Two of the Most Promising Potential Agents from Kazakhstan for the Biocontrol of Russian Olive (Elaeagnus angustifolia) in the USA with an Annotated List of Its Pest Insects from Central Asia

Abstract

Two of the most studied species, monophage Trioza magnisetoza Loginova, 1964 (Hemiptera, Triozidae) and narrow oligophage Altica ballasogloi (Jakobson, 1892) (Coleoptera, Chrysomelidae), are offered for biological control of Russian olive (Elaeagnus angustifolia) in the USA. The data obtained over 15 years and presented in this publication on biological and ecological features, host plants, damage to the host plants, and suggested approaches for establishing new populations of both species are sufficient for their use in biological control in North America. Currently, 72 species of insects from 58 genera, 33 families, and six orders are known in Central Asia as pests of Russian olive. The most numerous are insects from the order Coleoptera (36 species, 29 genera, 10 families), Homoptera (14 species, eight genera, six families), and Lepidoptera (13 species from 12 genera, 10 families). Twenty-four species from this list, including eight species of monophages and 16 species of oligophages, are the most suitable for biological control of Russian olive. In addition, six other species of insect pests with unexplored food specialization but associated with Russian olive might also be used.

1. Introduction

The genus Elaeagnus L. (Elaeagnaceae) (common names:—silver berry, Russian olive (oleaster), Persian olive in English;—Lokh in Russian,—Zhide, Zhiyde, Dzhida, or Dzhigida in Kazakh, Uzbek, Kyrgyz, and other Turkic local languages) consists of about 80 species native to Southern Europe, Western, Central, and Southeast Asia, as well as North America; the center of origin of the genus is considered to be Southeast Asia [1]. Currently, there is information on the growth of 3 species of Elaeagnus in Kazakhstan [2]: of them E. oxycarpa Schlecht. and E. angustifolia L. are indigenous, and E. orientalis L. was introduced probably from Transcaucasia and Turkey. All three species are widely cultivated by the local population as hedges, for fixing sand, riverbanks, and canals, as well as for landscaping arid areas and creating shelterbelts. One of these three species, Russian olive E. angustifolia has a very wide range and is distributed in the countries of the Mediterranean, Western, Central, and Eastern Europe, Western Siberia, Asia Minor, the Caucasus, Iran, Northern India, Central Asia, Western China (Xinjiang), and Mongolia. In addition, Russian olive was introduced into North America. It has been the subject of biological control research in the United States for almost 50 years. The 6th volume of “Flora of Kazakhstan” [3] provided information on only two species of Elaeagnus (E. oxycarpa and E. turcomanica) known from Kazakhstan. Moreover, in the essay on E. oxycarpa, the Russian olive (E. angustifolia) is mentioned only as a cultivated plant, known mainly in Europe. In this regard, it is necessary to conduct thorough studies on the systematics of all species of Elaeagnus observed in Kazakhstan, including molecular studies of Russian olive and other species biotypes from Kazakhstan and the United States. First, this applies to biotypes of closely related species of E. angustifolia and E. oxycarpa.

This publication aims to present the results of our research on insect species that damage Russian olive in the natural areas of its growth in Kazakhstan and other parts of Central Asia. Our work in Russian olive biocontrol studies began in 2006 with two research goals: (1) to find effective biological control agents of Russian olive in Kazakhstan and (2) to study their biological features under natural conditions. Conducted research shows that Altica balassogloi (Coleoptera, Chrysomelidae) and Trioza magnisetosa (Hemiptera, Triozidae) are the most preferable potential Russian olive biocontrol agents for introduction into the USA. The analyzed information and original observations and experiments on distribution, habitats, host plants, biological and phenological characteristics, parasites, and effectiveness for biological control and testing in natural conditions for both species are presented in this publication.

The first publications on insect species that damage Russian olive in its native habitat of Central Asia appeared in the middle of the 20th century. The reference book “Pest animals of Central Asia” [4] (1949) lists 20 species of insects living on Elaeagnus. The biological and environmental features of cerambycid, Chlorophorus varius—which damages Elaeagnus in Western Kazakhstan, have been studied fairly well [5,6,7]. Eulecanium (Parthenolecanium) persicae and Diaspidiotus elaeagni (Diaspididae), Xylotrechus grumi (asellus), X. namanganensis, Turanium scabrum (Cerambycidae) and others [8,9] were also found as pests of Russian olive, which grows in protective forest belts of Uzbekistan and Southern Kazakhstan. Around the same time, in Naryn Sands in Western Kazakhstan [10] and in South and Southeast Kazakhstan [11,12,13,14,15,16], other pests of Russian olive were also found: Trioza magnisetosa (Triozidae), Capitophorus hippophaes (Aphididae), Lepidosaphes turanica (Diaspididae), Tropinota (Epicometis) hirta (Scarabaeidae), Molorchus kiesenwetteri, Tetrops elaeagni, Chlorophorus elaeagni (Cerambycidae), Scolytus jaroschewskii (Scolytidae), Argyroploce lutozana (Torticidae), Ananarsia elaeagnella (Gelechiidae), and others. Quite complete reviews of the pests of the Elaeagnus were given by Mityaev I.D. [15] for Kazakhstan and Sinadsky Yu. V. [17] for Central Asia. Based on these and some other publications [11,17,18,19,20,21,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47], we have compiled a preliminary list of 72 species of insects that damage Russian olive and live in the Central Asian region. Brief characteristics of these species are given below in a separate section.

2. Materials and Methods

The research material is the results of observations, collections, and testing, which took place in the field seasons of 2006–2013 in the Southern Balkhash region (the valleys of the Ili, Karatal, Lepsy rivers), as well as in Almaty on the grounds of the Institute of Zoology of the Republic of Kazakhstan and the adjacent area of the Main Botanical Garden. In subsequent years (2013–2022), only phenological observations on Russian olive psyllid Triosa magnisetosa and cerambycid Altica balassogloi were carried out, and the state of populations of both species was assessed at previously selected monitoring sites. From mid-June 2006 to 2013, special exploratory studies were conducted in the Ili Valley and the lower reaches of the Lepsy River to detect modern habitats of Russian olive psyllid, Triosa magnisetosa, and the cerambycid, Altica balassogloi. In 2007, for the same purposes, the Karatal River valley and the Ili River’s lower reaches were examined, and monitoring observations of the state of already discovered populations in the Ili River Valley were carried out. In 2008 and subsequent years, observations continued at monitoring sites of the Ili and Karatal river valleys to study the biological and phenological characteristics of these insects, and from 2008 to 2014, insects were tested on experimental Elaeagnus trees in the vicinity of Almaty and the territories adjacent to the Institute of Zoology RK. In total, six Altica balassogloi populations and one large Trioza magnisetosa population were selected for research, the location of them is shown in Figure 1. During the studies, classical entomological techniques were used for searching, collecting, fixing, observing, and testing insects for host plant specialization [48]. To test both species to assess their nutrition on other plants, a certain number of eggs, larvae or adult insects were planted on other potential host plants in natural habitats. In addition, in 2008–2012, we worked out a methodology for establishing new colonies of both species by releasing adult insects on other Russian olive plants near Almaty.

This research on various noxious weeds from Central Asia (often considered native there) and their natural enemies was collected in the field to determine host range, then tested in cages overseas, and then shipped to labs in the U.S. for final testing.

3. Results

As a result of our research in Kazakhstan, we suggest two species as the preferential potential Russian olive biocontrol agents for introduction into the U.S. First, Altica balassogloi (Coleoptera, Chrysomelidae), which damages foliage and shoots and is distributed in South and Southeastern Kazakhstan (Arys, Ili, Karatal, and Charyn rivers riparian forests). Second, Trioza magnisetosa (Homoptera, Triozidae), which usually damages foliage on young trees and is distributed in south, central, and west Kazakhstan. It should be noted that over the past 15 years, in Southeast Kazakhstan, general warming of the climate and uneven seasonal precipitation have been observed. Winters were not snowy, and early springs, sometimes with April frosts, led to the death of buds, especially on young plants. For example, in 2007, sharp warming occurred already in the third decade of March, with heavy rainfall until mid-June and hot, arid summers and autumn. The years 2008 and 2015 turned out to be mainly arid when drought almost throughout the entire growing season covered not only deserts and piedmont steppes but also the lower zones of the mountains, and the burnout of the vegetation reached its maximum in July and early August. Such unusual weather conditions determined phenological shifts in the development of insects not only by year but even among different populations during one growing season.

3.1. Trioza Magnisetosa Loginova, 1964

Oleaster jumping plant lice, or Russian olive psyllid, is one of 23 species of the genus Trioza known in Kazakhstan (more than 300 species worldwide).

