The Inventory of Scale Insects (Hemiptera, Coccoidea) Associated With Olive Tree in North of Tunisia


 Background: This study was realized for more than four years (from 2014 to 2018) in olive groves of northern Tunisian governorates. Scale insect samples were collected from leaves, stems and fruits.Results: An annotated list of 22 scale insect species has been recorded. These species divided into 4 families. The family Diaspididae is the most species-rich, with 14 species in 9 genera; Coccidae contains 4 species in 3 genera; Pseudococcidae contains 3 species in 3 genera; and Asterolecaniidae contains 1 species in 1 genus.Conclusions: This paper contains 3 species recorded for the first time in the Tunisian fauna: Saissetia coffeae (Walker), Diaspidiotus ostreaeformis (Curtis) and Lepidosaphes conchiformis (Gmelin).


Introduction
The olive tree, Olea europaea (L.) (Oleaceae: Olea) is a species belonging to the family Oleaceae, characterized by evergreen leaves, native to the coastal areas of the eastern Mediterranean region, Lebanon and the maritime parts of Asia Minor north of the Iran at the southern end of the Caspian Sea. Its fruit is of major agricultural importance as a source of olive oil and table olives (Cimato & Attilio 2011). In Tunisia, the olive tree is the most cultivated fruit species, there are about 88 million trees spread over 1,880 thousand hectares (Larbi et al 2020).
Scale insects, sap-sucking hemiptera, are found on various parts of their hosts such as leaves, twigs, branches and roots (Kondo et al 2008). Once xed, Scale insects turn into a real automatic pump extracting the sap. Damage to plant tissue is often aggravated by toxic enzymes present in the saliva of some species. These enzymes are also responsible for the discoloration and premature fall of leaves as well as the deformation of plant tissues (Gullan & Martin 2003). Scale insects can also cause indirect damage by pathogens transmission or by accumulation of honeydew, which promotes the fungi establishment (Ross et al 2010  Geographic distribution. The scale is found in 19 countries on olive tree (García et al 2020). A serious pest of olive tree in Crete, Greece and Sicily (Liotta & Sammatrano 1981).
Biology. Pollinia pollini is found in most olive growing regions of the Mediterranean Region and in California. It is found on leaves, twigs and fruit of its exclusive host, the olive tree. Generally one (Liotta & Sammartano 1981)  Structure. Adult females are spherical, orange to red and covered with a grayish yellow waxy substance that protects entire colonies observed in the twigs and branches, or in crevices or cracks in the bark (Orecchia et al 2007). The males nymphs are lemon yellow in color, elongated, slightly attened towards one of its ends, whose nymphs are found on the leaves. The males adults are winged (Jarraya 2003 Geographic distribution. It originates from East Asia (Tereznikova 1981), widespread, is found in 140 countries (García et al 2020), including Tunisia on olive tree (Jarraya 1970).
Biology. Coccus hesperidum is a highly polyphagous species, feeding on plants belonging to 130 families, an important pest of various fruit trees and ornamental plants (Ebeling 1959, Hodgson & Henderson 2000. A tropicopolitan species commonly found on leaves and twigs (Hamon & Williams 1984). The females reproduce parthenogenetically in most areas. Males were observed in England (Newstead 1917) and in greenhouses in the USSR (Saakyan-Baranova 1964). Develops six annual generations in Israel (Bodenheimer 1951); 3-5 generations in the United States (Ebeling 1959).
Structure. The adult female of C. hesperidum is oval, at or slightly convex, and asymmetrical. Young adult green-yellowish to yellowish-brown, spotted with brown spots, sometimes coalescing in marbled areas. It has been observed that the colour of females often resembles the colour of this part of the plant where they feed. The length of the mature female is 1.5 to 4.5 mm. The legs and the antennae persist during the antère life. Biology. Lichtensia viburni develops on the underside of leaves and shoots, particularly in the thickest parts of the foliage; the damage is caused by nutritional stings and the production of honeydew which, in addition to making the leaves asphyxiated, promotes the formation of sooty molds, further aggravating the damage. Lichtensia viburni overwinters as a nymph which completes development in the following spring. Females lay their eggs in their sacs between May and June. The emergence of the rst generation nymphs requires about 2-3 weeks; the appearance of the second generation nymphs occurs between August and September (Quaglia 1986). In central and northern Italy, on olive trees, L. viburni is able to producing 1 or 2 generations per year (Kosztarab & Kozar 1988) Structure. The adult female is about 5 mm in lengh, has a yellowish body, with darker, oval and slightly convex spots; in females, the body appears covered with an ovisac of white wax, produced by the ceriparous glands of the back. Nymphs are greenish-yellow and oval. The male is winged and ickers from an elongated follicle. Geographic distribution. Saissetia oleae, which is thought to be native to South Africa (De Lotto 1965), is a cosmopolitan speices, is found in most Mediterranean countries (Jarraya 1970). Recorded also from California and Australia.
