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Carob pests in the Mediterranean region: bio-ecology, natural enemies and

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Phytoparasitica
https://doi.org/10.1007/s12600-019-00766-7
Carob pests in the Mediterranean region: bio-ecology,
natural enemies and management options
Antonio Gugliuzzo & Gaetana Mazzeo &
Ramzi Mansour & Giovanna Tropea Garzia
Received: 26 July 2019 / Accepted: 28 October 2019
# Springer Nature B.V. 2019
Abstract An overview on the bio-ecology, natural en-
emies and pest contol tools of the main pests infesting
carob tree (Ceratonia siliqua L.), pods and seeds in the
Mediterranean region is provided herein. Most of the
species are occasionally present on host carobs where
they did not cause serious damage. In particular, the
occurrence of mealybugs, soft and armored scales and
also mites is usually sporadic. This is also the case for
dipteran and lepidopteran pests, except for the most
damaging and economic species, the carob moth
Ectomyelois ceratoniae (Zeller), a highly polypha-
gous insect that can infest carob either in open-
field or in storage.
Cause of wounding are bark and wood-boring cole-
opteran insects, which can induce severe wilting and/or
death of carob branches and trunk. The recent introduc-
tion in Europe of two species of Xylosandrus spp.
(X. compactus and X. crassiusculus) is of increasing
importance, due to their proven initial aggressiveness
in Italy. Brief details regarding moth and rodent popu-
lations residing inside the storage buildings are also
emphasized. Obviously, one aspect warranting special
Gaetana Mazzeo and Ramzi Mansour are joint second authors.
A. Gugliuzzo : G. Mazzeo : G. Tropea Garzia
Department of Agriculture, Food and Environment, University of
Catania, Via Santa Sofia 100, 95123 Catania, Italy
R. Mansour (*)
Section of Biological Sciences, Higher Institute for Preparatory
Studies in Biology-Geology (ISEP-BG), University of Carthage, 6
Avenue 13 août, 2036 La Soukra, Tunis, Tunisia
e-mail: ramzi_mansour82@yahoo.co.uk
attention concerns the introduction and rapid spread in
the Mediterranean region of invasive alien insect species
such as some ambrosia beetles.
Keywords Southern Europe . Northern Africa .
Middle East . Invasive insect pest . Bio-ecological
aspects . Carob plant damage
Introduction
The carob tree (Ceratonia siliqua L.), belonging to the
Fabaceae family of the order Fabales, is a long-living
evergreen and thermophilous arboreal species. Probably
native to the eastern Mediterranean region, mainly to
Middle-East countries, this plant has undergone exten-
sive cultivation since ancient time. The area of diffusion
extends from the Iberian Peninsula to Turkey, including
Italian mainland, Israel and North Africa and also some
islands, such as Sicily, Malta and Cyprus (Spina 1986)
(Fig. 1). In other coastal areas of the world, the carob
tree was introduced at the end of the nineteenth century
(Batlle and Tous 1997) (Fig. 2). The plant is of particular
landscape, conservation, and economic importance and
it is characteristic of the olealentisc and carob groups (it
belongs to the alliance Oleo sylvestris-Ceratonion
siliquae Br.-Bl. 1936 emend. Rivas-Martínez 1975)
(Baumel et al. 2018).
Primarily cultivated for its edible pods but at present
also for powder (flour and fiber) and syrop, carob has
also several beneficial characteristics related to human
nutrition and animal feed. Indeed, it is frequently used

for controlling many human health troubles such as
diabetes, heart diseases, and colon cancer (Goulas
et al. 2016; Nasar-Abbas et al. 2016), and it also con-
tribute to reducing cholesterol level (Zunft et al. 2003;
Ruiz-Roso et al. 2010), obesity problems, infantile diar-
rheal disturbance and bacterial dysentery (Loeb et al.
1989; Nasar-Abbas et al. 2016; Theophilou et al. 2017).
Furthermore, carob is worthy of (i) ecological (adapta-
tion to drought, it is satisfied by poor and rock soils, it
can tolerate temperatures below 6 and above 50 °C), (ii)
biological (nitrogen fixation, resistance to fire, mutila-
tions and diseases), (iii) agronomical (higher crop yield
in arid areas in comparison with olive, almond, soft
wheat and barley), (iv) genetic (presence of great genetic
variability), and (v) socio-economical (stable source of
income for the local population, participates in the de-
velopment of national and regional economy) interest
(Sbay 2008). Likewise, the carob tree is able of
preventing soil erosion and strengthening rural area
development in the Mediterranean region and
worldwide.
In the Mediterranean countries, the economic impor-
tance of C. siliqua has increased considerably, due to the
development of carob industry for which carob flour and
seeds have become essential raw materials to be used.
The Food and Agriculture Organization of the United
Nations (FAO) has estimated a world harvested area of
41,996 ha with a total production of 136,540 metric tons
of carob pods (FAOSTAT 2017)*. (*Data refer to the
area from which a crop is gathered. Area harvested,
therefore, excludes the area from which, although sown
or planted, there was no harvest due to damage, failure,
etc.…).
The top five carob-producing countries are located in
the Mediterranean climate area of Europe: Portugal
(41,909 tons annually), Italy (28,910 tons), Morocco
(21,983 tons), Turkey (15,016 tons) and Greece
(12,528 tons). These countries hold 30%, 21%, 16%,
11%, and 9% of the total carob world production, re-
spectively. Other carob-producing countries include
Cyprus, Spain and Algeria.
Traditionally, carob orchards do not receive pes-
ticide sprays because they are generally free from
severe insect pest and disease attacks (Lisan 2012).
The evergreen habit of the carob tree would seem to
be an optimum substrate for leaf-chewing herbivores
but not the foliage that is quite leathery. Some pests
may cause severe damage to the host carob mainly
in the eastern Mediterranean territories representing
Phytoparasitica
the origin of this plant (see the oval areas in Fig. 1),
taking into account that all insects reported to attack
carob are polyphagous. Lepidopteran (butterflies and
moths) and coleopteran (beetles and weevils) species
are the most common insect pests recorded on carob
in almost all Mediterranean countries, while the
majority belong to the Order Hemiptera (more spe-
cifically scale insects) totaling 31 species (Table 1).
Here we explore, summarize and discuss (i) the
main bio-ecological aspects and natural enemies of
carob pests occurring throughout the Mediterranean
region, (ii) the nature of their induced plant damage,
and (iii) the potential pest management approaches
adopted so far against the most damaging species
infesting host carob either in open-field or in storage
conditions.
Scale insects (Hemiptera: Coccoidea)
Scale insects (Fig. 3) are often present in very small
numbers on carob trees, as consequence of both the
effective action of natural enemies and plant resistance
that causes high mortality of the crawlers (Longo and
Tirrò 2005). Thirty-seven polyphagous scale insects
species have been recorded on carob in the world and
among these, thirty-one occur in the Mediterranean
region (Longo and Tirrò 2005; García Morales et al.
2016) (Table 1).
Armored scales (Diaspididae) represent the dominant
group of scale insects. Although many of them are pests
of citrus and other crops, they are not considered as
significant pests of carob. Among these, Aonidiella
aurantii (Maskell), a biparental, ovoviviparous species,
that infests all the aerial parts of the plants, is widespread
all over the world, where it constitutes one of the most
important pests of citrus (García Morales et al. 2016).
Aonidiella aurantii forms abundant colonies on
branches and fruits and causes severe damage due to
the toxicity of the saliva and its high reproductive rate
(Tremblay 1995). It has been recorded on C. siliqua in
Palestine (as considered in Bodenheimer (1924)), Egypt
and Italy (Hall 1922; Bodenheimer 1924; Inserra and
Calabretta 1987). The congeneric Aonidiella orientalis
(Newstead) is widely distributed in tropical and subtrop-
ical regions where it is considered a pest of several
agricultural crops, usually living upon the leaves
(García Morales et al. 2016). This species has been
recorded on carob in Lebanon and Israel (Moghaddam
Phytoparasitica

