre esta plaga xilófaga de las higueras y alertar a los responsables

políticos regionales y nacionales para que la tomen en serio y aborden

los problemas emergentes del escarabajo de la corteza antes de que

sea demasiado tarde.

Palabras clave: huertos, Ficus carica, escarabajos de corteza,

Hypocryphalus scabricollis, Argelia.

Resumo

Em resposta aos alertas dos agricultores da região de Bejaia

(centro-norte da Argélia) sobre o declínio das suas gueiras,

foi realizado um levantamento entre 2019 e 2021 nas principais

localidades conhecidas pela cultura do go. Hypocryphalus

scabricollis (Eichho) (Coleoptera, Curculionidae: Scolytinae) foi

identicado como o agente causal do declínio da gueira na região.

Esta espécie é relatada pela primeira vez na Argélia. Aqui, uma

descrição morfológica e principais características biológicas desta

espécie são dadas. A distribuição de H. scabricollis na região de

Bejaia é ilustrada, e uma visão geral do seu comportamento, sintomas

e danos causados à planta hospedeira, e seu potencial impacto na

produção comercial de gos é discutida. Este trabalho visa fornecer

um banco de dados preliminar para a comunidade cientíca sobre

esta praga xilófaga das gueiras e alertar os formuladores de políticas

regionais e nacionais para levá-la a sério e abordar os problemas

emergentes do besouro da casca antes que seja tarde demais.

Palavras-chave: Pomares, Ficus carica, besouros de casca,

Hypocryphalus scabricollis, Argélia.

Introduction

The g tree (Ficus carica L.) is a globally important crop that has

been cultivated for at least 11,000 years originated in the Middle East

(Cutajar and Mifsud, 2017), and is well-adapted to the Mediterranean

climate. In Algeria, the vast majority of plantations are located in

the Kabylia region which represents 40 % of the national g orchard

(Chouaki et al., 2006), including the provinces of Béjaia (13352 ha)

and Tizi-Ouzou (6387 ha). The g fruit was one of the staple foods

and a source of income for the majority of farming families in the

region.

Fig trees host more than thirty insect pests and diseases (Cutajar

and Mifsud, 2017), and in the last few years, Mediterranean regions

have been invaded by alien wood-boring bark beetles (Family

Scolytinae) (Kirkendall and Faccoli, 2010; Rassati et al., 2016).

Bejaia, a region in north-central Algeria, is not safe from this

scourge, and warning signals have been given by farmers and local

associations due to the weakening of g trees. The decline of g tree

plantations in Kabylie is due to a group of xylophagous beetles in

the subfamily Scolytinae (Coleoptera, Curculionidae). The majority

of species belonging to this group attack dead wood, while some of

them can attack living and healthy trees (Kirkendall et al., 2015).

After analyzing samples from dierent orchards on infested trees, it

has been found that the bark beetle, Hypocryphalus scabricollis was

responsible for the dieback.

The bark beetle frequently attacks trees weakened by drought,

disease, injuries, nutritional deciencies, and sun scald (Cutajar

and Mifsud, 2017). It was discovered over a century ago in Burma

and Asia, where it is regarded a harmful organism, and it was just

discovered in Malta in 1991 (Mifsud and Knížek, 2009), in Sicily

in 2014 (Faccoli et al., 2016), in the northeast of Tunisia in 2016

(Gaaliche et al., 2018). It seems that this pest is continuously

expanding its range in the Mediterranean region. Confronted with

the rapid progression of g tree dieback caused by this pest and its

potential socioeconomic implications, we carried out surveys in the

main localities renowned for g production in Bejaia, Algeria. Given

that xylophagous pests of g trees have not been documented yet in

this country, this study represents a timely baseline for future work

on g pests.

Materials and methods

Study area

This investigation was conducted in Bejaia province, situated in

the central north of Algeria, in the Kabylia province (gure 1). It is

located 181 km east of Algiers (36°45′00″N 5°04′00″E), and extends

over an area of 3268 km

. The area is dominated by mountainous

massifs on 75 % of its surface, and the whole region is drained by the

Soummam River (A. S. W. B., 1996). This area is characterized by a

Mediterranean climate, with mild and humid winters alternating with

hot and dry summers. There is a rainy season from October to May,

and a dry season from June to September. It is subject to high water

conditions due to heavy, often irregular rainfall varying annually

between 600 mm and 800 mm (B. N. D. R., 1980).