Biology. Saissetia oleae is a polyphagous species, feeding on numerous cultivated and ornamental plants belonging to 80 botanical families (García et al 2020). In the Mediterranean basin, S. oleae is an economic pest of olive and citrus trees (Bodenheimer 1951). In the Tunisian coastal olive groves, S. oleae is considered to be the most important scale insect species (Jarraya 2003, Mansour et al 2011. In general, S. oleae shows only one generation per year (univoltine), but under mild climate in autumn, an incomplete second generation may occur (Gill 1988, Jarraya 2003).
Structure. The body of females is from 2.5 to 6 mm in size, convex, ranging in colour from light to dark brown. On the dorsal side there is visible a characteristic, protruding, H-shaped pattern, which allows to differentiate the species easily from another, similar species belonging to the same genus, i.e. S. coffeae (Tereznikova 1981 Geographic Distribution. Aonidiella aurantii has a relatively cosmopolitan distribution, Encountered in 87 countries, mentioned in Tunisia by Balachowsky (1932).
Biology. Aonidiella aurantii is highly polyphagous species; it has been recorded on 263 plant host species (García et al 2020). It is an ovoviviparous, biparental species that can infest all aerial parts of host plants (Ferris 1938). Larvae exhibit positive phototropism and tend to move to the outer canopy, settling on fruits and young leaves (Campos-Rivela et al 2012). It seems to show a preference for young trees with a good vegetative state (Bodenheimer 1951).
Structure. The adult female is circular, rather at, exuviae in the center, is rather thin and pale, is red-brown in color and severely sclerotized. The length of the body is 1.5 to 2 mm. The male is elongated oval, paler in color than in the female, exuvia slightly to one end (Ferris 1938, Longo et al 1994. Geographic distribution. Aspidiotus nerii is a cosmopolitan; It has a worldwide distribution, especially in the tropical and subtropical zones (Zahradnik 1990  Structure. Female is white or pale gray scale, the body length is about 2 mm, circular, at, subcentral exuviae. Male with similar color, slightly oval, exuvia subcentral (Ferris 1938 Geographic distribution. Chrysomphalus aonidum is found in 84 countries (García et al 2020), cited in Tunisia by Jendoubi (2012). Today, it is present in ve continents.
Biology. Chrysomphalus aonidum is a very polyphagous species, grows on the leaves and fruits of many host plants. Reproduction is sexual, each female lays between 50 to 150 eggs over a period of 1-8 weeks (Watson 2005). We record 3-4 generations per year in China (Miller & Davidson 2005) and 5-6 generations per year in California (Gill 1997).
Structure. The female scale is circular, at to moderately convex, 1.5-2.5 mm in diameter, of little variable color but tending to be rather dark brown or bluish-black with reddish brown central exuviae (Watson 2005).The exuvies placed in the center being slightly paler than the other parts; the male is oval a little elongated, exuvia near one end (Ferris 1938 Geographic distribution. Chrysomphalus dictyospermi is cosmopolitan (García et al 2020), mentioned in Tunisia by Balachowsky (1932). It is widespread in tropical and subtropical regions , Gill 1997. It is distributed predominantly in Mediterranean countries and in Middle Eastern countries (Lodos 1982).
Biology. Chrysomphalus dictyospermi is a highly polyphagous species (Borchsenius 1966). It is a serious pest of citrus and other trees such as olives and palms (Miller & Davidson 2005).