3.1.1. Distribution

Species is known in Romania; Ukraine [48]; Russia: Central and East-European area [49,50], South-European area (environs of Baskunchak Lake, Astrakhan region) [51]; Georgia [52,53] and Armenia [50,52]; Turkey [54,55,56]; Iran [57,58,59]; Kyrgyzstan; Uzbekistan; Tajikistan [51]; China: Shaanxi, Xinjiang, Gansu, Hebei [59]. In Kazakhstan, these jumping plant lice are widely distributed in the southern half of West Kazakhstan as well as in Central and South Kazakhstan [15,16,24,60,61]; some small populations were also found in the southern portion of East Kazakhstan [62] and in the vicinity of Almaty City. For the first time in the South Balkhash Lake region, we discovered some large populations of these jumping plant lice in June 2006 in the environs of Zhelturanga Town and Topar Town in the lower reaches of the Ili River.

3.1.2. Habitats

This species usually inhabits the lower reaches of the rivers at an altitude of 400–500 m above sea level, although in Tajikistan, sometimes it rises along river channels to 2500 m above sea level [51]. It prefers to settle on Russian olive, which grows in dry areas of the floodplain or in sandy, desert, and dry steppe floodplain terraces. An indication of the occurrence of Trioza magnisetoza on the needles of Picea shrenkiana in the mid-mountain belt of the Ketmen ridge (Southeastern Kazakhstan) at an altitude of 1920–2220 m above sea level [6] is erroneous, since earlier we observed some phenomena of wind introducing flying adults (during swarming) into the mountains on various random plants. In the Southern Balkhash region, the populations we discovered lived in the lower reaches of the Ili River in a grove dominated by Russian olive and Turanga (Populus diversifolia) inside a small inter-dune basin, where psyllids were found in large numbers on young and middle-aged trees of Russian olive (near the Zhelturanga Town) and in the grove along the edges of the dunes (surrounding Topar Town).

3.1.3. Host Plants

Trioza magnisetosa is a monophagous species on Elaeagnus angustifolia and appears to be one of the most promising biological agents of Russian olive in the US. The results of our many years of field observations and repeated attempts in 2008–2012 to transplant insects to other plant species in natural habitats for feeding showed a strict connection between this species and the Russian olive as a host plant. The host range tests in 2012–2013 conducted in laboratory conditions of the Institute of Zoology of the Republic of Kazakhstan also confirmed the monophagy of this psyllid species. Information about feeding this psyllid on Rhamnus L. (Rhamnaceae) [63] refers to the introduction of insects on alien random plants and requires clarification.

3.1.4. Biological and Phenological Features

Wintering. Winged adults of oleaster jumping plant lice overwinter in large clusters in the litter under leaves of Elaeagnus angustifolia; a small part of these insects is located in the upper layers of the soil. Often some concentrations of overwintering psyllids are observed near trunks.

Moving from the wintering places and copulation. Moving the winged adults from the wintering places in conditions of the South Balkhash Lake region occurs at the beginning or the end of April–the beginning of May; this depends on the weather conditions of spring and the presence of developed buds on the host plant. In more southern regions, moving from wintering places was observed in early/late March–early April [15], and it is associated with the appearance of buds on the Russian olive. Immediately after leaving the wintering sites, the psyllids move to the branches of oleaster and begin to feed first on the buds and then on the leaves and young shoots. The females opened at this time had no eggs at all in the oviducts. Only after a period of additional nutrition, which is necessary for the accumulation of fat reserves and maturation of eggs, do the adults begin to copulate, and then females begin to lay eggs. Additional nutrition occurs first on the buds (the end of April–May) and then on young shoots and leaves (the end of May–June).

Egg-laying. Females begin laying their eggs in mid-May, and through the end of mid-June, the bulk of egg laying occurs in late May–early June. The eggs are laid by jumping plant lice on the underside of the leaf. Eggs are about 0.40–0.45 mm long, smooth and oval, but pointed at one end and blunt on the other end. The pointed half of the egg becomes transparent 4–6 days after laying and faces the upper side of the leaf. On the contrary, the blunted half of the egg is covered with radiating leaf scales. Egg clutches are usually single, rarely double. The number of eggs laid on a single leaf varies greatly and depends on the abundance of females on the tree. In the South Balkhash Lake region, 20 to 30 eggs were found on one leaf, although up to 40 eggs were observed on some individual leaves. At the same time, in more northern populations with a small number of insects, clutches of 2–3 or 6–11 eggs are often laid on the leaves, depending on the population density [15]. The fertility of a single female can reach 450 eggs, as was also shown by other researchers [64]. At the place where the egg is laid, small bumps appear on the upper side of the leaf, which can easily be used to calculate the population of the leaves with eggs. The embryonic period lasts 14 to 17 days.

The development cycle then passes through five larval instars, which have a light gray with a silvery tinge that is not distinguishable in color from the leaves of Russian olive. Wing covers and complex facet eyes appear already in first-instar larvae and persist in all other instars; the larvae grow in size from age to age, so often the larval stages are referred to as nymphs of the 1st–5th age. The emergence of first-instar larvae from eggs was observed in the third decade of May. First, they stick to the lower side of the leaf and then migrate to the upper surface, spreading along the central and lateral veins of the leaf or sometimes sticking to the leaf petioles. With a high population density, there were an average of about 60 larvae per leaf. With a low population, the larvae are concentrated in groups of 6–9 individuals, and with mass reproduction, the psyllid larvae cover the entire leaf with a continuous layer on both sides.

Emerging and flight of the first-generation adults in the southern Balkhash region are observed at the end of the second decade of June. After emerging, adults almost immediately start feeding on leaves and copulating. During mass flying and with a large number of insects in the population, adults sometimes form flying clusters (swarms) that can be carried a considerable distance by the wind. This is how the population of jumping plant lice came to settle on uninfested Russian olive trees. Oviposition occurs from the end of the second decade to the beginning of the third decade of June until about the middle of July. The eggs are laid singly or in groups on the lower side of the leaf. After an embryonic period lasting about 2 weeks, the first-instar larvae emerge; these larvae first start feeding on the lower side of the leaves and then move to the leaf’s upper side and on the leaf petioles. The larvae grow and increase in size, passing through five instars.

Emerging and swarming of second-generation adults is observed in the southern Balkhash region in late July–early August. After additional feeding, the adult psyllids begin to copulate, and the females start laying eggs on the leaves. The entire cycle of development of the second generation ends by mid-September, when the third-generation adults appear, adults begin to feed sluggishly, and when the temperature drops, they gather in groups on the surface and the upper layers of the soil for subsequent overwintering.

During the year, three generations of psyllids usually develop in the southern Balkhash region and the more southern regions of Central Asia [51]. However, in 2008, due to severe drought, and in 2009, due to relatively cold weather conditions in the summer, we noted the development of only two generations of insects here (see

Table 1. Life cycle of Triosa magnisetosa in the southern Balkhash region.

Months
IV			V			VI			VII			VIII			IX			X-XII-I-III
Decades			Decades			Decades			Decades			Decades			Decades
1	2	3	1	2	3	1	2	3	1	2	3	1	2	3	1	2	3
Normal Spring
3 generation (overwintered adults)							1generation (adults)					2 generation (adults)					3 generation (overwintered adults)
W	W	W																W
	♂	♂	♂	♂	♂	♂	♂	♂	♂	♂	♂	♂	♂	♂	♂	♂	♂
	♀	♀	♀	♀	♀	♀	♀	♀	♀	♀	♀	♀	♀	♀	♀	♀	♀
			◎	◎	◎	◎	◎	◎	◎	◎	◎	◎	◎	◎
				oo	oo	oo		oo	oo	oo		oo	oo	oo
					L1	L1			L1	L1			L1	L1
					L2	L2			L2	L2			L2	L2
						L3	L3			L3	L3			L3	L3
						L4	L4			L4	L4			L4	L4
							L5	L5			L5	L5			L5	L5

Notes: W—wintering adults on the ground; ♂—male; ♀—female (adults moving and, on a tree); ◎—copulation; oo—eggs; L₁—first-instar larva, L₂—second-instar larva, L₃—third-instar larva, L₄—fourth-instar larva, L₅—fifth-instar larva.

).

3.1.5. Parasites

Tetrastichus sp. (Chalcidoidea, Eulophidae) and mites of the family Trombidiidae are parasitic on the larvae of psyllids.

3.1.6. Efficiency for Biological Control

Larvae of Russian olive psyllid (especially larvae of the last instars) cause the formation of chlorotic spots and bending and twisting of leaves. Such leaves turn yellow before time and fall off. Adults do not cause any externally noticeable harm, even with a significant population. The most incredible damage occurs during the mass reproduction of psyllids when the nymphs cover not only the leaves with a continuous layer but also their petioles and even the tips of young shoots. In this case, most Russian olive trees lose more than 50% of their foliage, and some lose it completely, which has been repeatedly described in the literature [10,15,24,64]. We observed such mass reproduction of the Russian olive psyllid population in the southern Balkhash Lake region only once in 2006. Unfortunately, during our observations in 2007–2018, we did not find mass population outbreaks in the following years, although changes in the normal development of Russian olive in these years were noted. Partial or complete loss of leaves in mid-summer and intense poisoning by saliva released by nymphs when sucking disrupt the normal development of trees, leading to severe oppression and slowing of growth rate. All this, together with other adverse factors (progressive salinization, excessive waterlogging of the soil, or conversely, a lack of ground moisture), usually leads to poor overwintering of plants, even to their death in the winter or spring periods. Thus, the Russian olive psyllid, without causing any noticeable harm to the plant in small populations, is an effective control agent over years in places of high population.