Fig. 1 Mediterranean distribution of the carob tree and territories of origin (oval areas) (Spina 1986, modified)

2004; Ben-Dov 2012). Aspidiotus nerii Bouché is a
widespread and polyphagous species that has been re-
corded also on carob in many Mediterranean countries,
i.e. Spain, Slovenia, western Mediterranean basin,
Syria, Turkey, Israel, Sicily, and Crete (Greece)
(Bodenheimer 1926, 1952; Balachowsky 1932; Martín
Mateo 1983; Podsiadlo 1983; Seljak 2010; Ben-Dov
2012; García Morales et al. 2016; Guillén et al. 2018).
In Spain the species attacks leaves and fruits of carob
causing damage (Guillén et al. 2018) such as yellowing
and drying out as consequence of the removal of sap
from plants (Tremblay 1995). The Florida red scale,
Chrysomphalus aonidum (Linnaeus), is widely distrib-
uted in many tropical and subtropical regions in North
and South America, Africa, the Mediterranean basin, the
Far East, Pacific Islands and Australia. The species

Fig. 2 World distribution of the carob tree (areas colored in black) (Batlle and Tous 1997)
 Phytoparasitica

Table 1 Carob pest species in the Mediterranean region and their occurrence based on the relevant scientific literature (F = Field; SB =
Stored building)

Order Family Pest species Occurrence

INSECTA
HEMIPTERA Monophlebidae Gueriniella serratulae F
Pseudococcidae Maconellicoccus hirsutus F
Planococcus citri F
Planococcus ficus F
Pseudococcus viburni F
Coccidae Ceroplastes floridensis F
Coccus hesperidum F
Coccus longulus F
Saissetia oleae F
Diaspididae Aonidiella aurantii F
Aonidiella orientalis F
Aspidiotus nerii F
Chrysomphalus aonidum F
Chrysomphalus dictyospermi F
Chrysomphalus pinnulifer F
Diaspidiotus lenticularis F
Diaspidiotus pyri F
Diaspidiotus zonatus F
Dynaspidiotus britannicus F
Dynaspidiotus ericarum F
Hemiberlesia cyanophylli F
Hemiberlesia lataniae F
Hemiberlesia rapax F
Lepidosaphes conchiformis F
Lepidosaphes pistaciae F
Lepidosaphes tapleyi F
Lepidosaphes ulmi F
Parlatoria oleae F
Parlatoria pergandii F
Saharaspis ceardi F
Voraspis ceratoniae F
COLEOPTERA Buprestidae Ptosima undecimmaculata F
Agrilus roscidus F
Anthaxia millefolii smaragdifrons F
Bostrichidae Apate monachus F
Sinoxylon sexdentatum F
Sinoxylon ceratoniae F
Bostrichus capucinus F
Trogoxylon impresssum F
Xyloperthella picea F
Scobicia chevrieri F
Cerambycidae Phenichroa fasciata F
Cerambyx welensii F
Phytoparasitica

Table 1 (continued)

Order Family Pest species Occurrence

Cerambyx cerdo F
Trichoferus fasciculatus F
Curculionidae Otiorhynchus ceratoniae F
Echinodera incognita F
Echinodera ibleiensis F
Kyklioacalles maroccensis F
Araecerus fasciculatus F
Torneuma maltense F
Xylosandrus compactus F
Xylosandrus crassiusculus F
Silvanidae Oryzaephilus surinamensis SB
Oryzaephilus mercator SB
Ptinidae Lasioderma serricorne SB
Dryophthoridae Sitophilus oryzae SB
LEPIDOPTERA Pyralidae Ectomyelois ceratoniae F/SB
Ephestia figulilella F/SB
Ephestia calidella F/SB
Ephestia vapidella F/SB
Ephestia cautella F/SB
Plodia interpunctella F/SB
Corcyra cephalonica SB
Cossidae Zeuzera pyrina F
DIPTERA Cecidomyiidae Asphondylia gennadii F
ACARI
TROMBIDIFORMES Tetranychidae Tetranychus urticae F
Bryobia siliquae F
MAMMALIA
RODENTIA Muridae Apodemus sylvaticus F
Rattus rattus mainly F
Mus domesticus mainly SB

infests leaves and fruits of many ornamental plants and
crops and it is known to be a serious pest of citrus
(García Morales et al. 2016), and it has already been
recorded on carob in Egypt (Hall 1922). Chrysomphalus
dictyospermi (Morgan), a widely distributed species
considered as a serious pest of citrus in the western
Mediterranean basin, in Greece and in Iran (García
Morales et al. 2016), has been recorded on carob in
Spain and in western Mediterranean areas
(Balachowsky 1932; Martín Mateo 1983).
Chrysomphalus pinnulifer (Maskell), considered as a
tea pest in Kenya and India and a potential international
invader of citrus-growing regions (García Morales et al.
2016), was also reported by Balachowsky (1948) on
carob trees grown in the Mediterranean region.
Among the genus Diaspidiotus, D. pyri
(Lichtenstein) has been recorded in thick incrustations
on branches of C. siliqua together with populations of
Hemiberlesia lataniae (Signoret) and Lepidosaphes
ulmi (Linnaeus) in Palestine (as considered in
Bodenheimer (1924)). Ben-Dov (2012) recorded
D. pyri, D. zonatus (Frauenfeld) and Dynaspidiotus
britannicus (Newstead) on carob trees in Israel.
Besides, D. britannicus, D. pyri and D. lenticularis
(Lindinger) were detected in Sicily (Inserra and
Calabretta 1987; Longo and Tirrò 2005). As such,