In most C. dictyospermi populations, the reproduction is sexual. However, uniparental (parthenogenetic) and biparental (sexual) populations of this species have been recorded in the USA (Brown 1965). The female lays between 80 and 200 eggs over a period of one to several months (Chkhaidze & Yasnosh 2001). In the USA, C. dictyospermi has 3 to 6 generations per year (Gill 1997), in Egypt, only 2 (Salama 1970). Mortality due to abiotic factors is high reach to 78% (Chkhaidze & Yasnosh 2001).
Structure. The female scale is greyish or brown in color with a coppery tinge; the shape is almost circular (1.5 to 2.0 mm in diameter), at and thin (Salama 1970, Watson 2005. Male scale covers are yellowish in color and elongated oval in shape with subterminal exuviae (Gill 1997). Biology. Diaspidiotus ostreaeformis is a very polyphagous species, most often living on deciduous trees, mainly rosaceae (Balachowsky 1950, Argyriou 1990). It mainly inhabits the ligni ed parts of the plant. In Central Europe, it has an annual generation and overwinters as a second stage nymph under a shield (Podsiadlo 2017).
Structure. The female scale is circular, moderately convex, exuviae subcentral. It is gray-brown in color, dark in the central part and margin sometimes with a white border (Ferris 1938). The diameter is about 1.5 mm. The male is oval to elongate, gray-green in color, almost white on the margins. The length is about 0.6-0.8 mm (Borchsenius 1935 Biology. This species is a pest of deciduous fruit trees, mainly pears and plums (Balachowsky 1950, Schmutterer 1957, as well to forest trees (Zahradnik 1990).
Structure. The adult female scale is almost circular (diameter 1.5-2 mm), convex and dark grayish-brown in colour; dark orange exuviae (Hall 1925  Structure. The adult female cochineal is 1.5-2.0 mm diameter, convex slightly elongated, yellow, transparent in the center and white in the circumference or around the exuviae; large exuvia, oval elongated ). If present, male scale cover elongate oval with yellow subterminal exuviae, smaller and sometimes paler than that of female. Body of adult female bright yellow (Gill 1997 Geographic distribution. Hemiberlesia rapax is native to Europe (Gill 1997), is a cosmopolitan ), mentioned in Tunisia by Balachowsky (1932).
Biology. Hemiberlesia rapax is a polyphagous pest, was observed affecting the stem, leaves, and fruit (Moghaddam 2004). This species is primarily found on over 117 genera in 60 plant families , Borchsenius 1966 and is considered as one of the 43 most damaging diaspidid species to agriculture (Beardsley & González 1975).
Structure. The female is 1.0-2.0 mm long, circular to somewhat elongate, convex, grey to white with yellow-brown central or subcentral exuviae. Ventral scale often well developed (Ferris 1938, Gill 1997. The male scale cover as similar to that of female but smaller and more oval, with yellow subterminal exuviae  Biology. Lepidosaphes conchiformis has 2 generations per year, overwintering as fertilized females. The female lays about 60 eggs. Eggs hatch from May to June ( rst generation) and from August to September (second generation) (Murakami 1970).
Structure. The female scale is light brown, small, wide posterior, 1.2-2.7 mm long, curved or straight, after completion of oviposition. The male is thin, membranous, white to purplish white, 0.7-1.0 mm long (Borchsenius 1958). The eggs are white (Kuwana 1925 Biology. Encountered on several cultivated and wild woody plants. Develop 3 generations a year. The rst generation is in march-april, the second is in june-july and the third is at the end of august (Ammar 1986).
Structure. The adult female is 1.0-3.5 mm long, convex, mussel-shaped, strongly tapered towards the exuvial end. The female body is white to yellowish, with yellowish-brown pygidium (Zahradník 1990). Scale cover of male is light brown, smaller, slenderer, with yellow terminal exuviae. Adult male is winged (Ghauri 1962 Trabut (1910), and seems to be rare.
Biology. In Greece, L. riccae undergoes 2 generations per year. It is observed on ripe olive fruit. The infested fruit was severely deformed (Argyriou & Kourmadas 1981).