3.1.7. Testing in Nature

Five tests were conducted in natural areas of Kazakhstan to develop new colonies of Russian olive psyllids. Tests were made in 2007 and 2008, none of which were established.

Test 1 (Mid–June 2007). In mid-June 2007, more than a hundred adult individuals from the vicinity of Topar town were tested on a medium-aged Russian olive bush in the vicinity of Almaty (the test failed to establish).

Test 2 (Mid–June 2007). Three hundred adult individuals were released on a young and relatively small Russian olive tree near Avat Town (50 km east of Almaty) on the bank of an irrigation channel. However, for unclear reasons, no psyllids survived in either location (tests 1 and 2).

Test 3 (2008). A new attempt was made to plant large groups (more than 300 individuals in each group) of Russian olive psyllids from the Topar population on two Russian olive trees (young and middle-aged) near Avat Town, but it also failed.

Test 4 (2009). Attempts were made to plant more than 300 psyllids of the Topar population on a healthy and young oleaster tree near Avat Town, which was initially successful.

Test 5 (2010). Three hundred more psyllids were released on a medium-aged tree in the Ili River floodplain near Bakanas City, which was initially successful.

In tests 4 and 5, where newly emerged adults were collected in one location and transferred to young, healthy Russian olive trees in a different location, adults fed and copulated and showed signs of successful establishment. However, in 2014 these populations disappeared due to a fire in the floodplain of the Ili River and construction work in the vicinity of the Avat Town.

Unfortunately, our monitoring studies in 2019 showed that both oleaster jumping plant lice populations found in 2006 in the lower reaches of the Ili River also disappeared as a result of anthropogenic influence: in 2018, the population died in the vicinity of Zhelturanga, and in 2019 in the vicinity of Topar towns. The main reasons for the death of populations are strong overgrazing and artificial fires, which are arranged by local residents. Overgrazing completely destroyed the layer of fallen leaves and mixed it with sand so that the psyllids’ wintering sites were completely destroyed so that adult psyllids had no place to winter. To continue research, it is necessary to find new large populations of Russian olive psyllids both in the southern Balkhash region and southern Kazakhstan.

In general, our experiments have shown the possibility of establishing artificial populations of psyllids on new and healthy young Russian olives by transferring feeding and copulating jumping plant lice to lay eggs on a new plant. The main threat to population establishment and maintenance is anthropogenic disruption of the site.

3.2. Altica Balassogloi (Jakobson, 1892) Coleoptera, Chrysomelidae (=Haltica Suvorovi Ogl., H. Lopatini Pal.)

The Russian olive (oleaster) leaf beetle represents a large genus of about 250 species and a worldwide distribution. There are 15 known species in Central Asia, including Kazakhstan [65].

3.2.1. Distribution

South and Southeast Kazakhstan, Uzbekistan, Kyrgyzstan, Tajikistan [30].

3.2.2. Habitats

It is a floodplain forest species throughout its range. In the southern Balkhash region, this species lives in floodplain forests of the Ili, Charyn, Karatal, and Lepsy rivers and sometimes enters the mountain floodplain forest at 2000–2500 m above sea level.

3.2.3. Host Plants

It is the oligophage of Elaeagnus spp. and sea-buckthorn (Hippophae rhamnoides), most commonly found on oleasters growing along rivers.

3.2.4. Biological and Phenological Features

There are two generations per year (see

Table 2. Life cycle of Altica balassogloi in the southern Balkhash region.

Months
IV			V			VI			VII			VIII			IX			X-XII-I-III
Decades			Decades			Decades			Decades			Decades			Decades
1	2	3	1	2	3	1	2	3	1	2	3	1	2	3	1	2	3
Normal Spring
W	W	W													W	W	W	W
		♂	♂	♂				♂	♂					♂	♂
		♀	♀	♀				♀	♀					♀	♀
			◎	◎					◎	◎
			oo	oo					oo	oo
				L1	L1					L1	L1
					L2	L2					L2	L2
						L3	L3					L3	L3
							P	P					P	P
Earlier Warm Spring
W															W	W	W	W
♂	♂	♂	♂	♂		♂	♂	♂	♂				♂	♂
♀	♀	♀	♀	♀		♀	♀	♀	♀				♀	♀
		◎	◎					◎	◎
		oo	oo	oo				oo	oo
			L1	L1	L1				L1	L1	L1
				L2	L2	L2				L2	L2	L2
					L3	L3	L3				L3	L3	L3
						P	P	P				P	P

Notes: W—wintering adults on the ground/under bark; ♂—male; ♀—female (adults moving and on a tree); ◎—copulation; oo—eggs; L₁—first-instar larva, L₂—second-instar larva, L₃—third-instar larva; P—pupa.

).

Adults of the second generation are in the over-wintering stage; beetles are located singly or in groups under the peeling bark of Russian olive, as well as in deep cracks in the bark and in the litter. There have been cases of beetles wintering under the bark of old large-stemmed willow trees (Salix). In the spring, with the onset of warm days, the beetles leave the wintering areas and are located on the trunk and branches of Russian olive, usually in mid-April or early May, although there are cases of both early, at the end of the first decade of April [66], and very late appearing on new buds and young leaves, and with a decrease in temperature in the evening, they go to the litter under the oleaster or hide under the bark and in its cracks.

Egg laying in normal weather conditions in Southeastern Kazakhstan begins at the end of April. Eggs are laid in groups on the leaves (usually on the underside) and on the petioles and young branches. The ovipositor usually has from 3 to 30 eggs, although it is not uncommon to come across leaves and twigs completely covered with egg masses (Figure 2a).

Larvae of the first instar usually appear in the second decade of May. The newly emerged larva has a dark yellow color, which darkens to a grayish-black color within half an hour, and the larvae begin to feed actively.

The development cycle of all three larval instars together takes about one month. By the end of the first decade of June, the third-instar larvae stop feeding, fall to the ground, and burrow under fallen leaves and in the litter near the roots of oleaster trees; after 2–3 days, these larvae turn into pupae.

First-generation adults usually emerge in large numbers at the beginning of the third decade of June. Emerged beetles immediately begin additional feeding and later copulation. Females begin laying eggs in early July, first-instar larvae appear from the second decade of July, and second-instar larvae are observed in the second half of July. Emerged larvae are first found on the lower surface of the leaves and finely skeletonize them (Figure 2b). Later, they crawl to the upper side of leaves and skeletonize them more closely, sometimes gnawing through. Pupation of third-instar larvae occurs in the second decade of August also in the litter or in the upper layer of soil.

Beetles of the second wintering generation appear from mid-August, at which time they begin to migrate to the litter or under the bark of the oleaster for wintering. In a cold spring with frosts and a cool beginning of summer, there are usually noticeable shifts in the timing of the development of the phases of the life cycle in the overwintered generation of leaf beetles. However, despite this, by mid-summer, phenological shifts usually stop, and the second generation appears in the second half of August.

3.2.5. Monitoring of Modern Populations

During route surveys of floodplains of the Ili, Karatal, and Lepsy rivers in 2006, we found several populations of oleaster leaf beetles, from which six populations were selected for monitoring observations in 2006–2018:

(1)

The Ili population (40 km north of Kapchagai, Russian olive thickets in the floodplain of the Ili River) was found on 13 June 2006. The population size for all the time of observations was very low; every year in the second decade of June, there were only about 15–20 beetles and 25–30 larvae of 1–2 ages. Near the place where the leaf beetle was found, a large young grove grows on the site of a previous fire, but it was impossible to find a single individual in it.

(2)

The Tasmurun population (70 km north of Kapchagai, near Miyaly village, Russian olive trees grew between the beginning of the Tasmurun canal and the Ili River) was found on 14 June 2006. Unburned bushes were still preserved in this part of the riparian forest, where a small number (27 individuals) of beetles, 2 oviposits, and several larvae of 1–3 ages were found. The number of insects in this population also remained very low in 2006–2018.