Dynaspidiotus ericarum (Goux) was reported by
Balachowsky (1948) on carob in the Mediterranean
basin. Hemiberlesia cyanophylli (Signoret), a species
causing damage to various ornamentals as well as to
avocado, Psidium guajava and tea, has been recorded on
C. siliqua in Israel and Egypt (Hall 1922; Ben-Dov
2012). The congeneric H. rapax (Comstock) has also
been recorded on carob trees in Sicily (Inserra and
Fig. 3 Scale insects infesting carob: a- Aspidiotus nerii on leaf; b-
Coccus hesperidum on pod; c- Planococcus citri on twig (Photos
Di3A)
Phytoparasitica
Calabretta 1987). Lepidosaphes spp., which are not
known to be serious pests of carob trees, were recorded
in Palestine (as considered in Bodenheimer (1924))
(L. conchiformis (Gmelin)), Turkey (L. pistaciae
(Archangelskaya)), Egypt (L. tapleyi (Williams), which
is an important pest of guava in this country) and Crete
(L. ulmi (Linnaeus)) (Bodenheimer 1924; Swailem
1972; Şişman and Ülgentürk 2010; Pellizzari et al.
2011). Parlatoria oleae (Colvée) and Saharaspis ceardi
(Balachowsky) have been reported in Sicily (Inserra and
Calabretta 1987) and Parlatoria pergandii Comstock
and Voraspis ceratoniae (Marchal) have been found to
occur on carob in Turkey and Morocco, respectively
(Lépiney and Mimeur 1931; Çalışkan and Rifat
Ulusoy 2017).
Soft scales (Coccidae) are phloem-feeders that usu-
ally produce abundant honeydew on which microscopic
fungi (sooty mold) can develop causing damage to the
plant (Williams and Watson 1988c). Feeding activity of
soft scales causes yellowing, drying out and death of the
plants. The species that infest carob have mainly been
recorded in Israel: these are Ceroplastes floridensis
(Comstock), Coccus longulus (Douglas) and Coccus
hesperidum (Linnaeus) (García Morales et al. 2016).
The latter species, known as a pest of crops and orna-
mental plants, has also been detected in small population
density in Sicily (Longo and Tirrò 2005), living on twigs
and on the upper face of the leaves (Tremblay 1995) and
producing abundant honeydew. On citrus in Italy it
performs 2 or 3 generations per year and overwinters
as nymph or as young female (Tremblay 1995).
Mealybugs (Pseudococcidae) represent diverse spe-
cies that generally secrete high amounts of honeydew
and usually constitute major pests of a wide range of
host plants around the world (Williams and Watson
1988b; Miller et al. 2002; Franco et al. 2009; Mansour
et al. 2017). Among mealybugs, Planococcus citri
(Risso) has been the only species recorded on carob in
Sicily (Italy) where it infests the basal part of the trunk
of plants that live in humid areas. This economically
important species is common on citrus that constitutes
its primary host plant worldwide, and it also can attack
many other crop and ornamental plants in the
Mediterranean region (Longo and Tirrò 2005; Franco
et al. 2004; Massimino Cocuzza et al. 2016; Mansour
et al. 2018). This mealybug species has been recorded
on carob in Israel and France (Ben-Dov 1994, 2012;
Signoret 1875). In France, it has been recorded together
with Gueriniella serratulae (Fabricius) hidden in the
Phytoparasitica
bark (Signoret 1875). Planococcus citri lives on all the
aerial parts of the plants and nymphs and adult females
overwinter hindered in the bark or on roots and basal
parts of the trunk (Tremblay 1995); and it should be
pointed out that in Sicily it has been observed on carob
trees, inside the galleries escavated by scolytids. The
host plant turns yellow, withers and fruits can fall down
(Tremblay 1995). The congeneric species Planococcus
ficus (Signoret) and Pseudococcus viburni (Signoret),
which are key pests of grapevine in several countries
around the world (Franco et al. 2009; Daane et al. 2012;
Mansour et al. 2018), have been detected on carob trees
in Malta (Mifsud et al. 2014).
The pink hibiscus mealybug, Maconellicoccus
hirsutus (Green), native to South Asia, is distributed in
many countries in the world (EPPO 2006; García
Morales et al. 2016; Negrini et al. 2017). This mealybug
species has been recorded on over 330 host plants
worldwide (García Morales et al. 2016; Chong et al.
2015) with some preference for Fabaceae, Malvaceae
and Moraceae (Ben Halima-Kamel et al. 2015).
Maconellicoccus hirsutus is a pest of Hibiscus rosa-
sinensis and other economically important host plants
including avocado, banana, citrus, cotton, grapevine and
mulberry in the EPPO region (Ben Halima-Kamel et al.
2015). This phloem-feeding insect, invasive in the
Mediterranean region, severely damages the plant by
releasing a toxin during feeding that causes severe
stunting, decline, and deformation of growing terminals,
premature senescence of flowers and leaves, and by
producing abundant honeydew which provides a grow-
ing medium for black sooty mold fungus. The latter
reduces the aesthetic value of plants and their normal
growth and reproduction (Chong et al. 2015). In addi-
tion, the white wax produced by nymphs and adult
females affects the growth of host plants and the mar-
ketable quality of fruits (Negrini et al. 2017). Adult
female body is greyish pink, covered with a thin white
cotton like wax, oval, flattened and 2–3 mm long. This
species is able to perform up to nine generations per year
in Brazil, with 98 eggs per female and 97% viability of
eggs (Negrini et al. 2017). Colonies live on leaves,
shoots and trunk moving to the trunk and on the collar
of the plant during the fall (Ben Halima-Kamel et al.
2015). Maconellicoccus hirsutus has been recorded on
carob in countries of the Mediterranean region such as
Egypt (Hall 1922) and Greece (Milonas and
Partsinevelos 2017). Recently, the pink hibiscus mealy-
bug has been recorded in Tunisia on Hibiscus plants, but
the polyphagy and the wide distribution of the insect
lead to an hypothesis of a geographic expansion and
pose a risk of its expansion to other North-West African
and South-West European countries (Ben Halima-
Kamel et al. 2015) where ornamental plants and crops
could be attacked, taking into account that this mealy-
bug species spreads in the Mediterranean basin together
with its two main parasitoids that can effectively control
its populations (Spodek et al. 2016).
Lepidoptera
Ectomyelois ceratoniae (Zeller)
The carob moth Ectomyelois (Apomyelois) ceratoniae
(Zeller) (Pyralidae) is a highly polyphagous insect with
a cosmopolitan distribution, which has been found on
43 hosts from 18 plant families, among them twenty-one
plants are of economic importance as agricultural com-
modities (Perring et al. 2016). This pest that is appar-
ently of Mediterranean origin (Heinrich 1956) can infest
various host crops either in the field or in storage,
including, among others, carob (De Stefani 1920;
Gentry 1965; Gothilf 1970; Doumandji 1978), date
(Warner et al. 1990; Blumberg 2008), pomegranate
(Al-Izzi et al. 1985; Massimino Cocuzza et al. 2016),
citrus (Gentry 1965; Rungs 1970; Ozturk et al. 2011),
almonds (Gentry 1965; Gothilf 1984; Navarro et al.
1986) as well as grapes (De Stefani 1920; Martinez-
Sanudo et al. 2013). Developmental biology, including
the number of generations per year, and fitness of
E. ceratoniae depend on abiotic (temperature, humidity,
and photoperiod) and biotic (host type and quality of the
host) conditions in which the insect develops (Nay and
Perring 2008; Perring et al. 2016).
Ectomyelois ceratoniae adults generally lay eggs on
damaged carob pods (Gothilf 1970), and in this context
it was proven that females have preference to oviposit
on carobs that were infested with fungi (Gothilf et al.
1975). In Sicily, the first individual adult moths emerge
in late April and damage can be observed on carob pods
(De Stefani 1920). In northern Algeria, E. ceratoniae
eggs are laid on carob pods or on mature fruits with the
occurrence of four generations per year from May–June
to early October, with the first generation being issued
from overwintered larvae (Doumandji 1978).
According to Ashman (1968) E. ceratoniae larvae do
not migrate but pupate within the carob pods in field

