The entomofauna on Eucalyptus in Israel: A review

The fi rst successful Eucalyptus stands were planted in Israel in 1884. This tree genus, particularly E. camaldulensis, now covers approximately 11,000 ha and constitutes nearly 4% of all planted ornamental trees. Here we review and discuss the information available about indigenous and invasive species of insects that develop on Eucalyptus trees in Israel and the natural enemies of specifi c exotic insects of this tree. Sixty-two phytophagous species are recorded on this tree of which approximately 60% are indigenous. The largest group are the sap feeders, including both indigenous and invasive species, which are mostly found on irrigated trees, or in wetlands. The second largest group are wood feeders, polyphagous Coleoptera that form the dominant native group, developing in dying or dead wood. Most of the seventeen parasitoids associated with the ten invasive Eucalyptus-specifi c species were introduced as biocontrol agents in classical biological control projects. None of the polyphagous species recorded on Eucalyptus pose any threat to this tree. The most noxious invasive specifi c pests, the gall wasps (Eulophidae) and bronze bug (Thaumastocoris peregrinus), are well controlled by introduced parasitoids. Potential entomological hazards of Eucalyptus in Israel are most likely to originate from the Australian insect fauna.


INTRODUCTION
The fi rst Eucalyptus plants were brought from Australia to the West in 1770 (Doughty, 2000). The earliest eucalypt seeds that reached Israel (Palestine at that time) were those of the Tasmanian blue gum, Eucalyptus globulus Labill. Apparently none of these trees survived for long (Karschon, 1963). The fi rst successful Eucalyptus stands were planted in Israel in 1884 at the Mikveh Israel agricultural school (near Tel Aviv), probably consisting only of river red gum E. camaldulensis Dehnh. In the following years this species became the main Eucalyptus used in the fi rst large-scale plantations in Israel (Karschon, 1963). In the fi rst decades of Eucalyptus planting in Israel, its role in draining swamps proved important in the struggle against malaria (Rosen, 1991) which at that time posed a major challenge in southern Europe, particularly around the Mediterranean (Bruce-Chwatt & Zulueta, 1980). In the last years of the 19 th century 200,000 E. camaldulensis seedlings were planted in the Northern Sharon area (known as Hedera forest) to drain the local wetlands and manage the mosquito populations (Liphschitz & Biger, 2000). During those fi rst 30 years, Eucalyptus comprised about a third of forest nursery production; its timber was harvested for agriculture and telephone poles and railway sleepers (El-Eini, 1999;Liphschitz & Biger, 2000). Subsequently, Eucalyptus, mainly E. camaldulensis, was extensively RESULTS Sixty-two phytophagous species of insects have been found on Eucalyptus in Israel, about 60% of which are indigenous; the remaining originate from different areas and of which 16% are Australian species (Fig. 2). Table 1 summarizes the information about fi fty-two non-Eucalyptusspecifi c phytophagous insects occurring on Eucalyptus in Israel. None of these species are considered to be a major pest of this tree.
As expected, the insects living on Eucalyptus belong to different insect orders, with Hemiptera the major group and Coleoptera the second biggest group. Most of the Hemiptera are exotic, unlike the Coleoptera (Fig. 3).
Among feeding guilds, sap feeders constitute the largest group, followed by wood feeders (Fig. 4). Most of the insects were recorded from E. camaldulensis and it is very possible that those with no host record were also collected from this species of Eucalyptus. Few species were collected from several species of Eucalyptus and even fewer from species other than E. camaldulensis (Fig. 5). Table 2 summarizes the specifi c invasive insects recorded on Eucalyptus. All ten species originated from Australia and seven of them were established in Israel in 2000. Among the eight phytophagous insect orders colonizing Eucalyptus there were no exotic species of Lepidoptera, Orthoptera or Isoptera (Fig. 3). Table 3 lists seventeen parasitoid species associated with the invasive Eucalyptus-specifi c species. Two species, Rhoptrocentrus piceus (Braconidae) (Halperin, 1976) and Megastigmus leptocybus (Torymidae) (Doganlar, 2015) are indigenous to Israel. Seven of the ten specifi c Eucalyptus insect species recorded in Israel are attacked here by one or more of their specifi c parasitoids (Table 3).