(3)

The Topar population (10–12 km south-west of the village of Topar, in the lower reaches of the Ili River, a small oleaster forest along a moist roadside depression on the edge of dunes), was discovered on 16 June 2006. In mid-June, 2nd–3rd instar larvae were already predominant here, and egg-laying and larvae of the 1st instar were rare. Despite the relatively high number of insects (an average of about 100 individuals per tree), this population did not cause much damage to its host plants in 2006. However, observations in 2007 showed that beetles and larvae of the overwintering generation had severely damaged individual trees growing along roadside ditches, and on some young bushes, all the leaves were eaten entirely. Compared to 2006, the number of leaf beetles in 2007 increased to an average of 120 individuals per tree. In 2008, the number of oleaster leaf beetles became even higher and reached an average of 160 individuals per 1 tree, although the number of leaf beetles in the adjacent barkhan (sand dune) area did not change and remained at the level of 2006—100 individuals per tree. The damage to host plants in 2008 was noticeably more remarkable than the previous year: devoid of leaves, which caused the drying and death of individual branches.

The increase in the number of beetles in 2008, in our opinion, was due to the early and hot spring, which also caused an earlier appearance of overwintered beetles and, accordingly, a phenological shift in the development of this (overwintered) leaf beetle generation. In 2008, beetles, after wintering, came to the crown of trees in the first decade of April. In late April and early May of the same year, copulation and egg laying took place, and larvae developed in May–the first decade of June. At the beginning of June, massive leaf damage was already observed on young plants, and on old trees, such damage was noted only in the lower part of the crown. At the end of May–beginning of June, there were no more beetles and ovipositors. The larvae of the 3rd age found on the branches were ready for pupation. Only pupae were found in the litter under the crown of trees; they were located among the plant remains or on the border with the soil at a depth of 1–2 cm; the pupae do not form cradles and lie freely in different poses, mostly on their sides. The first emergent adults in nature were found on 4 June. In artificial cages of 34 pupae collected for observation, all adults were born within 4 days (from 4 to 7 June 2008). In natural conditions, on trees growing in a wet depression along a roadside ditch, mass concentrations of beetles on tree crowns were observed as early as June 10. They actively fed, preferring shaded areas, avoiding direct sunlight, and constantly moving around the crown in choosing the most favorable leaves for food.

The mass emergence of first-generation beetles in 2008 was observed in the middle–early third decade of June, copulating beetles in the third decade of June, females started oviposition at the end of June, and mass oviposition was noted in early July. The first-instar larvae appeared at the end of the first decade of July, and the second-instar larvae appeared in the second half of July. The 1–3 instar larvae were recorded at the end of July, and their pupation in the tree litter began at the end of the first decade of August. Adults of the second generation of leaf beetles appeared in mid-August; at this time, there were some cases of their additional feeding with leaves and gradual departure for wintering in the litter and in the cracks of the bark of host trees.

Hereinafter, the population density decreased from 2009 to 2014 and remained at the same level—120 individuals per tree. In 201 to –2018, the number of insects in this population gradually decreased to an average of 95–100 individuals per tree. Accordingly, the damage to host trees has also been reduced.

(4)

The Karatal population 1 (15 km north of Ushtobe City, a grove of sparse old trees) was found for the first time on 15 May 2007. At this time, in the lower part of the crown of one of the Russian olive trees, on the upper side of the leaf, only five larvae of the 2nd age were found, one larva that had just transformed to the 3rd age, one ovipositor, and one female. This is all that could be found in this reasonably extensive grove. The appearance of beetles, the laying of eggs, and the development of larvae occurred in the early spring cycle.

(5)

The Karatal population 2 (22 km north of Ushtobe City, a vast stretch of floodplain forest consisting of old and medium-aged Russian olive trees mixed with willows) was discovered on 15 May 2007. This leaf beetle population was represented by small scattered spots, but the number of leaf beetles in individual spots was very high. In mid-May 2007, egg-laying larvae of 1–3 instars (mostly 1–2), males, and egg-laying females were recorded here. The leaves were usually damaged, mainly in the lower half of the crown. Most of the eggs were laid on the leaves, and in one ovipositor, the number of eggs located on the upper side of the leaf was usually less (5–15 eggs) than in the ovipositor on the lower side of the leaves (30–43 eggs). Large oviposits were also found on young branches, in the forks of branches, and on the petioles of leaves. Such egg-laying was sometimes observed in the 1950s in powerful centers of mass reproduction of the species on overpopulated bushes. An average of 5–10 adults and 15–20 oviposits were usually observed on the same branch length of 1.5 m. In this population, emerging larvae of the 1st age of the wintering generation were generally observed in the third decade of May. In general, this leaf beetle population developed almost a month earlier than the Topar population over the entire period of observations in 2007–2018. This is due to the peculiarities of the microclimate in this place.

(6)

The Karatal population 3 (55 km north of Ushtobe City, a moistened depression in the floodplain on the border with dunes along the drainage channel) was found for the first time on 15 May 2007, when this population lived only on a few low young bushes; the number of leaf beetles here was relatively high, about 430 beetles per plant. At this time, only copulating beetles were observed, and no egg-laying was found. The appearance of beetles from wintering sites on the oleaster crown here occurred 10–15 days later than in the Karatal population 2, even though they are located relatively close to each other (23 km). Here, local features of the microclimate and wintering places of this population are also affected. Unfortunately, observations in 2008 showed that this population has completely disappeared—no damage or beetles were found on the bushes. The leading causes of population death are drying up of the coastal lowlands, fire, and livestock that completely destroyed the litter under the Russian olive bushes.

Further searches for the leaf beetle in 2009–2018 in the Ili and Karatal valleys did not yield positive results. The main reason for the decline in the number of oleaster leaf beetles in the southern Balkhash region is frequent fires. For example, repeated surveys of areas of the Russian olive forest in the north of Bakanas that were densely populated by leaf beetles showed that even 25 years after the fire, the oleaster leaf beetle was not able to populate the safe forest.

In general, in the last few decades, the floodplain forests of the southern Balkhash region have been severely degraded due to negative anthropogenic impacts (fires, land withdrawal for agriculture, construction, etc.). Full-fledged floodplain forests have been preserved only in a few protected natural areas.

3.2.6. Efficiency for Biological Control

Since the mid-20th century, this species has been a dangerous pest of Russian olive [11,15,17,19,20,21,64,66]. The harm caused by the leaf beetle to Russian olive is especially evident during the mass reproduction of the beetle. Damaging trees for 2–3 years, the leaf beetle causes severe oppression and subsequent drying. Weakened trees that grow in less favorable conditions are particularly affected. Cases of mass reproduction of the leaf beetle during our observations in the southern Balkhash region in 2006–2018 were not observed. However, in the second half of the 20th century, such cases were common in Southeastern Kazakhstan. For example, in 1965, in the floodplain of the Charyn River in the Sarytogay forest (now the Charyn State National Natural Park), the oleaster leaf beetle caused massive damage to the Russian olive population in the time of mass reproduction. At this time, 432 leaves were damaged on a single branch of 600 leaves. At the end of summer, trees in large areas were stripped entirely [66]. In the mid-20th century, there was a mass reproduction of the leaf beetle in the lower reaches of the Karatal River, which caused significant damage to the populations of Russian olive; the area covered by the mass reproduction of the leaf beetle was about 10 hectares. Eating the leaves of trees by first-generation larvae reached 60% of the entire crown, and some trees lost their leaves completely [14]. Numerous mass breeding of beetles was also observed in southern Kazakhstan in the riparian forests of the Syr Darya river basin [11,17,19,20,21,63].

3.2.7. Testing in Nature Control

Altica balassogloi was tested on Elaeagnus angustifolia in the vicinity of the Avat Town (floodplain of the Besagach River, 50 km east of Almaty) to work out the method of establishing new beetle colonies (photo). On the afternoon of 17 June 2006, 55 first-generation beetles were planted on a young tree; beetles were collected in the vicinity of Topar Town in the lower reaches of the Ili River basin. The tested group of beetles did not establish; after 5 days, we did not find a single beetle on this or the neighboring bushes.

The next attempt was made on the evening of 16 May 2007, in the same place with beetles from the second overwintered generation, selected from the Karatal population 3. With a mighty northeast wind, we placed 76 beetles on the leeward side of the lower part of the crown. The beetles spread along the lower branches and began to eat the leaves; they managed to establish and start laying eggs on 1 June. Only three oviposits were found on the upper side of the leaves on the branch on which they were planted. In the future, the entire subsequent life of this population was associated only with this branch; no attempt was observed in the distribution of beetles to attack adjacent neighboring or remote branches. On the morning of 10 June, one ovipositor female, a pair of copulating beetles, one ovipositor, nine larvae of the first instar, and many leaves gnawed by beetles were recorded on this branch. In the evening of the same day, three larvae on one of the leaves disappeared; they may have been eaten by a ladybird larva crawling there. On 4 July, the beetles were no longer found, but there were many damaged leaves; at this time, there were small numbers of third-instar larvae feeding singly or in pairs on the upper side of the leaves. On 10 July, all the third-instar larvae disappeared; on 25 July, only one beetle was found. Since 31 July, no beetles, ovipositors, or larvae have been found despite our search for the leaf beetle in August and October. The population may have disappeared entirely again or migrated elsewhere.