conditions. Additionally, fully grown larvae of this in-
sect may also exit the carob fruit to pupate in the soil
(Morland et al. 2019). Cox (1976) demonstrated that the
duration of the pupal period was 6 days at 30 °C, 9 days
at 25 °C and 15 days at 20 °C and that the periods
required for complete development from egg hatch to
adult emergence were 23, 30 and 48 days, respectively.
Ectomyelois ceratoniae can develop two generations per
year on carobs in Cyprus and Sicily (Ashman 1968;
Longo and Tirrò 2005) while this pest can develop up
to four generations per year in date palm agro-ecosystem
conditions characterizing the Mediterranean region
(Calcat 1959; Lepigre 1963; Blumberg 2008).
In general, the main damage caused by E. ceratoniae
(Fig. 4) is due to infestation of the fruits by the larvae
(Perring et al. 2016). For instance E. ceratoniae
can negatively influence the nutritional value of
carobs (Doumandji 1978). In Cyprus, the effects
of E. ceratoniae appear on green developing pods
from about 2 months before harvest (June–July)
(Davies 1970).
Natural enemies of the carob moth in the
Mediterranean area mainly include parasitoids belong-
ing to eight hymenopteran families and attacking either
eggs, larvae or pupae of the host moths (Table 2).
In addition to Hymenoptera, natural enemies
attacking carob moth larvae in the Mediterranean basin
include the larval parasites Clausicella suturata
Rondani (Diptera: Tachinidae) and Pyemotes
ventricosus Newport (Acari: Pyemotidae) (Gothilf
1969; Kugler and Nitzan 1977).
A number of pest control options can be developed
and implemented against E. ceratoniae in the
Mediterranean basin. In this context, most of the avail-
able scientific literature focusing on the application of
various integrated pest management (IPM) tactics is
linked to managing this pest when developing on date
palm fruits. In general, these tactics mainly include
sterile insect technique, post-harvest chemical control
(fumigation) and biological control using microbial-
based pesticides and/or effective parasitoids.
Fig. 4 The carob moth: damage on pod (Photo Di3A)
Phytoparasitica
The sterile insect technique, a control tool using
gamma radiation to sterilize male and/or female carob
moths before their release, has been incorporated in
area-wide integrated pest management programs in
pomegranate plantations and was shown to significantly
reduce E. ceratoniae progeny and decrease adult emer-
gence and moth densities over subsequent generations
(Al-Izzi et al. 1993; Mediouni and Dhouibi 2007;
Chakroun et al. 2017). Alternatively, post-harvest fumi-
gation of host palm dates using either carbon dioxide,
ethyl formate or essential oils of Eucalyptus sp. leaves
was shown to be promising control alternative to the
traditionally used and problematic fumigation based on
methyl bromide (Mills et al. 2003; Ben Jemaa et al.
2012; Bessi et al. 2015).
However, biological control can be considered as the
most ecofriendly and promising control option against
this pest. A lipopeptide biosurfactant produced by
Bacillus subtilis SPB1 was shown to be highly effective
against E. ceratoniae infesting stored dates in Tunisia,
causing histopathological destruction in larvae tissues.
Accordingly, this biosurfactant with such properties can
be exploited for the formulation of a novel microbial
biopesticide for effective control of E. ceratoniae larvae
(Mnif et al. 2013) and as promising alternative to the use
of chemical fumigants as main control tool. Moreover,
interestingly, applications of Bacillus thuringiensis
(Berliner) as biopesticide were shown to be harmless
to the parasitoids Trichogramma cacoeciae Marchal,
Trichogramma bourarachae Pintureau & Babault, and
Trichogramma evanescens Westwood in pomegranate
plantations in Tunisia, implying that combined applica-
tion of Bt with release of either parasitoid species would
be a promising control approach against E. ceratoniae
(Ksentini et al. 2010a). As a suggestion for enhancing
and optimizing biological control against E. ceratoniae,
Perring et al. (2016) pointed out that conservation of
existing natural enemies, combined with augmen-
tative releases properly timed with the carob moth
life cycle and other management options could be
a suitable way towards achieving successful man-
agement of this pest. Of great importance is to
consider that parasitoids cannot provide sufficient
control of E. ceratoniae in the presence of repet-
itive applications of broad-spectrum insecticides
with detrimental side effects on non-target benefi-
cial arthropods. Hence, chemical pesticide input
should be further minimized when releasing para-
sitoids for controlling this pest.
Phytoparasitica

Table 2 Parasitoids attacking different life stages of the carob moth Ectomyelois ceratoniae in the Mediterranean basin ((E) = attacks eggs;
(L) = attacks larvae; (P) = attacks pupae)

Scientific name and attacked moth’s life stage Hymenopteran Family References

Nemeritis canescens Gravenhorst (L) Ichneumonidae Lepigre (1963)

Venturia canescens Gravenhorst (L) Ichneumonidae Aubert et al. (1984)
Herpestomus arridens Gravenhorst (L) Ichneumonidae Aubert et al. (1984)
Diadegma oranginator Aubert (L) Ichneumonidae Aubert et al. (1984)
Pristomerus vulnerator Panzer (L) Ichneumonidae Gothilf (1969)
Trichogramma cacoeciae Marchal (E) Trichogrammatidae Khoualdia et al. (1995); Ksentini et al. (2010b)
Trichogramma evanescens Westwood (E) Trichogrammatidae Ksentini et al. (2010b)
Trichogramma bourarachae Pintureau & Babault (E) Trichogrammatidae Ksentini et al. (2010b)
Trichogramma oleae (Voegele & Pointel) (E) Trichogrammatidae Ksentini et al. (2010b)
Trichogramma embryophagum Hartig (E) Trichogrammatidae Doumandji-Mitiche and Doumandji (1982);
Doumandji-Mitiche and Idder (1986)
Trichogramma cordubensis Vargas & Cabello (E) Trichogrammatidae Idder et al. (2013)
Phanerotoma leucobasis Kriechbaumer (L) Braconidae Mesbah et al. (1998); Bouka et al. (2001)
Phanerotoma ocuralis Kohl (L) Braconidae Khoualdia et al. (1996)
Phanerotoma dentata Panzer (L) Braconidae Lepigre (1963)
Phanerotoma flavitestacae Fischer (E-L) Braconidae Gothilf (1969); Daumal et al. (1973)
Apanteles myeloenta Wilkinson (L) Braconidae Wilkinson (1937); Gothilf (1969)
Apanteles lacteus (Nees) (L) Braconidae Gothilf (1969); Halperin (1986)
Habrobracon brevicornis Wesmael (L) Braconidae Lepigre (1963); Gothilf (1969)
Habrobracon (Bracon) hebetor Say (L) Braconidae Gothilf (1969); Dhouibi and Jemmazi (1993);
Bouka et al. (2001)
Rhogas testaceus (Spinola) (L) Braconidae Gothilf (1969)
Perisierola gallicola Kieffer (L) Bethylidae Gothilf (1969)
Goniozus legneri Gordh (E) Bethylidae Gothilf and Mazor (1987)
Antrocephalus mitys (Walker) (L) Chalcididae Gothilf (1969)
Brachymeris aegyptiaca Masi (P) Chalcididae Gothilf (1969)
Anisopteromalus mollis Ruschka (L) Pteromalidae Gothilf (1969)
Copidosomopsis (Pentalitomastix) plethoricus Encyrtidae Gothilf (1978); Gothilf and Mazor (1987)
Caltagirone (E-L)
Perilampus sp. (L) Perilampidae Bitaw and Saad (1990)