Figure 1. Study area and surveyed localities of the g killer bark

beetle. Source: own elaboration.

This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.

Chelli et al. Rev. Fac. Agron. (LUZ). 2023 40(2): e2340223-6 |

Sampling methodology

The bark beetle specimens found under the bark of g trees and

plant parts such as stems and branches were collected from six sites

in the Bejaia region. The sites, which ranged in elevation from 35 to

945 meters, were visited over a two-year period, from March 2019 to

April 2021 (table 1).

Table 1. Geographic data of the surveyed sites in Bejaia region.

Sites Localities

Elevation

(m)

Latitude Longitude

Inra Oued Ghir 35 36°42′25″N 4°57′23″E

Igher n’Deni

Benimaouche

620 36°29′56″N 4°46′47″E

Ait Ouamer 945 36°29′12″N 4°44′43″E

Guenana

Kendira

813 36°32′22″N 5°00′46″E

Tibkert 848 36°33′15″N 4°58′23″E

Ait Sidi Ali Berbacha 480 36°60′74″N 4°99′48″E

Source: own elaboration.

Once a month, adults and larval stages collected from infested

trees were stored in 70 % alcohol for further identication. Plant

parts potentially containing eggs were also picked once a month and

placed in plastic bags, then transferred to large plastic boxes (50 x

30 x 40 cm) covered by ne mesh. These samples were deposited

in the laboratory of the National Institute of Agronomic Research

(NIAR) and maintained at an average temperature of 20 °C and

relative humidity of ~70 %, which will allow the larvae, nymphs, and

immatures present in the wood to reach the adult stage and emerge.

Morphological examination of adult bark beetle specimens

observed was carried out using a binocular magnifying glass and

relevant identication work was related to bark beetles (Faccoli et

al., 2016; Mifsud and Knížek, 2009). Macro-photography used in this

report was done using a Panasonic Lumix DMC-FZ50 camera. For

the Hypocryphalus scabricollis specimens, a digital camera mounted

on a microscope was used. A total of 30 individuals were deposited at

National Institute of Agronomic Research (NIAR).

External morphological characters were taken from the accurate

descriptions reported by Mifsud and Knížek (2009), Faccoli et al.

(2016) and Cutajar and Mifsud (2017).

Results and discussion

Identication and morphological description

Morphological examination of adult specimens that emerged and

were observed under the bark of trunks and branches of dead and

wilted trees revealed the presence of two dierent bark beetle species

belonging to two tribes and two families of Scolytinae: Hypoborus

cus (Erichson) and Hypocryphalus scabricollis (Eichho). The

former species was already reported on the g tree by Mifsud

and Knížek (2009) along with other species of Scolytinae such as

Liparthrum mori (Aubé) and Hypothenemus leprieuri (Perris). The

latter species, H. scabricollis, is a new record as a g pest in Algeria

(table 2). Both species were found in association with Hypocryphalus

scabricollis under the bark of dead wood in the Beni Maouche

locality (table 2), and also in close association with another species of

Cerambycidae, Trichoferus fasciculatus (Faldermann, 1837) in most

of the surveyed orchards.

Description and identication of the beetle

Proper identication of the main pest causing the damage,

the bark beetle, H. scabricollis, is essential, especially since other

similarly looking bark beetles might be present in the same tree at the

same time (Cutajar and Mifsud, 2017). Females lay small, oval, and

whitish eggs just beneath the outer bark (gure 2A). Hypocryphalus

scabricollis adults are small, hard-bodied, rather squat shape insects

(gure 2D).

Figure 2. Life stages of Hypocryphalus scabricollis on g trees:

(A) Eggs; (B) Larvae; (C) Pupae; (D) Adults. Source: own

elaboration.

Body length is about 2 mm. The colour changes from yellowish

brown (young bark beetle) to dark brown (adult bark beetle). When

viewed from above, the head is partly or completely hidden by

the pronotum. Frons convex, attened above epistoma, strongly

shagreened, nely sparsely punctuate; its eyes are emarginated;

antenna characterised by a 4-segmented funicle and a rounded

antennal club. The pronotum is bicoloured, lighter posteriorly, and

nearly as wide as it is long. The anterior margin of the pronotum is

armed by 5-6 conspicuous and protruding teeth of which the two

central ones are bigger than the others. The elytral surface of H.

scabricollis, instead, is covered with dense but microscopic scalelike

setae and erect sparse hairs. Larvae are whitish (gure 2B), apodous,

robust, arcuate in shape, and may have a dark brown head. Pupae are

o-white and plump (gure 2C). H. scabricollis could be confused

with other bark beetle species such as, Hypoborus cus (Erichson),

where an association with this species is observed in one of the

surveyed localities of the Bejaia region (table 2).