In 2008, oleaster leaf beetles from the Topar population were planted on a medium-aged Russian olive tree in the vicinity of the Institute of Zoology in Almaty. For testing on experimental bushes in Almaty, 224 beetles were taken, which were transplanted to the lower branches on 12 June 2008. In the future, the transferred beetles were kept only on one tree and did not fly away. Immediately after landing on the lower branches, the beetles started feeding on the leaves. In the third decade of June, they laid eggs; in late June–early July, the first larvae were born; they enormously ate the lower part of the crown. Some of the leaves were almost entirely eaten. According to observations on 11 July, only six third-instar large and two second-instar larvae remained on the crown, actively feeding on the leaves, although numerous exuvia of first, second, and third-instar larvae were found on the branches. At this time, most of the larvae migrated to the litter and have already started pupating. In September, several second-generation beetles that went to winter were found under the bark of the trunk and in the litter under the tree crown. Unfortunately, in the spring of 2009, overwintered beetles were not found.

In our opinion, the low survival rate of transplanted beetles is primarily due to the food and geographical conservatism of the transplanted population (the beetles did not fly away and remained only on the original branches), caused, apparently, by the small number of “colonists”, as well as the enormous influence of predators attacking both adults (birds) and leaf-eating larvae (predatory bugs, ladybug larvae, photo). For example, when beetles were released near the Institute of Zoology, there was a noticeable concentration of insectivorous birds (mainly Indian Myna Acridotheres tristis) on the surrounding trees for an hour. Unfortunately, given the low number of leaf beetles in 2006–2022, we have not yet been able to transplant many beetles (2–3 or more thousand) without causing damage to the natural population.

3.3. Preliminary Annotated List of Insect Species Damaging to Russian Olive in Central Asia

Order HEMIPTERA

Suborder Auchenorrhyncha

Family Cicadellidae

Macropsis elaeagni (Emeljanov, 1964) (=M. unicolor). Monophagous insect of Elaeagnus angustifolia; floodplain forest species that settled in Kazakhstan with Russian olive plantings [15,16,35]. Emerging first-instar larvae occur in the second half of April–early May and coincide with the appearance and budding of the oleaster. The larvae suck on the buds, then on the leaves and tops of shoots and young twigs. Adults are found from June to August, and individuals are found until October. The species is distributed in southern Russia, Kazakhstan, Uzbekistan, Tajikistan, and Kyrgyzstan.

Macropsis elaeagnicola (Dubovsky, 1966). Monophagous insect of Elaeagnus angustifolia. The species lives in the mountains, settlements, and woodlands of Russian olive. Larvae begin emerging in May, and adults appear in June and July. The larvae suck the leaves and tops of the shoots. The species is widely distributed in Northern Kazakhstan along with oleaster plantings. It is known from Uzbekistan, Kyrgyzstan, and Southern and Northern Kazakhstan [35].

Suborder Sternorrhyncha

Superfamily Psylloidea

Family Triozidae

Trioza magnisetosa Loginova, 1964 (see chapter above).

Trioza elaeagni (Scott, 1880) (=furcata). Monophagous species of Elaeagnus angustifolia, floodplain forest species. It is also found on oleaster landings in settlements in western, central, and southern Kazakhstan [15,38]. Winter adults, two generations per year. Second-generation adults were recorded in October, leaving for the winter—in early November. It is known from Uzbekistan, Tajikistan, and the Caucasus region and is found in Central Asia with T. magnisetosa.

Superfamily Aphidoidea

Family Aphididae

Capitophorus archangelskii (Nevsky, 1928). Monophagous insect of Elaeagnus angustifolia, non-migratory species. Overwinter eggs in the forks of branches, bases of buds, petioles of last year’s leaves, and in the crevices of the bark on the trunk and branches. The first larvae emerge in early April, and their mass appearance is observed in mid-April. They feed on the buds and then on the tops of young shoots. The damage to Russian olive trees is significant: the leaves turn yellow and fall off, the shoots bend and slow down in growth, and with the strong infestation, the tree loses up to half of the entire foliage. It is distributed in Western, Central, and Southeastern Kazakhstan.

Capitophorus hippophaes (Walker, 1852) (=gillettei). Oligophagous of Russian olive and Hippophae rhamnoides. The eggs overwinter in the buds‘ sinuses and branch forks. With a large population, it causes the fall of leaves of Russian olive and Hippophae rhamnoides. The species is known from Northern, Central, and Southern Kazakhstan.

Capitophorus elaeagni (Del Guercio, 1894). Oligophagous of Russian olive and Hippophae rhamnoides, it lives on the underside of leaves, optionally migrates on Cirsium incanum in summer, and lives in willow-oleaster floodplain forests. Known all over the world.

Aphis craccivora (Koch, 1854). A broad polyphagous insect that damages numerous cultivated and wild plants from the family Ranunculaceae, Rosaceae, Fabaceae, Caryophyllaceae, Chenopodiaceae, Malvaceae, etc. It is also observed on oleaster; aphids settle in numerous colonies in the lower part of the crown at the ends of young shoots, which later bend and wither. It is distributed in Europe, Anterior and Central Asia, Southern Siberia, the Far East of Russia, North and South America, and Africa. It is the most harmful in Central Asia, Azerbaijan, and Southern Kazakhstan ([15,16]; information about Aphis medicaginis and A. fabae belongs to Aphis craccivora).

Superfamily Coccoidea

Family Monophlebidae

Drosicha turkestanica (Archangelskaya, 1931). A wide polyphagous, the primary host plants are willow, poplar, and oleaster. One generation develops per year. Eggs and first-instar larvae overwinter under the bark of trees, often near the ground surface or on the roots of plants. The larvae emerge from hiding places in early spring and spread over various plants. In late March–April, emerging second-instar larvae appear; they begin to move along tree trunks, feeding on leaves. In mid-to late May, after emerging, the third-instar larvae start to gather in colonies on twigs, bark cracks, or exposed areas. Adults are born at the end of June–the first half of July, and mating occurs. Females, after fertilization, are driven into the cracks of the bark on the trunk near the earth’s surface; during oviposition, they are covered with a white wax fluff. Within females, Cryptochetum turanicum (Diptera, Cryptochaetidae) flies develop as an endoparasite. The larvae and adults of the coccid are also eaten by the larvae of the ladybeetle Rodolia fisheri (Coleoptera, Coccinellidae), which are similar in body shape and color to the victim.

Family Coccidae

Parthenolecanium corni (Bouche, 1844) is a wide polyphage that also feeds on Russian olives. The species is known worldwide.

Parthenolecanium persicae (Fabricius, 1776) is a wide polyphage that also feeds on Russian olives. The species is known from Europe, Transcaucasia, and Central Asia.

Family Diaspididae

Lepidosaphes turanica (Archangelskaya, 1937). Monophagous species of Elaeagnus angustifolia. It lives on branches and trunks and is very harmful, drying both branches and entire trees. It was first described from Uzbekistan but is now also known from Iran, Kazakhstan, and Western China.

Lepidosaphes ulmi (Linnaeus, 1758). It is a broad polyphagous species, a serious pest of apple trees, and is also noted on oleaster. It causes the drying of Russian olive branches and is widely distributed around the world.

Diaspidiotus elaeagni (Borchsenius, 1939). The oligophagous species lives on Elaeagnus angustifolia and Hippophae rhamnoides. The species lives in floodplain forests and floodplains of mountain rivers and develops two generations per year, and the second instar overwinters. Egg laying occurs in May and August, and the fertility of one female is up to 40 eggs. It is known from Turkey, Armenia, Georgia, Iran, Central Asia, and China.

Suborder Heteroptera

Family Miridae

Orthotylus elaeagni (Jakovlev, 1881). Monophagous insect of Elaeagnus angustifolia, when mass reproduction causes the death of shoots. Two to four generations develop yearly; eggs overwinter, and larvae appear in early May. It is known from Western, Southern, and Southeastern Kazakhstan.

Deraeocoris pilipes (Reuter, 1879). Polyphagous species living on oleaster (Elaeagnus spp.), willows (Salix spp.), and elm (Ulmus spp.). It is known from Eastern and Southeastern Kazakhstan, Uzbekistan, and Tajikistan.

Glaucopterum kareli (Wagner, 1963). A narrow oligophagous species, it feeds on Elaeagnus angustifolia and E. orientalis. The species is known from Turkey, Kazakhstan, Turkmenistan, Tajikistan, and Mongolia [67,68].

Family Pentatomidae

Brachynema germarii (Kolenati, 1846). Polyphagous insects living on the oleaster. It is widely distributed from the Canary Islands and the Mediterranean through Transcaucasia, the Near and Middle East deserts, Central and Southern Kazakhstan, and Central Asia to Mongolia and Northern China [69].