Other lepidopteran species (Cossidae). In addition to attacking ripe carob pods,

In addition to the more economically important pest
E. ceratoniae, other species of the Lepidoptera were
reported to infest carob throughout the Mediterranean
area. These include (i) the raisin moth Ephestia
figulilella Gregson, the dry fruit moth E. calidella
(Guenée), the citrus stub moth E. vapidella
(Mannerheim), the almond moth E. cautella (Walker),
the Indian meal moth Plodia interpunctella Hübner, the
rice moth Corcyra cephalonica (Stainton) (Pyralidae),
and (ii) the leopard moth Zeuzera pyrina (L.)
larvae of the raisin moth E. figulilella, an insect of
cosmopolitan distribution, can mainly infest palm dates
for which it is considered a serious pest, as well as
raisins, field-grown grapes, fallen figs and other host
plants (Kehat and Greenberg 1969; Cox 1975;
Khajepour et al. 2011; Perring et al. 2016). There
are 4–5 generations per year for E. figulilella in
palm dates and overwinters as larvae (all stages),
while pupation occurs during the spring; adult
male moths live for about 11 days and adult fe-
males live an average of 16 days (Perring et al.

2016). Natural enemies of E. figulilella include the
hymenopteran parasitoids Habrobracon hebetor
Say and Venturia canescens Gravenhorst that at-
tack host larvae (Johnson et al. 2000).
Both E. calidella and E. figulilella may lay eggs in
the holes induced by carob moth emergence from the
carob pod (Cox 1976). According to Wheatley (1972),
E. cautella larvae can easily develop in carobs following
its previous infestation by E. ceratoniae. However, E.
vapidella that infests carob and citrus in Mediterranean
countries, feeds on bark, especially damaging on young
grafted stock (Gentry 1965). The pyralid moths
E. calidella, E.vapidella, and P. interpunctella common-
ly infest carob fruits in Sicily (Longo and Tirrò 2005).
However, the leopard moth Z. pyrina is a wood borer
that can infest various cultivated host plants grown in
the Mediterranean basin mainly including, among sev-
eral others, carob, apple, pear, and olive. In general,
larvae of Z. pyrina infestation begins in twigs, then, they
bore and tunnel into the branches of the plants and feed
upon the living wood within which they cause damage
(Howard and Chittenden 1909). Larvae of the leopard
moth attack wood of carob trunks and branches in Spain
and Sicily, resulting in severe damages to young trees
(Longo and Tirrò 2005; Sbay 2008; Lisan 2012). In
Sicily, the adult flight activity of Z. pyrina occurring in
carobs extends from June to October (Longo and Tirrò
2005). Zeuzera pyrina also constitutes a key pest of
apple and pear in northern Italy, where adult emergence
extends from mid-May to early September, has only one
generation per year in this Mediterranean locality
(Castellari 1986). Pheromone-based mass trapping of
male moths, applied during consecutive years, is con-
sidered a promising management tool against Z. pyrina
infesting carob in Sicily (Longo and Tirrò 2005). As
such, this borer can also be controlled by introducing a
wire into the galleries to destroy the larvae or by filling
the holes with pesticide paste (Batlle and Tous 1997).
Diptera
Asphondylia gennadii (Marchal)
Typically, the carob midge complex (Asphondylia spp.)
that infests the pods of the carob tree in Cyprus over-
winters as first instar larvae (three instar larvae during
the whole cycle) in carob pods where they also pupate
(Orphanides 1975). In Cyprus, the first adults of the
Phytoparasitica
overwintering generation of the carob gall midge
Asphondylia gennadii (Marchal) (Cecidomyiidae)
emerge from swollen, deformed pods of carob in spring
and early summer (Gagné and Orphanides 1992) and
may develop a maximum of seven generations per year
(Orphanides 1975). Asphondylia gennadii was also
found infesting and damaging carob pods in Crete
(Greece) (Skuhravá and Skuhravy 1997) and Mallorca
(Spain) (Skuhravá and Skuhravy 2004). In Malta, first
instar larvae of this insect are found in very young, small
pods of carob trees at the beginning of April and adults
emerged in early May (Skuhravá et al. 2002). Attacks of
carob by larvae of A. gennadii cause stunting of the pods
(Ashman 1965) and their deformation, which also remain
small and become brown (Marchal 1904). According to
Davies (1970) the symptoms of attack by this pest in
Cyprus are commonly termed “Brachykarpia” (short
fruit) disease. In the Pantelleria Island (Sicily), A.
gennadii can infest carobs from autumn to spring, within
which it induces galls, and it can also be seen in spring
within Calicotome spinosa (L.) legumes and in summer
on Capparis spinosa L. inflorescences (Peri et al. 2006).
It is worth mentioning that during spring-summer, the
carob gall midge can infest several secondary (alternate)
host plants such as pepper, caper, mustard, potato, aspho-
del, garden rocket and squill, in addition to infesting
newly formed carob pods in July–August in Cyprus
(Orphanides 1975). In Sicilian Islands, the carob gall
midge, which has also been considered as key pest on
crops of caper (C. spinosa), can be attacked by two
hymenoptera species: Eurytoma dentata (Mayr) and
Pseudocatolaccus nitescens (Walker) (Peri et al. 2006).
Coleoptera
Coleopteran pests of carob occurring in the
Mediterranean region belong to five families. These
are the Buprestidae, Bostrichidae, Silvanidae,
Cerambycidae, and Curculionidae.
Among Buprestidae the only species reported as
important pest of carob is Ptosima undecimmaculata
(Herbst) (syn. flavoguttata), occasionally found on de-
bilitated or dead wood (Longo and Tirrò 2005).
Larvae have xylophagous behavior and develop in
wood of dead trees but also in living branches; they
tunnel under the bark, becoming full-grown after two
or three years. Adults are found on dead branches and
trunks from March–May to September (Schaefer 1950;
Phytoparasitica