DISCUSSION
In Israel, as in many other countries, Eucalyptus trees are valued for their rapid growth and capacity for adapting and Tunisia) which covers about 2.5 million ha. There is a lot of information about specifi c Australian invasive insects of Eucalyptus in the Mediterranean area (Kenis & Branco, 2010;Maatouf & Lumaret, 2012;Suma et al., 2018), but the presence of indigenous insects on Eucalyptus trees in these areas are rarely researched or reported.
Major threats to Eucalyptus plantations in Israel are posed by drought related to global warming, arson and invasive insect pests. By contrast, the overall damage to Eucalyptus in Israel caused by pathogens is limited and considered commercially insignifi cant. The present study reviews the information on the indigenous and alien invasive insects developing on Eucalyptus and their natural enemies in Israel.

SOURCES OF DATA
In this study, we processed and analysed both previous published records and the authors' observations over the last thirty years.   quickly to different climates. Generally, insect pests are not a major threat to Eucalyptus plantations in Israel. However, both invasive and indigenous species may become a problem in the future. Among the sixty-three phytophagous species of insects recorded so far on Eucalyptus in Israel, thirty-seven are native, twenty-six are invasive and ten of the latter are specifi c to Eucalyptus.

Sapsuckers
Indigenous and invasive species of sapsuckers form the dominant group of insects on Eucalyptus in Israel. They are mostly found on Eucalyptus growing as ornamental trees in irrigated gardens, wetlands and along streams, which continue to grow during the long warm dry season. There are only slight changes in the cambial activity of E. camaldulensis, even under different climatic conditions or during different seasons of the year (Waisel et al., 1966). Water availability and an appropriate temperature regime are the main factors inducing seasonal changes in cambial activity (Kozlowski et al., 1991;Whitehead & Beadle, 2004). This may well account for the long growth period of Eucalyptus trees growing where the supply of water is adequate during the dry season and their suitability for sap-suckers. In Israel, most of the sapsuckers are practically absent in planted forests where the trees only experience a short rainy season and consequently can only grow for a short period of time. Two of the Eucalyptus-specifi c sapsuckers, Glycaspis brimblecombei Moore and to a lesser extent Thaumastocoris peregrinus Carpintero and Dellapé are nevertheless still frequently recorded in forest plantations in the Northern and central areas in Israel (but see below for more about their biological control and pest status). The sapsuckers include six species of thrips, none of which are considered to be signifi cant pests of Eucalyptus. Three are native; the invasive Thrips australis Bagnall (see below) is specifi c to Eucalyptus; Heliothrips haemorrhoidalis (Bouché) and Retithrips syriacus Mayet are minor pests of fruit trees.
The scale insects (10 species), thrips (5 species), aphids (4 species) and planthoppers (1 species) not specifi c to Eucalyptus (Table 1) are pests of many agricultural crops. However, their low frequency of occurrence on Eucalyptus indicate that these trees are not an important refuge for them or a signifi cant source of these pests for agriculture. While the Hemiptera on Eucalyptus might constitute a refuge for their natural enemies, this possibility has yet to be studied.

Stem borers
Coleoptera form the second largest group of Eucalyptus insects in Israel and includes the highest number of indigenous species. Most of the species are woodborers, which are polyphagous and develop in the dying or dead wood of Eucalyptus trees. Together with two termite species (Table 1), these wood feeders are common in Eucalyptus plantations, where they exploit an abundance of dying and dead wood. The invasive borers Phoracantha semipunctata (Fabricius) and P. recurva Newman occur in many other countries (Paine et al., 2010). Both borers are very common in Israel (Golan, 2011) and other Mediterranean countries (Rassati et al., 2016). The frequent occurrence of these borers is due to the abundance of reproductive substrate in the form of trees dying due to drought or forest   fi res, or fallen branches, the latter are frequently found beneath large Eucalyptus trees growing on wet sites. Neither these borers are primary pests of Eucalyptus in Israel and thus may serve as indicators of the physiological condition of the trees. There are many fi eld studies on the resistance of Eucalyptus to Phoracantha (mainly P. semipunctata) (Chararas, 1969;Hanks et al., 1995), which indicate that the trees become susceptible to attack by these borers when they fail to cope with harsh environmental conditions, mainly as a result of drought. Dying Eucalyptus trees and dead wood are a refuge for polyphagous borers, e.g. the bostrichid Apate monachus Fabricius, which may switch to attack live trees of other genera, or the powder posts beet les Lyctus spp. and Stromatium fulvum Villers that damage timber and wood products. Generally, native Australian coleopteran borers have not become signifi cant pests of Eucalyptus trees. However, a rather rich fauna of bark and ambrosia beetles have adapted to develop in Eucalyptus plantations in Brazil (Flechtmann et al., 2001), where many of these beetles are polyphagous and generalists, which is typical of many tropical species of scolytids. Lombardero and Fernández De Ana Magán (1997) (Gebeyehu et al., 2005) are serious pests of Eucalyptus in those areas. Eucalyptus trees are also frequently planted in deserts in the Northern Hemisphere (Teketay, 2000;Jeddi et al., 2009). Despite the fact that the Mediterranean is rich in species of cossids (Yakovlev & Dubatolov, 2013), there are no records of carpenter worms from Eucalyptus in this area. This is probably due to the absence of species of Myrtaceae that could serve as a source of species of cossids that could then develop on