Family Lygaeidae

Spilostethus pandurus (Scopoli, 1763) (=Lygaeus pandurus). Polyphagous species, but prefers plants of Lamiaceae, significantly fallen seeds of many plants, and juice of green parts. In Kazakhstan, it usually lives on Calligonum, Atraphaxis, and sometimes Elaeagnus angustifolia. One generation per year, adults overwinter. This species is widespread worldwide and found in South Africa, Southern Europe, Kazakhstan, and China.

Order COLEOPTERA

Family Scolytidae

Scolytus jaroschewskii (Schevyrew, 1893). It is known as a pest of Russian olive in the floodplain forests of Central Asia. Larvae overwinter, pupae in May, and adults in late May. The species inhabits the trunks and branches on the north side and leads to weakened and dried-out trees.

Scolytus schevyrewi (Semenov Tjan-Shansky, 1902). Wide polyphagous species; it mainly lives on native elm species and occasionally on willows (Salix spp.), apricots, cherries, peaches (Prunus spp.), and Russian olives. Despite its Asian native distribution (Russia, Kazakhstan, Kyrgyzstan, Tajikistan, Turkmenistan, Uzbekistan, China, Mongolia, and Korea), this species appeared in the USA in 2003 as a pest in Colorado and Utah. Later, it has since been found to occur in 10 western and central states. This insect attacks elms stressed by drought. Infested trees are killed by such attacks.

Family Bostrichidae

Enneadesmus scopini (Fursov, 1936). Usually inhabits weakened oleaster trees; in Tajikistan, it is also known as Gleditsia triacanthos (Fabaceae). One generation develops per year. The larvae overwinter at the end of passages gnawed through the wood; in late March or early April, the larvae awaken and continue to sharpen the passages. In the first decade of May, the larvae finish feeding and prepare chambers 1.5–2 mm wide and 5 mm long for pupation. The pupal stage lasts 10–15 days, and the beetles emerge from mid-May to early June. In June, the first larvae appear, and the larvae feed until the beginning of winter. Developing on the branches, this species circles them with its moves, causing the branches above the settlement to shrink. The species is known from the floodplain forests of Central Asia (Amu Darya basin) and Kazakhstan (Ili, Karatal, and Syr Darya River basins).

Lyctus turkestanicus (Lesne, 1935). This species develops on thin (up to 5 mm in diameter) shrinking shoots or branches of oleaster and inhabits the floodplain forests of Uzbekistan, Turkmenistan, and Western China.

Family Scarabaeidae

Tropinota hirta (Poda von Neuhaus, 1761). Beetles eat the flowers of many fruit trees; after fruit trees blossom, the images usually move to the oleaster flowers. Beetles damage mainly unopened flowers of Russian olive. The range of the species extends from Central and Southern Europe to Central Kazakhstan.

Tropinota turanica (Reitter, 1889). It feeds on the flowers of many plants. In Southern Kazakhstan, it is listed as an oleaster pest [16]. The species is known from Central Asia, Southeastern Kazakhstan, and Western China.

Oxythyrea cinctella (Schaum, 1841). Among other flowering plants, this scarab also damages Russian olive flowers, eating their ovaries. The species are known from Portugal, Spain, southern Italy, the Balkan Peninsula, the Caucasus and Transcaucasia, Iran, Afghanistan, Central Asia, Southeastern and Eastern Kazakhstan, and Western China.

Adoretus nigrifrons (Steven, 1809). It damages Russian olive and other plants’ flowers and inhabits floodplain forests, plains, and foothills. Adults fly from April to mid-September. It is known from the Caucasus, Transcaucasia, Central Asia, and Kazakhstan.

Protaetia marginicollis (Ballion, 1870). It feeds on the flowers of Russian olives and other flowering plants and lives in floodplain forests. It is distributed in the eastern part of Central Asia, in Kazakhstan, the upper reaches of the Ili River and the Syrdarya River Valley.

Family Cerambycidae

Aeolesthes sarta (Solsky, 1871). Polyphagous species. The preferred hosts of this insect are Ulmus minor, U. pumila, Populus alba, P. diversifolia, P. euphratica, P. talassica, P. canadensis, Salix acmophylla, S. songarica, S. turanica, Platanus orientalis, P. hispanica, Malus domestica, and Juglans regia. In general, it may damage species of Elaeagnus, Acer, Betula, Fraxinus, Gleditsia, Juglans, Malus, Morus, Platanus, Populus, Prunus, Pyrus, Quercus, Robinia, Salix, Ulmus, and other hardwood and fruit trees. This species is an important pest of many ornamental and deciduous fruit trees [26,27,28,70]. It attacks both stressed and healthy trees of different ages. Successive generations remain on the same tree for several consecutive years, eventually causing its death. Sometimes, young larvae encircle a tree, feeding on the cambium, which leads to the rapid death of the tree. Young trees with thin bark are most susceptible to the beetle, and 1–3 larvae may be enough to kill a tree [71]. It is distributed in South Kyrgyzstan, Uzbekistan, Tajikistan, Turkmenistan, Afghanistan, India (Western Himalayas), Iran, and north Pakistan.

Anoplistes halodendri halodendri (Pallas, 1776) (=Asias halodendri). Polyphagous species. It can feed on Russian olive. Distribution: Bulgaria, Ukraine, Albania, Romania, Kazakhstan, Siberia, and European Russia.

Anoplophora glabripennis (Motchulsky, 1853). Polyphagous species usually prefer Acer, Populus, Salix, Morus, Malus, Prunus, and sometimes Elaeagnus. Adults feed on the bark and leaves of trees, preferring to attack young shoots. They overwinter in the egg, larval, or pupal stages. It originates from China but has become widely distributed and found in Central Asia, Europe, and North America in recent years.

Chlorophorus elaeagni (Plavilstshikov, 1956) is a polyphagous species that lives on tamarisk, oleaster, and Halimodendron halodendron. The larvae live in the trunks and thick branches of weakened Russian olive trees, causing the plant to die. The mass emergence of adults happens from mid-June. The species is known from Russia (Dagestan) and Western and Southeastern Kazakhstan (floodplain forests of the Ili and Karatal rivers).

Chlorophorus faldermanni (Faldermann, 1837). Polyphagous species, it lives on young trees of Russian olive, Halimodendron halodendron (Syr Darya river floodplain), and poplar (Northern Iran). The appearance of the adults begins in mid-May and continues until the end of September. The larvae grind holes up to 10–30 cm in the wood and cause significant damage to Russian olive trees. This species is distributed in Uzbekistan, South Kazakhstan, Afghanistan, and China.

Molorchus kiesenwetteri (Mulsant et Rey, 1861). It is associated with Russian Olive, inhabiting thin branches of 0.3–1.5 cm diameter. It causes the drying of Russian olive branches. It is known from Uzbekistan, Turkmenistan, and Western Kazakhstan.

Tetrops elaeagni (Plavilstshikov, 1954). The larvae live only on Elaeagnus spp. The species is known from Kazakhstan, Uzbekistan, Turkmenistan, and the south of European Russia.

Tetrops formosus (Baeckmann, 1903). The larvae live mainly in weakened and shrinking Russian olive trees and apple trees (Kyrgyzstan). The passages are drilled under the bark in the upper layer of wood. Pupae appear in early May, and the imago emerges in the second half of May. This rare species is known from Kazakhstan, Kyrgyzstan, and Western China.

Turanium scabrum (Kraatz, 1882). This species lives on Russian olive, although it is also recorded on apple trees [15]. Larvae of the last and pre-last instars overwinter at the end of passages located in the wood of trunks and branches. Pupation in Southeastern Kazakhstan occurs in late April–early May; the appearance of adults begins in the middle of the first decade of May; swarming of adults occurs in the second half of May–early June. This species is very harmful and is known from Uzbekistan, Kazakhstan, and Russia (Orenburg).

Xylotrechus asellus (Thieme, 1881) (=grummi). It lives on the Russian olive. Larvae overwinter and pupae are formed in late May and mid-June; imago flights begin in the first half of June and continue until the end of June. Larvae populate the trunks of usually old or severely weakened trees; they cause severe damage, leading to the tree’s death. The species shows a very large conservatism in choosing a tree; if the larvae have populated it, they will live on it until it is destroyed. It inhabits floodplain forests throughout Central Asia, Southern and Southeastern Kazakhstan.

Xylotrechus namanganensis (Heyden, 1885). Wide polyphagous species, it lives on Juglans, Prunus, Malus, Morus, Crataegus, Elaeagnus, Populus, Ulmus, Celtis, Salix, Betula, Alnus, Platanus, as well as other deciduous trees in Kyrgyzstan, Kazakhstan, Tajikistan, Turkmenistan, Uzbekistan, Afghanistan, and China.

Family Buprestidae

Anthaxia elaeagni (Richter, 1945) (=Cratomerus elaeagni). It lives only on Elaeagnus spp. and inhabits the branches and trunks of weakened trees in the floodplain forests of Central Asia. Larvae overwinter, in early May; larvae of the last age and pupae are recorded, imago in May–June. It causes significant damage to Russian olive.