Volkovitsh et al. 2015). A serious infestation was re- Braham and Gahbiche 2016). Chemical control is pos-
ported by Borg (1930) in Malta where, in many cases, sible against adults of A. monachus by spraying the
the trees were saved by cutting and burning the trunk and branches of ornamental plants in nursery with
infested branches. Once more in Malta this species long-lasting insecticides as suggested for pomegranate
is known to develop in trunks and thick branches and carob or ornamental plants in nursery (Bonsignore
(Mifsud and Bílý 2002). 2012; Massimino Cocuzza et al. 2016). Very few natural
Another buprestid species, Agrilus roscidus enemies of A. monachus are reported until recently.
Kiesenwetter, has been reported attacking carob trees These include, among others, the hymenopterous pred-
and developing in its branches, in Malta (Mifsud and ator Leucospis dorsigera Fabricius (Peretz and
Bílý 2002) and Israel (Volkovitsh 2004). Moreover, Cohen 1961), and the parasites Sclerodermus spp.
Anthaxia (haplanthaxia) millefolii smaragdifrons and other braconid species closely related to the
Abeille, was collected in Tunisia on small carob twigs genus Glyptocolastes (Glyptodoryctes) (Rodriguez-
of few millimeters (Curletti 1981). According to Perez 1975).
Volkovitsh (2004) some other species of the genus Some other bostrychids recovered from carob trees
Anthaxia were previously found on carob in Israel. include Sinoxylon sexdentatum Olivier (Longo and
The family Bostrichidae includes Apate monachus Tirrò 2005), S. ceratoniae (L.) that is the most common
Fabricius (Fig. 5), a wood boring beetle whose larvae bostrichid in Israel (Halperin and Damoiseau 1980), and
can develop on over 80 host plants including, among Scobicia chevrieri (Villa and Villa) present on dead
others, apricot, grapevines, peaches, apples, pears, avo- wood, which is also widespread in Israel (Halperin and
cados, citrus, pomegranate and ornamental plants. Damoiseau 1980), Malta (Nardi and Mifsud 2015) and
This species is relatively widespread in tropical Italy (Longo and Tirrò 2005). Other less common spe-
Africa and it is also found in several Mediterranean cies (sporadically reported) are Bostricus capucinus (L.)
countries (e.g. Tunisia, Corsica (France), Spain, south- (Halperin and Damoiseau 1980), Trogoxylon impressum
ern Italy, including Sicily and Sardinia). On Carob, it (Comolli) and Xyloperthella picea (Olivier) found under
was reported in a nursery in southern Italy on the Ionian bark (Nardi and Mifsud 2015). Trogoxylon impressum is
coast of Calabria (Bonsignore 2012), in Sicily (Longo most widespread in woods in Italian storage conditions
pers. comm.), in Israel (Halperin and Damoiseau 1980),
and in Malta (Nardi and Mifsud 2015). It is considered
the most destructive pest of the family Bostrichidae in
Israel (Geis 2002). The presence of tunnels and adults of
this species was also reported on olive trees, citrus fruits,
almond trees and vines in precarious vegetative condi-
tions in eastern Sicily (Di Franco and Benfatto 2008;
Conti et al. 2013; Suma et al. 2013; Longo 2014). The
adults, with a dark-brown body, are up to 19 mm long
and have the front wings truncated back, with the ante-
rior edge of the apical declivity provided with some
small teeth. They are normally present from the begin-
ning of June until October; they are excellent flyers and
are carried on various spontaneous and cultivated arbo-
real plants where they dig tunnels in the living wood,
more or less linear, of variable diameter and length in
relation to the vegetable substrate (Longo 2014). The
damage can be important in young plants in water stress
after transplanting. In order to reduce the population
density, it could be suggested to eliminate dead or
decaying wood, also of neighboring spontaneous and
cultivated plants, where the eggs and larvae are normal-
ly found (Peretz and Cohen 1961; Zanardi et al. 1969; Fig. 5 Apate monachus: adult on carob twig (Photo Di3A)

