Assessment of Biological and Ecological Characteristics of Sievers Apple Tree Pests in Trans-Ili Alatau, Kazakhstan

: This research aimed to evaluate the occurrence of three signiﬁcant pests, namely the apple ermine moth ( Y. malinellus Zell.), the rosebush leaf roller ( A. rosana L.), and the hawthorn leaf roller ( C. crataegana Hb.), commonly found in Sievers apple trees. The research was conducted within the Ili-Alatau state national natural park, focusing on populations of the Sievers apple tree on the northern slope of the Trans-Ili Alatau mountain range. The study revealed varying pest abundances across different monitoring sites within the park. The apple ermine moth ( Y. malinellus Zell.) exhibited lower occurrence compared to A. rosana L. and C. crataegana Hb. The Aksai and Kuznetsov Gorge populations of the Sievers apple tree showed higher susceptibility to the ermine moth. The rosebush leaf roller ( A. rosana L.) was dominant in the Aksai and Oi-Zhailau populations, while the hawthorn leaf roller ( C. crataegana Hb.) exhibited higher abundance in several monitoring sites. Phenological studies revealed that Y. malinellus Zell. have a life cycle of one year, the developmental stages of A. rosana L. last for approximately 9–10 months, and the life cycle of C. crataegana Hb. is also one year. The data obtained allowed us to assess pest status, which will hopefully help in developing protective measures for suppressing their outbreak in the region.


Introduction
Ile-Alatau State National Nature Park was established in 1996 with an area of 202,292 ha located near to the city of Almaty, Kazakhstan.Later, the area was gradually reduced.The boundaries of the Park have undergone multiple changes, and now the area of Ile-Alatau State National Nature Park is 186,400.2ha [1].Ile-Alatau State National Nature Park is located along the northern slope of the Zailiisky Alatau Mountains from the Shamalgan River in the west to the Sholak River in the east.Its length from west to east is 120 km, and its cross-section is 30 km.The southern boundary of the park runs along the main ridge of the Zailiiskiy Alatau and partly borders on the state border between Kazakhstan and the Kyrgyz Republic from the southwest.The northern boundary of the park runs along the foothills of the Zailiisky Alatau, covering wild forests.The main protected wealth of Ile-Alatau State National Nature Park is forest land.They cover an area of 75,207 ha, including a forested area of 62,262 ha and non-forested area of 10,969 ha.Thus, the forest cover of the protected area is 37.7% [2].
Apple and apricot forests are represented by massifs of different sizes, small groups, and individual trees throughout the territory of the national park.The Sivers apple tree is distributed practically in all gorges of the national park, namely Issyk, Mikushino, Soldatsay, Talgar, Kotyrbulak, Big and Small Almaty, Aksay, Kaskelen, and Turgen, at an to other pests and diseases.Appropriate pest management practices, including cultural practices, biological controls, and chemical treatments, can help to manage and reduce the impact of these pests [14,15].
The early seasonal defoliation of trees is particularly hard on the organism of fruit trees, so the radial growth of trees can be significantly reduced for several years after the outbreak of insect pests.This reduction in tree growth facilitates the establishment of pathogenic fungi, bacteria, and insect pests on the tree, which, in turn, can further desiccate the trees [16,17].For example, the outbreak of apple moths in 1998-2003 in the Dzhungar Alatau and in 2008-2011 in the Trans-Ili Alatau endangered priceless Sievers apple trees [18].For 8 years in a row, during summer, the trees stood leafless, and after secondary leaf formation, they were weakened and subsequently dried out.Notably, the apple moth is also threatening the cultivated gardens and apple trees in the Trans-Ili Alatau, and some areas of apple orchards have been badly damaged by pests [19].
The ecological characteristics of pests are important to understand because they can help to identify the factors that contribute to pest outbreaks and the development of effective pest management strategies.To prevent widespread pest damage in apple forests, it is essential to establish regular scientific pest monitoring programs that track the dynamics of pest populations and their natural enemies and provide information on the phytosanitary status of a particular area during certain phenological periods.Such programs should be implemented alongside forest management and protective measures [20].
This study aimed to assess the occurrence of three major pests (Yponomeuta malinellus Zell., Archips rosana L., and Cacoecia crataegana Hb.) that are commonly found in Sievers apple trees.Additionally, it aimed to investigate the life cycle characteristics of these pests in order to provide preventive recommendations.By understanding the phenological aspects of these pests in the Northern Tien Shan region, it becomes possible to enhance the survival of trees and effectively manage their harmful populations.