Capnodis miliaris (Klug, 1829). Polyphagous species, it is an essential pest of poplar and willow and occasionally lives on oleaster. The adults emerge between the end of May and August, feed on leaves and young shoots, and then overwinter in the soil or under the dried leaves. One generation develops in two years. It is known in Turkmenistan, Tajikistan, Israel, Turkey, Northern Iran, and Armenia.

Family Bruchidae

Spermophagus sericeus (Geoffroy, 1785). These beetles feed on flowers, gnawing out generative organs during the flowering of many plants. They are also found on Russian olives in southern Kazakhstan [15]. They are known from Europe, Kazakhstan, Siberia, and Mongolia.

Family Curculionidae

Rhyncolus culinaris (Germar, 1824). It lives in the wood of many coniferous and deciduous trees and on oleaster in the floodplain forests of the Amu Darya. Larvae overwinter, and feeding begins in early spring. It causes significant damage to decayed wood and to live Russian olive trees [17]. It is known from many parts of Eurasia.

Platymycterus trapezicollis (Ballion, 1878). Polyphagous species. Beetles are very harmful to the foliage of Russian olives, poplars (especially Populus diversifolia), Halimodendron halodendron, Robinia pseudoacacia, and Alhagi spp. When feeding, the beetles gnaw out the edges of the leaf blade or skeletonize the leaves. Adults appear by mid-May and are observed in mass in June–July. They are known from Central Asia.

Polydrusus obliquatus (Faust, 1884) (=ferghanensis). It is a polyphagous species. In Kazakhstan, it is found on oleaster, willow, peach, apple, and pear. It is very harmful; beetles in May gnaw the bark of young shoots, leaf petioles, and the edges of the leaf blade; sometimes, trees lose up to half of their foliage [16]. It is known from Central Asia.

Polydrusus pilifer (Hochhuth, 1847). A polyphagous species, it is often found on strawberries (Fragaria sp.). On oleaster in Southern Kazakhstan [16], beetles eat the edges and petioles of leaves, buds, and the tops of young shoots. It is known from Central Asia.

Chloebius immeritus (Schoenherr, 1826). Polyphagous beetles damage leaves and flower buds, mainly on Russian olive and licorice; in floodplain forests, this species prefers to feed on oleaster. Adults appear in late April, and copulation occurs in the first half of May. It is known for being from Central Asia and Kazakhstan.

Chlorophanus caudatus (Fahraeus, 1840). It is a polyphagous species that damages the leaves of oleaster, willow, turanga, and tamarisk in floodplain forests. Adults appear in early May and are present in the ground in June. It is known from Central Asia and the Caucasus.

Megamecus cinctus (Faust, 1887). It is observed on Elaeagnus spp., including Russian olive, as a harmful species known from Central Asia.

Sitona macularius (Marsham, 1802). Polyphagous species. It is known as a pest of lentils and almonds and has also been noted on Russian olive (Schaffner et al., 2007). Widely distributed in the Palearctic, the species is also known in the United States.

Prisistus caucasicus (Kirsch, 1878). It is found in Elaeagnus spp. [72] and is known in Russia (Moscow and Ryazan regions, Caucasus), Georgia, Armenia, Azerbaijan, Kazakhstan, Uzbekistan, Turkmenistan, Tajikistan, Iran, and Afghanistan.

Family Rhynchitidae

Temnocerus elaeagni (Korotyaev et Legalov, 2006.) Oligophagous species, it lives on Elaeagnus and found also on Salix. Species is described from Central and Southeast Kazakhstan [73].

Family Chrysomelidae

Altica balassogloi (Jakobson, 1892) (see chapter above).

Altica deserticola (Weise, 1889). A polyphagous species, it feeds on the leaves of Russian olive, willow, tamarisk, and Halimodendron halodendron. In the floodplain forests of Central Asia, the leaf beetle mainly damages the foliage of Russian olives, causing the trees to lose their growth, shrink, and not bear fruit [17]. There are two generations per year. It is known from Central Asia.

Family Meloidae

Epicauta erythrocephala (Pallas, 1776). It is a widespread polyphagous species, a pest of potatoes, beets, and other crops. In the floodplain forests of Central Asia, it damages foliage on Russian olive, ash, Ammodendron sp., Zygophyllum sp., and other plants.

Order HYMENOPTERA

Family Formicidae

Tetramorium caespitum (Linnaeus, 1758). In May-July, this ant species was noted in Southern Kazakhstan as a pest of young oleaster shoots in the lower part of the crown. Ants in groups of up to several dozen individuals chewed or nibbled the tops of young shoots along with the leaves, causing the tops of the shoots to wither [16]. The species is known in Northern Eurasia.

Family Megachilidae

Megachile dohrandti (Morrawitz, 1880). In the floodplain forests of Central Asia, this leaf-cutter bee cuts out pieces of leaves and uses them to build its nests in the old passages of the cerambycid beetle Xylotrechus asellus. In the floodplain forests of the Amudarya River, more than one-third of the leaves on individual trees are affected by this bee [17]. It is known from Central Asia, Kazakhstan, and southern China.

Order LEPIDOPTERA

Family Torticidae

Apotomis lutosana (Kennel, 1901). This oligophagous species, which lives on various species of Elaeagnus, is noted as a pest on European olive plantations, Olea europaea [73]. Larvae damage oleaster trees, feeding between spun leaves of oleaster and skeletonizing them. Parasitoid is Nemorilla maculosa Meig. (Tachinidae) [74]. It is distributed in Romania, the Trans-Caucasus, South Russia (Caspian area), Kazakhstan, Turkmenistan, Uzbekistan, and Tajikistan [75].

Pandemis chondrillana (Herrich-Schäffer, 1860). Wide polyphagous species, its larvae prefer apple, pear, apricot, plum, almond, peach, cherry, quince, poplar, willow, as well as rose, pomegranate, cotton, pistachio, lilac, and oak. It was also recorded on Elaeagnus. There are 2 to 3 generations yearly in Southern Kazakhstan, Uzbekistan, and Tajikistan. Second- and third-instar larvae (sometimes also fourth-instars) hibernate in dense silken cocoons. In wintertime, they are usually in bark cracks on the root neck or under leaf remains webbed to bark, as well as on the trunks and branches. The larvae start feeding in April at the beginning of blossoming; they make shelters by webbing two to four leaves together or by rolling the leaf around its central vein. The pupae of the hibernated generation appear in the first decade of May, and the mass appearance—in May; this stage lasts 8–15 days. Adults emerged in mid-May–beginning of June and fly until late June and again from mid-August until mid-September. There are two known parasitoids: Sympiesis albiventris Storozheva (Eulophidae) and Actia pamirica Richter (Tachinidae). Most damage is caused by the second- and third-instar larvae. It is distributed in Southern and Eastern Europe, Russia (from the European part to Southwest Siberia), Asia Minor, Iran, Pakistan, Kazakhstan, Mongolia, and North-Western China [76].

Archips rosana (Linnaeus, 1758). This widely polyphagous species occurs on apple, pear, plum, hop, raspberry, hawthorn, and privet, as well as on Abies, Acer, Alnus, Betula, Cistus, Corylus, Cydonia, Fraxinus, Hippophae, Laurus, Lonicera, Medicago, Morus, Myrtus, Plantanus, Populus, Prunus, Quercus, Rhododendron, Rosa, Salix, Syringa, Tamarix, Tilia, Ulmus, Urtica, Vaccinium, and Viburnum. In Kazakhstan, it is also observed on Elaeagnus angustifolia: larvae in April–May, pupae in the second half of May, and adults from the beginning of June. There is only one generation yearly. It damages leaves, flowers, and fruitlets; it is distributed and abundant throughout Europe, Asia Minor, the Trans-Caucasus, Kazakhstan, and North America.

Family Gelechiidae

Ananarsia eleagnella (Kuznetsov, 1957). It is a widely polyphagous species associated with Elaeagnus spp. and Hippophae spp.; it was also noted to feed moth larvae on Crataegus oxyacantha and Malus domestica in experimental conditions [40,43]. It feeds on leaves and develops in stems, buds, and fruits. In Kazakhstan, young caterpillars appear in the second half of May on shoots of Russian olive (this year) between newly unfolded leaves of apical buds. They glue several leaves together with a web and, having settled between them, scrape off the epidermis or chew through a hole in it. Grown caterpillars bite into the apical parts of young shoots and make heart-shaped moves. Affected shoots at first do not stand out among healthy shoots, but later, their ends shrink and bend hook-like, sometimes bursting along the course. This species can cause severe damage to the growth of Russian olive, affecting up to 50–70% of all shoots in large trees and almost 100% in young bushes, as observed in Central Kazakhstan [15]. The species is known from Central Asia and Kazakhstan.