According to Faccoli et al. (2016), H. scabricollis can be

distinguished from other species by the body length, antennae and

pronotum shape. Indeed, H. cus is usually smaller (1-1.3 mm in

length) than H. scabricollis, with a pronotum covered by long,

recumbent, white scale-like setae. Moreover, H. cus has entire eyes,

which are instead emarginated in H. scabricollis. Lastly, in H. cus,

no teeth occur along the anterior margin of the pronotum.

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of adult individuals on dead branches surveyed in March and April

as well as in August and September. The large number of individuals

found in the branches of trees prospected in spring and summer

explains perfectly what was observed in the laboratory. In fact, under

laboratory conditions, we have assisted two major emergences of

adults. The rst emergence of young adults in the plastic boxes began

on the 25th of March and extended to the rst fortnight of April, and

the second one starts around the 20th of August and continues until

the rst week of September. These records indicate that this bark

beetle has more than one generation per year in the Bejaia region.

The spring generation probably occurs in early spring when the

temperatures start warming, allowing mature adults to emerge from

the tree. After emergence, adults may re-infest the same tree or, in

most cases, disperse to attack other new susceptible trees (gure 3B).

After mating, this bark beetle drills a small entrance hole in a branch.

Females dig a gallery and lay eggs just beneath the outer bark. After

hatching eggs, the larvae mine galleries that branch out from the egg-

laying gallery. The last larval stage will end in pupation giving rise

to immature adults, which, after a maturation phase of a few days,

emerge at the end of the summer, forming the autumn generation

(gure 4).

The females of this generation will in turn lay eggs in early

autumn. Thus, the eggs laid will give rise to young larvae that will

develop during this season and probably hibernate in the last larval

stage or as pupae. Nevertheless, some older adults are noted inside the

branches analysed in December, January and February; they seem to

be able to survive the winter and participate in the production of the

spring generation (gure 4).

Host plants and damage importance

In its native area the Asian thermophilous regions, H. scabricollis

appears to be quite polyphagous and has been found in association

with many tropical trees, including Intsia bijuga (Colebr.) Kuntze,

1891(Fabaceae), Madhuca longifolia (L.) J. F. Macbr. (1918)

(Sapotaceae), Bombax malabaricum DC. (1824) (Malvaceae),

Canarium euphyllum Kurz (1872) (Burseraceae), Excoecaria

agallocha L. (1759) (Euphorbiaceae), Ficus elastica Roxb. ex

Hornem., 1819 (Moraceae) (Wood and Bright, 1992). In the

Mediterranean region, it has only been found on plants of the genus

Ficus. In Malta, it was initially recorded from Ficus retusa (Mifsud

and Knížek, 2009); subsequently, it has been mainly found on wild

and cultivated g trees (Mifsud and Knížek, 2009). In Sicily (southern

Italy), this bark beetle has been found on both wild and cultivated

varieties of the common g (Faccoli et al., 2016). However, in the

Maghreb region, in the Mornag area (north-east of Tunisia) (Gaaliche

et al., 2018), and recently in the Bejaia region (north-central Algeria),

it was only found on F. carica. Whether in Malta, Italy, Tunisia or

Algeria, H. scabricollis has only been found on plants of the genus

Ficus. The majority of the orchards studied, H. scabricollis attacks

dead or dying trees, but in other localities, it attacks healthy trees,

causing dieback or mortality. This was observed at the Ait Ouamar

site, one of the orchards in the Beni Maouche locality. When looking

at the g tree from afar, the rst apparent symptom of attack by this

bark beetle is the partial desiccation of some branches, which will

eventually lead to the death of the whole tree (gure 5A).

Table 2. Identication of bark beetle species and the infested

section of g trees in Bejaia region.