Distribution and Study Area
Our research involved examining multiple populations of the Sievers apple tree within Ili-Alatau state national natural park, specifically on the large northern slope of the Trans-Ili Alatau mountain range.All studied wild natural populations are located at altitudes of 900-1500 m above sea level, though on slopes of southern exposition, they may rise up to 1500-1700 m (Figure 1).Samples were taken from monitoring sites of Ile-Alatau State National Park, such as the Aksai forestry, the Soldatsai forestry, the Issyk forestry, the Small Almatinka gorge, the Oi-Zhailau gorge, the Kuznetsov gorge breeding-genetic reserve (Figure 2).
In the Soldatsai population of the Talgar area national park, M. sieversii are found in the form of small massifs, groups, and individual trees, predominantly of yellow fruit forms.In the Issyk River gorge population, the Sievers apple trees are found individually and in groups at altitudes of 1200-1800 m above sea level on slopes of northern exposition and along the river bed.
In the Alma-Arasan gorge population of the Medeu area of the national park, the Sievers apple tree grows in small groups or individual trees.In the Aksai area of the national park, the apple trees are found as individual trees amidst other trees and shrubs [21].

Sampling Methods
The extent of the spread of harmful organisms was identified by completing a route survey of the monitoring sites and catching insect pests with an entomological net.In each monitoring site, 10 trees of different ages were selected.Sampling was carried out in April, during daylight hours, as the post-embryonic development of these pests begins in this month.The caterpillars begin to hatch in April, and they damage the leaves of trees.In the Soldatsai population of the Talgar area national park, M. sieversii are found in the form of small massifs, groups, and individual trees, predominantly of yellow fruit forms.In the Issyk River gorge population, the Sievers apple trees are found individually and in groups at altitudes of 1200-1800 m above sea level on slopes of northern exposition and along the river bed.
In the Alma-Arasan gorge population of the Medeu area of the national park, the Sievers apple tree grows in small groups or individual trees.In the Aksai area of the national park, the apple trees are found as individual trees amidst other trees and shrubs [21].In the Soldatsai population of the Talgar area national park, M. sieversii are found in the form of small massifs, groups, and individual trees, predominantly of yellow fruit forms.In the Issyk River gorge population, the Sievers apple trees are found individually and in groups at altitudes of 1200-1800 m above sea level on slopes of northern exposition and along the river bed.
In the Alma-Arasan gorge population of the Medeu area of the national park, the Sievers apple tree grows in small groups or individual trees.In the Aksai area of the national park, the apple trees are found as individual trees amidst other trees and shrubs [21].

Pests Counting
Pests were counted by methods generally accepted in entomology.Thus, leaf damage by leaf rollers (hawthorn and rosebush leaf) per 10 model trees were accounted by damage degree as follows: 1: Weak, 2: Medium, and 3: Severe.Damage to leaves by apple moth was determined per 10 model trees on a four-point scale, which was as follows: 0-no damage, 1-damaged leaves on single branches, 2-leaves damaged by 10-25%, 3-leaves damaged by 50-75%, and 4-completely damaged.
One hundred leaves per tree were assessed three times between April and July.The prevalence of the dominant pest species was investigated according to the "Methodological guidelines for monitoring pests, weeds and crop diseases" [22].
The results of studying the species composition of pests were recorded using the following scale: 0-species in the collection is absent; +-a rare occurrence of species (5-10% of leaves, generative and axial parts of the tree are infested or damaged); ++-average occurrence of species (10-25% of leaves, generative and axial parts of the tree are infested or damaged); +++-high occurrence (25-50% of the surface of analysed tree organs are infested and damaged).