Structure. the body of the female remaining within the whitish exuvium of the 2nd stage nymph. The bodies of all stages, including the male, are purple, except before molting, when they are brownish. The shield is elongated, white-grey, about 2.1 mm long, with the darker dorsal exuvium of the 1st stage nymph embedded at one end. The shield of the male is white, slightly curved, about 1.8 mm in length.  (Huffaker et al 1962, Argyriou 1990). The larvae that settle at the beginning of the development cause anomalies and deformations on the fruits, which makes them unpleasant. On olives, the spots are black. According to Stafford (1948), the oil content of heavily infested olives can be reduced by 20%.
Overwintering occurs as fertilized adult females, although a small portion of the population can overwinter at the second stage (Huffaker et al 1962). Adult males are required for breeding (Stafford 1947). Adult female lay a maximum of 100 eggs, the laying lasts 2-3 weeks (Huffaker et al 1962).
Structure. The eggs and immature stages are pink to violet. The adult female is 1.0-2.0 mm diameter, convex, circular to elliptical, white to very light grey with darker, subcentral to terminal exuviae. Pygidium with 4 pairs of lobes (Rahman & Ansari 1941).
Male scale cover white, oblong, about 1.0 mm long, with a brownish-yellow terminal exuviae often marked with dark green. Adult male is winged (Ghauri 1962). in Tunisia by Ben-Dov (1994). It is a common greenhouse pest around the world, but can also be found outdoors in warm climates (Tenbrink & Hara 2007 Structure. Adult females with an oval body measuring 4.5 mm long, a pinkish-gray color and covered with a powdery whitish wax. These females have a long tail as long as the body (Goolsby 1994). Males are smaller, slender, darker in color, and winged.

Discussion
With the advent of national and international commercial exchanges. Several species of scale insects have been introduced to Tunisia due to the free trade of live plants and fresh produce. Most of these species would pose an economic or environmental.
In Tunisia, about 75 scale insect species have been recorded by Mansour et al. (2016). The great majority of these species are of no or minor economic importance.
On olive tree, Jarraya (2003) started to listing scale insect species. This work have been followed by Mansour et al (2011). The survey performed in 2009 in Tunisian olive groves, revealed the occurrence of six scale insects. The identi ed species were: the armoured scales A. nerii, L.ulmi, and P. oleae, S. oleae and F. follicularis and the mealybug species P. cycliger.
Our recent study carried out only in the north of Tunisia revealed more species of scale insects on olive tree than those described by Mansour et al. (2011); those are, 22 species including 3 species encountered for the rst time in Tunisia on olive trees.
According to Mansour et al. (2011), only one scale insect specie was found in olive groves, namely either S. oleae or P. cycliger. The mealybug P. cycliger was the most common species reported within olives groves of the Northwest region of Tunisia. While, in the Northeast regions, S. oleae was proven to be occurring throughout olive groves of the Northeast region of Tunisia.
However, in our study the most widespread species in the olive groves of the north are P. pollini, P. oleae, A. nerii and S. oleae. This goes hand in hand with the study of Longo & Suma (2008), in italien olive groves, stated that the most common scale insect species are P. pollini, S. oleae, P. oleae and in restricted areas L. ulmi.
Finally, our manuscript presents a geographic distribution, generalized description of their biology, and damage of collected species. This checklist is therefore to be considered as a starting point for further investigation. Further investigations may reveal the presence of other species of scale insects on olive tree in some localities of Tunisia.

Conclusion
This present inventory on olive tree in North of Tunisia, allowed us to identify 22 species of scale insect belonging to 4 families and to 16 genera. Most of these species were found in very low numbers or were rare. Moreover, the olive producers generally did not consider scale insects as economic pests.
This list of species should be considered preliminary. Future investigations may probably reveal the presence of other scale insect species in many hard-to-reach locations. Additional studies are also needed to identify the exhaustive list of predators and parasitoids associated to these phytophages. Some species of scale insects have been encountered for the rst time on olive trees in Tunisia. Only four species could be considered as potential pests: P. pollini, P. oleae, A. nerii and S. oleae. A control program could be especially considered against these species.
Most cochineal species found in olive groves have a wide geographical distribution. The coastal regions characterized by a mild climate: Grand Tunis, Bizerte, and Cap Bon seem to be the most favorable areas for extensive biodiversity.

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