Defoliators and Scarabaeidae
The defoliators form the third largest group with thirteen species, all of which are native. The eight species of Lepidoptera form the second largest taxonomic group of native species. None of the defoliators are serious pests of Eucalyptus in Israel and few are considered important pests of other crops. Minor damage caused by the weevil Achradidius milleri (Boheman) and a leaf cutting bee Megachile sp. to recently planted Eucalyptus in the Coastal Plain soon after planting in the Western Negev is reported by Halperin (1961aHalperin ( , 1973. Megachile spp. observed in late spring, during the nesting period of the bees, may also have caused some damage to young trees soon after planting (Halperin, 1961b). Two other native defoliators, the Moroccan locust Dociostaurus maroccanus (Thunberg) and the cypress false silk moth, Pachypasa otus (Drury), are considered minor pests in Eucalyptus stands in dry areas in Israel. Rarely, local small outbreaks of the Moroccan locust may affect pockets of Eucalyptus trees planted in the Jordan Valley. The locusts are attracted to these trees, which are planted in earthen constructions that collect fl oodwater by damming a gully or streambed along the roads. In this area, these trees are the sole green vegetation remaining during the summer months. The native area of the cypress false silk moth P. otus is between Italy, Armenia and Iran, with different tree hosts in the different environments (Battisti et al., 2016). In Israel, although Cupressus sempervirens L. is the main host it develops on Eucalyptus in semi-desert areas. The defoliation due P. otus often remains unnoticed. However, when the mature larvae descend in great numbers prior to pupation, they may cause public concern due to the sensitivity of some people to the urticating hairs that are on the fi rst abdominal segment of the last instar (Battisti et al., 2016). Mansfi eld (2016) indicates that among the native colonizers, leaf chewers in particular, quickly colonize Eucalyptus trees. In Israel, aside from D. maroccanus and P. otus, other local defoliators are rarely found on Eucalyptus. There is only a single record of Lymantria dispar (L.) on E. camaldulensis in Hadera (central Coastal Plain of Israel). Rare outbreaks of this gypsy moth are reported here

Australian insects specifi c to Eucalyptus
Ten species of Australian insects specifi c to Eucalyptus are presently established in Israel. Most if not all occur in other Mediterranean countries and in other Eucalyptusgrowing countries in the Americas and south Asia. Thrips australis was probably the fi rst of this group to become established in this area. It is found both in Israel and elsewhere on many different plants and its females oviposit primarily on the white fl owers of various Eucalyptus species (Mound & Masumoto, 2005). Until 2000 P. semipunctata was the best known Eucalyptus insect in Israel; it was unintentionally introduced from South Africa on shipments of Eucalyptus wood used for fortifi cations during the early 1940s (Bytinski-Salz, 1966). During the last two decades, eight other species became established in this country.  (Protasov et al., 2007a) and T. australis (Mound & Masumoto, 2005). Similarly, while it is possible that Q. nova might develop on other genetically closely related congeners of E. camaldulensis, in reality, only P. semipunctata and P. recurva thrive on various Eucalyptus species growing in Israel. All other species mentioned above have been observed only on E. camaldulensis, including L. invasa and O. maskelli after the establishment of their natural enemies (Mendel et al., 2017).