(Nardi and Mifsud 2015) and in Pantelleria Island
(Sicily) (Nardi and Ratti 1995).
Cerambycidae species (Fig. 6) found on carob wood
are polyphagous on dead branches and twigs and are not
considered herein as pests.
There are many reports of these beetles in the
Mediterranean area, especially in Sicily (Baviera et al.
2017). Among the noxious species, Penichroa fasciata
(Stephens) is reported on C. siliqua in Sicily (Sama and
Schurmann 1980) and in the smaller Italian Islands of
Pantelleria and Lampedusa (Romano and Sparacio
1995). Currently, this species is widespread and com-
mon in the whole area of Sicily (Baviera et al. 2017).
The life cycle of P. fasciata lasts 2 years, and adults
come out in May–August. Cerambyx cerdo Linnaeus
occurs in mainland Italy and Sicily but it is uncommon
in natural habitats since living mostly in urban areas on
Quercus ilex (L.). Mifsud (2002) stated that the presence
of this species on carob trees in Malta might be linked to
occasional adaptations. Cerambyx welensii (Küster) (=
velutinus) and C. miles Bonelli are also widespread in
Sicily (Batlle and Tous 1997; Baviera et al. 2017) and
Malta (Mifsud 2002). However, Trichoferus
fasciculatus (Faldermann) (9–16 mm in size) is a rela-
tively common longhorn beetle species occurring in
mainland Italy, Sicily (Sama 2005; Baviera et al.
2017)) and Cyprus (in dead branches) (Ambrus et al.
2014). This species has also been reported in smaller
Sicilian islands including Lampedusa, Linosa (Romano
and Sparacio 1995), Lipari (Cecchi and Lo Cascio
2000), and Salina (Sparacio et al. 2003). Trichoferus
fasciculatus also develops on several fruit and ornamen-
tal trees such as Ficus, Sorbus, Nerium, Vitis, Spartium,
Castanea, Ulmus, Morus, Punica, Robinia, Pistacia,
etc. Larvae feed especially in the wood of dead twigs
Fig. 6 Exit hole of a cerambycid beetle infesting carob (Photo
Di3A)
Phytoparasitica
of 1–3 cm of diameter and also in branches and trunks.
The life cycle of the adults lasts 1–2 years and they
normally appear in May–September. Other cerambycid
species can be found on carob, but their role is still not
well known. They are listed in Mifsud (2002), Sama
et al. (2010), Ambrus et al. (2014) and Baviera et al.
(2017), often as larvae developing in dead wood.
Among the Curculionidae, the weevil Otiorhynchus
ceratoniae Davidian, Gültekin & Korotyaevis has been
reported to feed on carob leaves as recorded from a
restricted area of eastern Mediterranean Turkey
(Davidian et al. 2017). Ceratonia siliqua leaves suppos-
edly damaged by O. ceratoniae adults were observed at
the level of lower branches. Authors supposed that
adults feed on leaf margins producing small and semi-
circular notches bitten out of the periphery of the lamina,
characteristic signs of Otiorhynchus spp. damage.
However, they found O. ceratoniae specimens only in
the litter beneath the carob trees, where no other weevil
was found. This Otiorhynchus species seems to be the
only specialized weevil known to feed on carob tree;
nevertheless no other reports on its presence occurred in
the scientific literature.
A d d i t i o n a l l y, t h r e e d i f f e r e n t s p e c i e s o f
Cryptorhynchinae (Curculionidae) were reported on
C. siliqua by Astrin et al. (2012): Echinodera incognita
(Hoffmann), E. ibleiensis (Stüben) and Kyklioacalles
maroccensis (Stüben). Echinodera incognita was found
in North-East Málaga (Spain) during 2009 in associa-
tion with Olea spp. and C. siliqua. Echinodera ibleiensis
was recorded in Sicily during 2002 in association with
Castanea spp., Quercus spp. and C. siliqua.
Kyklioacalles maroccensis was instead found in 2009
on the Anti-Atlas Mountains of Morocco in association
with Argania spinosa and C. siliqua (Astrin et al. 2012).
However, no further information about the occurrence
and the level of damage of these beetles on carob tree
was found in the scientific literature.
Mature fruits of C. siliqua can be infested by the
cosmopolitan “coffee bean weevil” Araecerus
fasciculatus (De Geer) (Anthribidae), as recorded from
the Maltese Islands in the Central Mediterranean area by
Mifsud and Colonnelli (2010). Adults are about 4 mm
long with a mottled, dark-brown appearance, particular-
ly on the elytra (CABI 2019). Araecerus fasciculatus is
known as a pest of coffee and cacao grains. It also can
attack a wide range of other stored seeds like hazelnuts,
legumes, drugs, maize, and others (Valentine 2005), and
can complete its life cycle in citrus fruits in the field
Phytoparasitica
(Grout et al. 2001). The impact of A. fasciculatus is
particularly severe at high humidity storage conditions
(El-Sayed 1935; CABI 2019). High air temperature
treatments can determine 100% of A. fasciculatus mor-
tality outside (45 °C for 12 h or 50 °C for 6 h) and inside
(55 °C for 24 h) the seeds (Rachmanto et al. 2018).
Laboratory trials using insecticides by dipping adult
beetles showed that the most effective substances
in inducing insect mortality were cypermethrin,
deltamethrin, dichlorvos, profenofos and trichlorfon
(Grout et al. 2001).
The curculionid species Torneuma maltense Magnano
& Mifsud, endemic to the Maltese Islands, was found in
the soil in association with roots of several
Mediterranean maquis species (Pistacia lentiscus L.,
Olea europaea L., Laurus nobilis L., Salix pedicellata
Desf. and Q. ilex) including C. siliqua (Magnano and
Mifsud 2001; Mifsud and Colonnelli 2010). Adults are
brown in color and 2.2–3.2 mm long (Stüben 2007).
Recently, two invasive ambrosia beetles, Xylosandrus
crassiusculus (Motschulsky) and X. compactus
(Eichhoff) (Coleoptera: Curculionidae: Scolytinae) have
been identified as carob tree pests (Longo and Tropea
Garzia 2016; Francardi et al. 2017; Vannini et al. 2017;
EPPO 2019). Ambrosia beetles transport and inoculate
the symbiotic ambrosia fungi into the walls of their
gallery where the growing mycelium will serve as food
source for the larvae. First symptoms of ambrosia beetle
infestations on small woody parts can be leaves and stem
necrosis, followed by flagging and wilting of the whole
twig due to the pathogenic action of the symbiotic fungi.
Several entry holes, wood necrosis, and sap emission
from large branches and trunks can be observed on
attacked carob trees. The granulate ambrosia beetle,
X. crassiusculus, is known as a successful invasive spe-
cies that can infest economically important crops as well
as forest and ornamental woody species (EPPO 2019).
Xylosandrus crassiusculus adults are reddish-brown in
color and about 3 mm long. They can be distinguished
from other xyleborines thanks to the lack of declivital
striae and to the presence of several confused declivital
granules giving a dull appearance (Rabaglia et al. 2006).
This beetle can colonize all the woody tree parts, with
attacks have been observed on twigs, branches and
trunks (Gallego et al. 2017; EPPO 2019). In Europe,
attacks of carob trees by X. crassiusculus were detected
in Italy (Pennacchio et al. 2003; Tinivella et al. 2010),
France (Nageleisen et al. 2014), Spain (Gallego et al.
2017) and Slovenia (Kavčič 2018). Besides, this Asian
wood-boring beetle, considered as one of the most suc-
cessful invaders, is widespread in Africa (Wood and
Bright Jr. 1992; Atkinson et al. 2000), Australia (IPPC
2017), Pacific Islands (Beaver 1976), and Americas
(Atkinson et al. 1988; Rabaglia et al. 2006; Flechtmann
and Atkinson 2016; Landi et al. 2017). Typical signs of
the X. crassiusculus infestation are represented by char-
acteristic compact cylinders of frass pushed out from the
tunnels excavated by the females. The polyphagous
black twig borer, X. compactus (Fig. 7), which probably
originates from East Asia, attacks more than 200 plant
species, usually on twigs and small branches (EPPO
2017).
Xylosandrus compactus females are dark black in
color and characterized by smaller size 1.6–1.8 mm
and the presence of strial setae on the declivity
(Rabaglia et al. 2006). This beetle was recorded in
Italy on laurel and many other plants (Garonna et al.
2012; Francardi et al. 2012) as well as on a large number
of Mediterranean maquis species including C. siliqua
(Longo and Tropea Garzia 2016; Vannini et al. 2017;
Gugliuzzo et al. 2019b). Moreover, X. compactus was
recorded during 2016 in France (EPPO 2017), the only
other European country where the beetle is present.
However, the black twig borer is now widely distributed
in Africa, Asia and South America and introduced in the
Pacific Islands, New Zealand and South-East USA. In
all of these geographical regions the pest is known as a
borer of seedlings, shoots and small twigs (Ngoan et al.
1976; Greco and Wright 2015). Xylosandrus compactus
also causes severe economic damage to coffee and
cacao in several tropical regions (Brader 1964; Egonyu
et al. 2009; Kagezi et al. 2014; Greco and Wright 2015).
Typical symptoms of the black twig borer infestation are
necrosis of terminal leaves and stem and flagging of
branches (Hara and Beardsley 1979). However, in Sicily
heavy infestations occurred on carob trees also on
large branches and trunks with diameters greater
than 30 cm and 80 cm, respectively (Gugliuzzo
et al. 2019a) (Fig. 8).
These infested trees showed several entry holes,
wood necrosis, and sap emission. The most common
symbiotic fungi associated with X. compactus are
Fusarium solani (Mart.) Snyd. & Hans, Ambrosiella
xylebori Brader ex Arx & Hennebert and
A. macrospora (Francke-Grosm.) L.R. Batra (Ngoan
et al. 1976; Muthappa and Venkatasubbaiah 1981;
Bhat and Sreedharan 1988; Daehler and Dudley 2002;
Bosso et al. 2012; Bateman et al. 2016). Volatiles

Fig. 7 Xylosandrus compactus attacking carob: a- Eggs; b- Larvae; c- Pupae; d- Adults (Photos Di3A)
generally released by stressed plants (Ranger et al. 2010;
Burbano et al. 2012) and in particular ethanol (Ranger
et al. 2012) represent the most attractive semiochemicals
for many ambrosia beetles including Xylosandrus spe-
cies (Ranger et al. 2011; Reding et al. 2013). Some
studies showed that ethanol is used by ambrosia beetles
to locate host plants (Miller and Rabaglia 2009; Ranger
et al. 2012). In fact, the presence of different Xyleborini
species can be evaluated using ethanol-baited traps
(Reding et al. 2010, 2011) and this attractant appeared
to be more effective when used in combination with
Japanese beetle traps rather than with Lindgren funnel
traps (Burbano et al. 2012). Similarly, red cross-shaped
sticky traps baited with ethanol used to evaluate the
flight activity of X. compactus in infested carob trees
generated promising results (Gugliuzzo et al. 2019b).
Due to the difficulty to reach the ambrosia beetle colo-
nies inside the infested wood, one of the very few
options for controlling these pests is the Push-Pull
Strategy (Cook et al. 2007; Gillette et al. 2012). This
control tactic can be carried out with ambrosia beetle
placing the anti-aggregation pheromone verbenone in
slow-release dispensers on the trees and the ethanol-
baited traps at a sufficient distance to catch flying adults
(Burbano et al. 2012; Ranger et al. 2013; Van Der Laan
and Ginzel 2013). Among biological control tools, the
application of entomopathogenic fungi against
X. crassiusculus was evaluated in laboratory bioassays
Phytoparasitica
using two commercial Beauveria bassiana strains and
Metarhizium brunneum F52 (Castrillo et al. 2013). The
tested entomopathogens were virulent to
X. crassiusculus causing more than 70% of mortality
5 days after inoculation. Moreover, the mycoparasitic
fungi Trichoderma harzianum T-22 reduced
X. crassiusculus brood size thanks to the competition
with the symbiont and the more rapid growth on it
(Castrillo et al. 2016). Mizell and Riddle (2004)
assessed insecticide efficacy by dipping tree bolts: they
obtained lowest number of attacks per bolt with
bifenthrin and cypermethrin.
There is still scarce information on control options
adopted against X. compactus. Natural enemies have
been reported in association with the pest, but very
few studies on their real impact against the pest are
available. Sreedharan et al. (1992) observed larvae of
the predatory beetle Callimerus sp. (Coleoptera:
Cleridae) consuming an average of 18 larvae or pupae
of the beetle per day under laboratory conditions.
Moreover, Cryptamorpha desjardinsi (Guérin-
Méneville) (Coleoptera: Silvanidae) was found feeding
on X. compactus larvae on infested coffee branches and
inside coffee berries (Greco 2010). The formicid ant
Plagiolepis sp. was reported in Uganda colonizing over
18% of X. compactus galleries and preying on all life
stages of the beetle (Egonyu et al. 2015). The predatory
ant Pheidole megacephala, which is common in coffee
Phytoparasitica