Family Sub-family Tribe Species Location

Infested

plant part

CURCULIONIDAE Latreille,

1802

Scolytinae

Latreille,

1804

Hypoborini

Nüsslin,

1911

Hypoborus

cus Erichson,

1836

Benimaouche

(Igher

N’Deni)

Dead

branches and

twigs of Ficus

carica

Scolytinae

Latreille,

1804

Cryphalini

Lindemann,

1876

Hypocryphalus

scabricollis

(Eichho,

1878)

In all

surveyed

localities of

the Bejaia

region

Usually under

the bark of

dead wood of

F. carica, and

often on the

main trunk

and branches

of suering

trees.

Source: own elaboration.

Biology and behaviour

Globally, the life cycle of a bark beetle is organized, in each

generation, around a basic life cycle in 4 phases: reproduction,

development, maturation, and dispersion. Like all other bark beetles,

H. scabricollis spends most of its life under the bark of dead or dying

g trees where it passes through four successive stages: egg, larva,

pupa, and adult (gure 3A).

Figure 3. Illustration of the life cycle of Hypocryphalus scabricollis

(B) and its interaction with the g trees (A) in Bejaia

region, Algeria. Source: own elaboration.

Based on our monthly in-situ observations in the orchard of

the National Institute for Agronomic Research (NIAR) and of the

dierent emergences of adults from the branches placed in the boxes

under laboratory conditions, we can say that H. scabricollis develops

at least two annual generations in the Bejaia region. Indeed, our

various eld surveys have given us an idea of its life cycle. In the

eld, the presence of the species as larvae and adults on dead wood

and dying tree branches is almost always noted throughout the year.

However, we noted the presence of eggs over two distinct periods.

The females seem to lay eggs in May and September. Our monthly

eld observations have also allowed us to note a remarkable presence

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Chelli et al. Rev. Fac. Agron. (LUZ). 2023 40(2): e2340225-6 |

Figure 4. Diagram illustrating the succession of generations of

Hypocryphalus scabricollis on g trees. Source: own

elaboration.

Figure 5. Signs of Hypocryphalus scabricollis attacks on g trees

in the dierent localities of the Bejaia area. Source: own

elaboration.

A closer examination of the branches and trunks of aected trees

reveals numerous small round holes of about 2 mm in diameter (gure

5B). On the branches and at the base of the trunk, the bark cracks and

may peel o in some places (gure 5C). Scraping of the bark at the

entry point shows damage to the tissue just below the bark (gure

5D). By lifting the bark, we can observe adults associated in some

cases with larvae and characteristic gallery patterns if the infestation

is not too recent (gure 5E-H). The proliferation of these galleries

weakens attacked branches or trees, eventually leading to death in

high-pressure situations (gure 5I). Damage initially limited to one

or more branches can spread more or less rapidly to the whole tree

and kill it if there is no rapid intervention. Such harm is caused by

both adults and larvae killing the tissue just under the bark, and the

tree quickly succumbs if the attack is very severe. This conrms the

information reported by Mifsud and Knížek (2009) in Malta, as well

as by Gaaliche et al. (2018) in Tunisia.

No statistics are currently available to calculate the number of

trees aected by this pest. However, in the Béjaia region, during

our eld surveys, we noted the presence of this insect in all the

localities known for g production, and the degree of infestation

varies considerably from place to place, especially depending on the

degree of orchard maintenance and the trees’ physiological condition.

Nevertheless, the orchards of Beni Maouche and those of Kindera are

the most aected by this pest, and mortality rates averaged around

10 %. In contrast, Faccoli et al. (2016) stated that over an eight-year

period, more than 50 % of Maltese island g trees were destroyed by

this bark beetle. According to the testimonies of some farmers in the

Beni Maouche community (Bejaia), this plague has been intensifying

for about three years, and these attacks are undoubtedly linked to

global warming because, in recent years, the North African region

has had a succession of heat waves and hot, dry summers following

abnormally mild winters (Khelifa et al., 2021), which seem to

have favorably inuenced outbreaks of this beetle. Several authors

studying bark beetles associated with certain forest trees observed

and conrmed this pattern, indeed, these current climate changes are

highly susceptible to inuencing plant-insect interactions (Raa et

al., 2008; Rassati et al., 2016), and chronic water stress over long

periods of time due to climate warming is generally the main cause of

observed forest diebacks (Allen et al., 2010; McDowell et al., 2013).

In any case, there seems to be a correlation between drought phases

and attack intensity.