Ananarsia lineatella (Zeller, 1839). A polyphagous species, but it lives mainly on Prunus spinosa, Malus spp., Armeniaca spp., Persica spp., Cerasus spp., Amygdalus spp., and Acer tataricum, where it damages leaves, shoots, and fruits. Widely distributed in Central and South Europe, Russia (European part), Caucasus; Transcaucasia, Central Asia, China, North Africa, Asia Minor, Nearest East, Iran, Afghanistan, India, Australia, and North America [33].

Family Geometridae

Lycia hirtarius (Clerck, 1759). Wide polyphagous species feeding on birch, oak, poplar, willow, blackthorn, raspberry, rose, and oleaster. Pupae overwinter in the soil. The caterpillars appear in June and are observed until October, and the imago flies from late May to August. They eat the leaves of oleaster, but the damage is insignificant. Widespread species in the Palearctic: Europe, Asia Minor, Central Asia, Kazakhstan, and the Far East [77].

Family Noctuidae

Acronicta rumicis (Linnaeus, 1758) is a wide polyphagous species, a caterpillar in Southern Kazakhstan eats the leaves of Russian olive, the harm to oleaster is insignificant. It is a widespread species in the Palearctic.

Family Cossidae

Cossus cossus (Linnaeus, 1758). A broad polyphagous species, it lives on ash, willow, many fruits, and other deciduous trees. In the floodplain forests of Central Asia and Kazakhstan, this species is common on willow but also lives on Russian olive. The species is distributed throughout Europe, the Caucasus, Central Asia and Kazakhstan, Siberia, and the Far East of Russia, as well as in Western and Northern China.

Family Sphingidae

Hyles hippophaes (Esper, 1793). Oligophagous species in Central Asia and Kazakhstan; subspecies of H. h. bienerti Stgr. It feeds on Russian olive and sea buckthorn and has been noted as a pest of Russian olive leaves [17]. The caterpillars completely ate the leaves on some trees. There are two generations per year. Pupae winter, flights of adults of the overwintered generation occur in May; after that, females lay their eggs singly. Emerging caterpillars have a developing period of 20–30 days; pupation occurs in the litter, and the mass flight of first-generation butterflies occurs in July. It is found in Afghanistan, Armenia, Azerbaijan, China, France, Georgia, Germany, Greece, Iran, Iraq, Kazakhstan, Kyrgyzstan, Mongolia, Pakistan, Romania, Serbia and Montenegro, Spain, Switzerland, Syria, Tajikistan, Turkey, Turkmenistan, and Uzbekistan.

Family Pyralidae

Euzophera alpherakyella Ragonot, 1887. It damages shoots of Elaeagnus in Tajikistan and Kazakhstan. Distribution: South Russia, Tajikistan, Southeast Kazakhstan, and West China.

Family Nolidae

Meganola elaeagni (Shchetkin, 1980) is a narrow oligophage noted as an endemic pest of Elaeagnus orientalis and E. angustifolia in Tajikistan and Turkmenistan.

Family Lymantriidae

Lymantria dispar (Linnaeus, 1758). Wide polyphagous and quarantine species. Feeding on leaves of Quercus, fruit trees, Populus, Betula, Larix, Elaeagnus, etc. Adults of Asian populations can fly, but adults of European populations cannot. Distributed in Europe (widely) and the Mediterranean region; Russia (widespread); Baltic countries; Belarus; Moldova; Ukraine; Transcaucasus; Kazakhstan; Central Asia; India; Afghanistan; Iran; Iraq; China; Japan; Korea; and Taiwan, as well as introduced in Canada and the USA.

Family Lasiocampidae

Malacosoma paralella (Staudinger, 1887). Wide polyphagous and quarantine species. It damages leaves on Atraphaxis pyrifolia, Berberis integerrima, Cerasus verrucosa, Chaenomeles japonica, Cotoneaster acutiuscula, C. insignis, C. suavis, Crataegus hissarica, C. pontica, C. turkestanica, Cydonia oblonga, Fraxinus sogdiana, Hippophae rhamnoides, Juglans regia, Lonicera korolkowii, L. nummulariifolia, Malus domestica, M. sieversii, Myricaria bracteata, Populus alba, P. tremula, Prunus mahaleb, P. avium, P. armeniaca, P. bucharica, P. cerasus, P. divaricata, P. dulcis, P. padus var. pubescens, P. persica, Pyrus communis, Quercus boissieri, Q. macranthera, Q. robur subsp. robur, Ribes nigrum, R. rubrum, Rosa canina, R. corymbifera, R. kokanica, R. maracandica, Rubus idaeus, R. turkestanicus, Salix excelsa, S. tenuijulis, Sorbus persica, S. turkestanica, and Ulmus sp. Significant damage also occurs on Berberis, Chaenomeles, Cotoneaster, Crataegus, Cydonia, Malus, Prunus, Pyrus, Rosa, Salix, and Sorbus species. Leaves of other plants are occasionally damaged. It is distributed in Turkey, Syria, Armenia, eastern Kazakhstan, Kyrgyzstan, Uzbekistan, Tajikistan, Turkmenistan, and North Iran [78].

Order DIPTERA

Family Agromyzidae

Amauromyza elaeagni (E. Rohdendorf-Holmanova, 1959). A common species in Central Asia and Southeast Kazakhstan, the oleaster fly miner develops in several generations yearly. The first mines’ appearance on Russian olive leaves was noted in the second half of May and mass in June. Mines of round or irregular shape from 0.5 to 2 cm in diameter are usually located on the edge of the leaf; one leaf was observed from 1–2 to 15 min. The larvae that have settled in the leaves feed continuously for 7–10 days, then chew through a hole in the epidermis and leave the mine, burrowing into the litter and pupating. Damage caused by the fly-miner leads to drying up to 10% of the foliage.

Family Cecidomyiidae

Cantarinia elaeagniflorae (Fedotova, 1988). Oligophagous species, according to Z. A. Fedotova [34], live on Elaeagnus oxycarpa, and E. angustifolia, forming flower galls on them. The species was described as being from Southeastern Kazakhstan (Southern Balkhash Lake region).

4. Discussion

Currently, in Central Asia, 72 species of insects from 58 genera, 33 families, and six orders have been detected as pests of Russian olive. The most numerous are insects from the order Coleoptera (36 species, 29 genera, 10 families), Hemiptera (14 species, eight genera, six families), and Lepidoptera (13 species from 12 genera, 10 families). For biological control of Russian olive in the United States, 24 species from this species list are suitable:

Monophages (8 species): Cicadellidae: Macropsis elaeagni, M. elaeagnicola, Triozidae: Trioza magnisetosa, T. elaeagni, Aphididae: Capitophorus archangelskii, Diaspididae: Lepidosaphes turanica, Miridae: Orthotylus elaeagni, Cerambycidae: Molorchus kiesenwetteri.

Oligophages (16 species): Aphididae: Capitophorus hippophaes, Capitophorus elaeagni, Diaspididae: Diaspidiotus elaeagni, Miridae: Glaucopterum kareli, Bostrichidae: Lyctus turkestanicus, Cerambycidae: Tetrops elaeagni, Xylotrechus asellus, Buprestidae: Anthaxia elaeagni, Curculionidae: Megamecus cinctus, Prisistus caucasicus, Rhynchitidae: Temnocerus elaeagni, Chrysomelidae: Altica balassogloi, Torticidae: Apotomis lutosana, Sphingidae: Hyles hippophaes, Nolidae: Meganola elaeagni, Cecidomyiidae: Cantarinia elaeagniflorae.

In addition, it is possible to use another six species of insect pests that have been noted on Elaeagnus but whose feeding specialization has not yet been clarified: Bostrichidae: Enneadesmus scopini, Cerambycidae: Tetrops formosus, Turanium scabrum, Formicidae: Tetramorium caespitum, Megachilidae: Megachile dohrandti, Pyralidae: Euzophera alpherakyella.

5. Conclusions

Kazakhstan’s most studied species of fauna for biological control of Russian olive in the United States are the monophagous Russian olive psyllid Trioza magnisetoza and the narrow oligophagous species Russian olive leaf beetle Altica ballasogloi. Information on the distribution, biological and environmental characteristics, feeding, and damage to the host plant is sufficient for using these species in biological control in North America. However, due to the degradation of the natural ecosystems of the southern Balkhash region due to anthropogenic influence, the state of the populations of both species has deteriorated in the last 30 years; some populations have disappeared, while others have declined in number. For this reason, it is necessary to continue searching for this species and work out methods for establishing new artificial populations in nature and the laboratory.

The research was mainly aimed at a detailed study of the life cycle of two species and the harmfulness of Russian olives in their original natural habitats in Central Asia. Within our research and for the first time, experiments were conducted on the movement of part of the populations of both species to other suitable habitats in Southeast Kazakhstan. This is the first stage in developing technologies for their use in North America (in particular, in the USA). As a result of the conducted research, it was proven that both species, among other species of phytophages of Russian olive, are the most suitable for further work on their use in biocontrol of Russian olive on another continent.