Management and natural enemies
In Israel, the management practices adopted, including chemical control and biological control, were directed against several species of the Eucalyptus-specifi c insects. The fi rst management action was undertaken in the fi rst half of the 20 th century and aimed at preventing the damage caused by P. semipunctata to telephone poles, which were then made of Eucalyptus trunks. To prevent damage by boring and powder post beetles (Lyctinae) the poles were impregnated with zinc chloride (Neumark, 1953). Later, a technique to protect fresh support poles made of Eucalyptus from damage by P. semipunctata was developed and extensively applied during the 1960s in fruit plantations in Israel. It consisted of spraying a 0.5% solution of lindane in a gasoil, which proved highly effective in eliminating or minimizing damage by borers (Chudnoff & Spetter, 1962). Phoracantha semipunctata was the fi rst of the Eucalyptus pests for which classical biological control was used. Of the several species of parasitoids that were sent from Australia to Israel in 1982, three braconids, Syngaster lepidus Brullé, Jarra phoracantha Marsh & Austin and Liodoryctes sp., were released (Mendel et al., 1984b). Some of the most effi cient Australian natural enemies fortuitously arrived and became established in Israel. Phoracantha recurva spread in the Mediterranean with its egg parasitoid Avetianella longoi Siscaro which was fi rst reported in the central Mediterranean parasitizing P. semipunctata (Ben Jamaa & Dhahri, 2009;Longo et al., 1993). This wasp attacks the eggs of P. semipunctata (Luhring et al., 2004) more effectively than those of P. recurva. In Israel, it is frequently recovered from eggs of both Phoracantha species, with no apparent effect on their population density (Golan, 2011). Similarly, to what happened in other countries in the Mediterranean area, Psyllaephagus bliteus Riek establishment followed the arrival of Glycaspis brimblecombei Moore (Laudonia & Garonna, 2010;Boavia et al., 2016;Mendel et al., 2017). Megastigmus zebrinus Grissell was recorded recently together with its gall wasp host Q. nova (Mendel & Protasov, in prep.) but the time of their establishment is unknown. The list of parasitoids and the year of their initial discovery, or recovery in Israel, is detailed in Table 3. In general, native insect enemies have switched to attacking the Australian insects that develop on Eucalyptus in Israel, but usually their role in regulating their numbers is insignifi cant. Generalist predators that typically prey on aphids and scale insects are frequently found in colonies of G. brimblecombei in Israel (Protasov et al., in prep.) and other areas (Erbilgin et al., 2004;Laudonia & Garonna, 2010). Megastigmus leptocybus, a local parasitoid has become fortuitously associated with L. invasa galls, but its rate of occurrence is low and it occurs in only one area in Israel (Protasov et al., 2008). Native Megastigmus spp. are frequently recovered from galls of L. invasa in almost every country where this insect has become established (Doganlar, 2015). Mendel et al. (1984a) report that the Syrian woodpecker is an important predator of larvae of P. semipunctata and P. recurva. Golan (2011) reports high levels of predation of adults of the latter borer by bats and aggregation of the adult borers on Eucalyptus trap trees.
To date, nine of the ten Eucalyptus-specifi c phytophagous insects are not considered signifi cant pests of live trees. Both Phoracantha spp. are reported as secondary pests developing on dying trees, or cut timber. The psyllids, B. occidentalis and P. biemani, the thrips T. australis and the gall wasp O. nova, occur at very low densities and are usually undetectable. The two gall wasps O. maskelli and L. invasa, and the bronze bug T. peregrinus are controlled by introduced parasitoids. The red gum psyllid G. brimblecombei is still a nuisance on ornamental E. camaldulensis trees, as the level of parasitism is less than 5%, probably due to unfavourable climatic conditions during the main period of activity of the psyllid (Protasov et al., in prep.). Psyllaephagus bliteus was introduced into California in 2000 for the control of G. brimblecombei (Daane et al., 2005) and became established in Europe as a fortuitous biological control agent (Caleca et al., 2011;Perez et al., 2011). While in some tropical areas parasitism may be > 90% (Filho et al., 2015), in the Mediterranean area P. bliteus has a minor role in regulating psyllid populations. Therefore, the biological control provided by P. bliteus is not suffi cient to prevent outbreaks of G. brimblecombei (Daane et al., 2012;Boavia et al., 2016;Margiotta et al., 2017).