Regional and national decision-makers must take this alarming

situation caused by the emergence of this bark beetle seriously to

avoid scenarios such as the one recorded in Algeria in the 1980s

on Aleppo pine (Pinus halepensis Mill., 1768) (Pinaceae) by the

pine procession caterpillar Traumatocampa pityocampa (Denis &

Schiermüller, 1775) (Notodontidae) (Kadik, 1987). The failure to

manage this problem in due time has favored the pest’s geographic

expansion, leading to large areas of infestation in the early 2000s.

Control means

In general, there are no eective methods or treatments available

to control bark beetles. Control is dicult because the insect spends

most of its life cycle under the bark, sheltered from potential insecticide

treatments. No chemical treatment is currently registered to control

this bark beetle on living trees. Since infested trees cannot usually be

saved, preventive rather than curative control is preferable. Measures

such as avoiding water stress in summer (watering), fertilizing and

amending the soil, or installing pheromone traps to prevent adult

beetles from colonizing healthy trees are promising. Currently, farmers

are advised to quickly fell, remove, and burn the infested trees from

the orchard. In the biological control of Hypocryphalus scabricollis,

research should be focused on the natural enemies, predators, and

parasites associated with this bark beetle, and promising solutions

may emerge from the work of Belokobylskij and Maeto (2009) and

Mifsud et al. (2012). These researchers have identied parasitoid

species from the genus Ecphylus Foerster, 1863 (Braconidae) on bark

beetles. According to Belokobylskij and Maeto (2009), all species of

the genus Ecphylus are larval ectoparasitoids of Scolytinae and rarely

of Bostrichidae and Cerambycidae. However, Mifsud et al. (2012),

identied thirty-ve specimens of Ecphylus caudatus Ruschka, 1916

This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.

Rev. Fac. Agron. (LUZ). 2023, 40(2): e234022. April-June. ISSN 2477-9407.6-6 |

(Hymenoptera: Braconidae: Doryctinae) from dead branches of F.

carica infested with the bark beetle, Hypoborus cus. According to

these authors, it is important to recall that this parasitoid, E. caudatus,

was recorded by Belokobylskij in the Mediterranean basin and in the

Maghreb region, Algeria, Morocco, and Tunisia. This ectoparasite

deserves to be tested on the larvae of H. scabricollis. This approach

may prove successful in the coming years. Finally, various chemical

studies should also be initiated to identify and synthesize the

pheromonal molecules of this species. An attempt will then be made

to use them as a means of detecting and capturing this pest.

Conclusions

The investigation report on the phenomenon of g tree decline

in some localities of the Bejaia region has allowed us to provide

some answers to the distress and expectations of local farmers. The

eld survey revealed that the wilting and dieback of trees are due

to a new xylophagous pest recently introduced in Algeria. This is

Hypocryphalus scabricollis, a bark beetle known in the countries

where it occurs as the “g tree killer”. The eld survey showed that

this new bark beetle prefers to attack old and weakened trees, but

in some cases, young trees are not spared. The damage committed

by this pest in the various g tree plantations is probably the result

of two essential complementary factors: on the one hand, inadequate

management of the orchards; and on the other hand, the existence of

receptive trees, i.e., decreased tree vitality due to water stress caused

by successive droughts, which favours infestation and increases the

degree of tree decline. This new alien bark beetle seems to develop

at least two generations per year in the Bejaia region’s climate: a

spring generation and an autumn generation. In Algeria, if the g

tree is well known botanically, much remains to be done on the

phytosanitary aspect. The problem associated with the emergence

of this bark beetle should be addressed seriously with the intention

of integrated management by the relevant services. Following this

account dedicated to this bark beetle found in Bejaia area. Further

research should be carried out in the coming years to obtain even more

information on its biology and behaviour, and focus on parasitoids

and predators potentially associated with this bark beetle in order to

use them as biological agents for its control.

Acknowledgements

We would like to thank all the people and colleagues the National

Institute of Agricultural Research from who helped us during the

various surveys and eld trips. Finally, we thank Meziane Youcef

president, and the vice-president, Ait Haliali Mohand Zine of the

Figure growers’ association of Sedouk who assisted and oriented us

towards the plantations aected in Beni Maouche area. This research

was supported by Ministry of Higher Education and Scientic

Research (MESRS) Algeria.

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