Pests Types and Identification
The pests that were most relevant to our research objectives were apple ermine moth Yponomeuta malinellus Zell., hawthorn leaf roller Cacoecia crataegana Hb., and rose leaf roller Archips rosana L. The first item we inspected were leaves contaminated by pests at different stages of their development, including larvae of different ages, pupae, and adults [23,24].Various identification tables that have been widely referenced in the scientific literature were used.All collected insects were thoroughly studied under a microscope and photographed.

Phenological Characterization of Pests
The phenological characteristics of the three dominant pests were studied both in the field and in the laboratory via artificial cultivation of all development stages in cages (2018-2019, the Institute of Zoology of the RK National Academy of Sciences).The collected moths and larvae were placed in 0.5 L glass jars or glass tubes together with their host M. sieversii leaves.Infested leaves were also kept separately in other test tubes.These artificial cages were marked with serial numbers, and a register, which listed their respective details, was made; these details included entry number, place and time of collection, information on the plant and the nature of its damage, etc. Subsequently, the larvae were transplanted into separate tubes for shedding and keeping [24,25].
Laboratory tests were carried out according to the method of Dobrovolsky [26] and Fasulati [27].Insect pests were grown from April to July.Samples were kept in a growth chamber.The feeding ration was changed as required.The day-night cycle regime was kept the same as it would be naturally.The temperature regime and relative humidity were set close to natural conditions.
In the laboratory, the tubes with twisted leaves were covered with gauze and labeled.The keeping and feeding of larvae in test tubes were strictly controlled, constantly maintaining the appropriate moisture degree, which is necessary for the normal development of larvae [28].To this end, the jars with the larvae were not kept long under the direct rays of the sun in order to avoid the tubs fogging up, since over-moistening and overheating would negatively affect the development of the larvae.Monitoring sites (Table 1) were laid in wild fruit forests of the Trans-Ili Alatau at various heights from 1345 to 1714 m.

Statistics
The data obtained from the study are the results of triplicate measurements.The resulting measurements were analyzed using XlStat 2020 (Addinsoft Inc., Lille, France).The differences between the samples were evaluated using one-way ANOVA; p < 0.05 was considered statistically significant.