Other Eucalyptus-specifi c species in the Mediterranean
Six other insects specifi c to Eucalyptus occur in the Mediterranean, but not in Israel. The potential hazard associated with these species is limited as they do not, or rarely attack the species planted here. Ctenarytaina eucalypti (Maskell) (Hemiptera: Aphalaridae) is narrowly hostspecifi c, feeding only on a limited range of Eucalyptus spp. that originate from temperate Australia and Tasmania, and is unsuited to a warm Mediterranean climate. However, in Italy it was recorded in 1982 and was for almost 20 years the only psyllid species known to develop on Eucalyptus spp. (Suma et al., 2018). The parasitoid Psyllaephagus pilosus Noyes appears specifi c to C. eucalypti and was successfully introduced into California and Europe (Hodkinson, 1999). Ctenarytaina spatulata has been present in Europe since 2003 (Valente et al., 2004). Its favoured host trees are not common in Israel and its performance on E. camaldulensis is poor (Queiroz et al., 2010). Two species of Eucalyptus snout beetles occur in Europe. One of them, Gonipterus platensis Marelli is present on the Iberian Peninsula, where it mainly attacks E. globulus (Gonçalves et al., 2019) (an uncommon tree in Israel) and is well controlled by the egg parasitoid Anaphes nitens (Girault) in a warm Mediterranean climate (Valente et al., 2018 (Franco et al., 2016); C. citriodora is a common Table 3. Parasitoids (Hymenoptera) of invasive specifi c phytophagous insects on Eucalyptus camaldulensis* that were established in Israel by classical or fortuitous biological control ("a" indicates the year of discovery of both native and non-native species, "n" refers to native species, "b" indicates the year of recovery of the introduced species). * For more details see Table 2. ** Develops in various cerambycids. *** Recovery was recorded once, establishment was not confi rmed. **** Not the original host.
ornamental tree in Israel. The third eulophid is Leprosa milga Kim & La Salle, a seed gall inducer found in 2006 in Apulia, Italy (De Marzo, 2008).

Shift of local insects to Eucalyptus and Eucalyptus-specifi c species to local vegetation
Morphological classifi cations and molecular phylogenies suggest that the Myrtaceae family originated in Gondwana and most of its members naturally occur in the Southern Hemisphere and India (Thornhill et al., 2015). Native insects that have become pests on Eucalyptus outside Australia are generally either highly polyphagous, or have native Myrtaceae as their natural hosts. Insects in the latter group may be preadapted to shift to eucalypts as hosts (Paine et al., 2011). Brandle et al. (2008) suggest that after introduction the number of native species colonizing exotic plant species increases with time. However, as in California (Paine et al., 2011), the switch of a native herbivorous insect to becoming a serious pest of Eucalyptus in Israel is unlikely. Branco et al. (2015) examined 590 colonizations by native insects of exotic trees in Europe. These authors suggest that cases of major damage were positively correlated with the geographical extent of the exotic trees and the presence of congeneric native trees. The only Myrtaceae occurring in the Mediterranean basin are three Myrtus spp. that occur in the Mediterranean region of southern Europe, the Saharan mountains and Iran (Johnson & Briggs, 1981), none of which naturally occur in Israel. There is no information on the insect fauna of Myrtus communis, the most common native member of Myrtaceae in the Mediterranean area. About 12 insect species are listed on M. communis in Israel, including scale insects (7 species), thrips, aphids and whitefl ies (Avidov & Harpaz, 1969;Y. Gottlieb, pers. commun.), all of which are polyphagous and most of them were also recorded on E. camaldulensis in our survey. None of the ten invasive species of insects specifi c to Eucalyptus (Table 2) are recorded occurring on M. communis in Israel. Furthermore, to the best of our knowledge, none of the specifi c phytophagous insects on Eucalyptus occur on members of tree genera other than Eucalyptus sensu lato in other areas. None of the Eucalyptus-specifi c species pose a threat to these trees in Israel, while the most noxious invasive species are well controlled by introduced parasitoids. Although the indigenous Australian insect fauna may constitute a potential threat to Eucalyptus in Israel, our experience suggests that their abundance can be controlled by the introduction of their specifi c natural enemies.