Fig. 8 Carob tree damaged by

Xylosandrus compactus
(Photo Di3A)

fields infested by X. compactus, was unable to enter Mites (ACARI)

inside the beetle galleries but it was able to prey upon
all stages of X. compactus in a Petri dish bioassay Drought stress on carob foliage is an important factor
(Ogogol et al. 2017). A parasitoid of the genus limiting the role of phytophagous mites, which typically
Eupelmus (Hymenoptera: Eupelmidae) has been found feed on leaf surface by their slender stylets. In such
in association with X. compactus in India. However, the conditions, the increasing concentration of the sap and
maximum incidence (20.5%) of this species was ob- also the presence of leathery leaves directly affect the
served only during the presence of higher densities of mite performance and the ability to damage the leaves.
X. compactus populations (Balakrishnan et al. 1989). Two tetranychid species were reported on C. siliqua
Moreover, Tetrastichus xylebororum Domenichini leaves (Migeon and Dorkel 2019), but no real damage
(Hymenoptera: Eulophidae), a bethylid species was observed. In the case of Bryobriinae, females and
(Hymenoptera: Bethylidae), and other natural enemies larvae of Bryobia siliquae Hatzinikolis & Emmanouel
were reported in India, Ivory Coast and Indonesia in were found in Greece on isolated trees on both leaf
association with the pest (Balakrishnan et al. 2011). The surfaces near the main vein (Hatzinikolis and
entomopathogenic fungus B. bassiana was able to infect E m m a n o u e l 1 9 9 1 ) . A m o n g Te t r a n y c h i n a e
21% of the beetles occurring in robusta coffee infested Epitetranychus althaeae v. Hainstein (syn. Tetranychus
branches after augmentative spray applications of spores urticae Koch) was associated to carob foliage in
(Balakrishnan et al. 1994). The insecticide chlorpyrifos Palestine (as considered in Klein (1936)). Moreover,
(240 g a.i./ L emulsion), used on flowering dogwood in Oligonychus perseae Tuttle Baker & Abbatiello
Florida, caused 83% of mortality toward all stages of (Baker and Tuttle 1994), a spider mite native to
X. compactus (Mangold et al. 1977).
Coleopteran pests that have been frequently reported
to infest stored carob pods include Oryzaephilus
surinamensis (L.), O. mercator (Fauvel) (Silvanidae),
Sitophilus oryzae (L.) (Dryophthoridae) and
Lasioderma serricorne (F.) (Ptinidae) (Pemberton and
Rodriguez 1981; Hagstrum and Subramanyam 2016;
Hagstrum et al. 2013). These insect species are
also universally known as destructive pests of
stored cereals and their derivatives, legumes and
vegetables. The most notable damage is mainly
due to the trophic activity of the larvae, and the feeding
generally results in weight loss, fungal growth and loss
of the carob quality. Fig. 9 Carob branch damaged by rodents (Photo Di3A)

Central America (Tuttle et al. 1976), was known as a
pest of Persea americana Miller and also of many other
plants. The species has already been reported in Israel
(Ben-David et al. 2007), Portugal (mainland and
Madeira) (Borges et al. 2008), Spain (mainland and
Canary Islands) (Alcázar et al. 2005; Migeon and
Dorkeld 2019) and Italy (Zappalà et al. 2015) on avo-
cado plants. However, it might be possible to record
O. perseae on carob trees in the Mediterranean terri-
tories, considering that it was already, but sporadically,
found on carob in California (Baker and Tuttle 1994).
Rodents (RODENTIA)
Among mammalian pests, small rodents including the
house mouse, Mus musculus domesticus, are able of
seriously damaging carob pods in storage structures,
while the wood mouse Apodemus sylvaticus (L.) and
the roof rat Rattus rattus (L.), in some particular cases
(i.e. high population density and low food availability),
could gnaw through the outer bark layer and eat
the wood (Longo and Tirrò 2005) (Fig. 9). The
chewing activity disrupts the plant’s ability to
transport nutrients and water between the leaves
and roots, also lead to the death of the portion
of the plant above the damage. Besides, occasion-
ally, small rodents like gophers (Pitymys spp.) can
severely damage the root system of young carob
trees (Batlle and Tous 1997).
Conclusion and future outlook
The carob tree has long been cultivated mainly in coun-
tries of the Mediterranean basin. This plant has several
agro-ecological, socio-economical, as well as human
health benefits. For such a reason protecting it from
pests and diseases is a crucial issue nowadays. This
long-living evergreen crop may be attacked by a number
of pests (mainly insects), which may significantly de-
crease overall crop production and yield. In this context,
based on the scientific literature, some insect species
such as the carob moth E. ceratoniae and some
bark and wood-boring coleopterans received par-
ticular attention regarding the application of some
pest management measures to limit their further
spread and to protect carob cultivation in the
Mediterranean basin.
Phytoparasitica
Typically, control of these insects mainly rely on
application of broad-spectrum synthetic insecticides.
Nevertheless, this approach cannot be regarded as envi-
ronmentally safe and sustainable control tactic against
the major pests of carob, obviously due to the detrimen-
tal side effects of synthetic active substances exhibited
on non-target beneficial arthropods. Importantly, some
prophylactic and cultural practices, avoiding rapid
spread of the pest, and exploitation of natural resources
through conservation biological control using effective
parasitoids and predators could be the most promising
and sustainable control options of these insects. Still,
much more field surveys and research efforts should be
performed in the near future to enhance our knowledge
about bio-ecological aspects and natural enemies of
insect pests infesting and damaging carob. This step
would be necessary to suitably develop and implement
the most effective and eco-friendly pest management
options with the aim of sustaining carob crop yield in
the Mediterranean area and worldwide.
Compliance with ethical standards
Conflict of interest The authors declare that they have no con-
flict of interest.
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