Pest Infestation of Apple Tree
To date, more than 130 species of pests of wild Sievers apple tree populations and other fruit species have been recorded in the mountainous wild fruit forests of the Trans-Ili and Dzhungar Alatau [28,29].The pests that cause the most environmental damage are insects, among which the most significant (52%) are species of the order Lepidoptera (69 species of 57 genera).We identified three dominant species that cause significant damage to wild populations of apple trees (Table 2).Meanwhile, the hawthorn leaf roller C. crataegana Hb. has an average occurrence and contamination degree in the Kuznetsov and Soldatsai gorges, but at other monitoring sites, it has a high degree of abundance and contamination.There was a moderate distribution of A. rosana L. and C. crataegana Hb. in the Kuznetsov Gorge genetic reserve, although apple ermine moths are abundant here (as in the Aksai and Oi-Zhailau gorges).It was found that, in the Trans-Ili Alatau, the occurrence of Y. malinellus Zell. is lower than A. rosana L. and C. crataegana Hb.
The Sievers apple tree of the Aksai and the Kuznetsov Gorge populations is more affected by the ermine moth compared to the trees growing in other monitoring sites.Our findings revealed that the rosebush leaf roller damaging the Sievers apple tree foliage is also dominant in the Aksai and Oi-Zhailau populations, although its number in the Small Almatinka population is noticeably lower.Hawthorn leaf rollers are also abundant in the Aksai population, but their abundance is noticeably lower in the Soldatsai and the Kuznetsov Gorge populations.
The study revealed that the three dominant species that damage the leaf of M. sieversii have the highest abundance in the Aksai apple tree population.Meanwhile, the least damage from the three dominant species was noted in the Small Almatinka population.Data on damage to foliage and trees from the three dominant pests (Y.malinellus Zell., A. rosana L., C. crataegana Hb.) in the monitored sites of the Trans-Ili Alatau are presented in Table 3.
The degree of damage to the leaves of M. sieversii by Y. malinellus Zell. in the monitored sites ranged from 19.5 to 28.7%, while for A. rosana L. and C. crataegana Hb., this figure ranged from 30.8 to 21.2% and from 25.4 to 15.6%, respectively.The pests' mediated tree damage values were as follows: 17-24% for Y. malinellus Zell., 28.2-20.3%for A. rosana L., and 21.6-15% for C crataegana Hb.The wintered larvae of the first age of the apple ermine moth appear in mid-April, when the average daily temperature is usually above 13 • C. The apple ermine moth larvae (arachnid moth) start life in the open for 10-12 days upon the first shedding.Larvae completely eat leaf blades to the base of veins and weave arachnoid nests on paired leaves.The pupation period coincides with the time of dropping the excess ovary from 11-15 June to 1-5 July, depending on the development of larvae.Pupa develops 8-15 days (occasionally up to 20).Pupation takes place in dense white opaque cocoons densely grouped in packs of up to several hundred.The imago stage begins from 1 to 5 July, and the moths live 20-30 days, being active from early July to August and not needing additional nutrition.The active flight of moths is observed in twilight hours, while in the daytime, they hide on the underside of leaf blades.Mating occurs 2 weeks after dropping the pupae, and 5-6 days later, the imago begins to lay eggs.Embryonic development observably started from 21-25 July to 6-10 August.On average, a female apple moth lives for about a month, and a male apple moth lives for about twenty days.Larvae hatch from the eggs after 8-15 days in winter under moisture-proof shields (Figure 3).The life cycle of the apple ermine moth takes around 2-3 months to complete, and there can be multiple generations per year depending on the climate and conditions (Figure 4) [30,31].
hide on the underside of leaf blades.Mating occurs 2 weeks after dropping the pupae, and 5-6 days later, the imago begins to lay eggs.Embryonic development observably started from 21-25 July to 6-10 August.On average, a female apple moth lives for about a month, and a male apple moth lives for about twenty days.Larvae hatch from the eggs after 8-15 days in winter under moisture-proof shields (Figure 3).The life cycle of the apple ermine moth takes around 2-3 months to complete, and there can be multiple generations per year depending on the climate and conditions (Figure 4) [30,31].hide on the underside of leaf blades.Mating occurs 2 weeks after dropping the pupae, and 5-6 days later, the imago begins to lay eggs.Embryonic development observably started from 21-25 July to 6-10 August.On average, a female apple moth lives for about a month, and a male apple moth lives for about twenty days.Larvae hatch from the eggs after 8-15 days in winter under moisture-proof shields (Figure 3).The life cycle of the apple ermine moth takes around 2-3 months to complete, and there can be multiple generations per year depending on the climate and conditions (Figure 4) [30,31].-pupae; hide on the underside of leaf blades.Mating occurs 2 weeks after dropping the pupae, and 5-6 days later, the imago begins to lay eggs.Embryonic development observably started from 21-25 July to 6-10 August.On average, a female apple moth lives for about a month, and a male apple moth lives for about twenty days.Larvae hatch from the eggs after 8-15 days in winter under moisture-proof shields (Figure 3).The life cycle of the apple ermine moth takes around 2-3 months to complete, and there can be multiple generations per year depending on the climate and conditions (Figure 4) [30,31].tion.The active flight of moths is observed in twilight hours, while in the daytime, they hide on the underside of leaf blades.Mating occurs 2 weeks after dropping the pupae, and 5-6 days later, the imago begins to lay eggs.Embryonic development observably started from 21-25 July to 6-10 August.On average, a female apple moth lives for about a month, and a male apple moth lives for about twenty days.Larvae hatch from the eggs after 8-15 days in winter under moisture-proof shields (Figure 3).The life cycle of the apple ermine moth takes around 2-3 months to complete, and there can be multiple generations per year depending on the climate and conditions (Figure 4) [30,31].

Phenology of Archips rosana L.
During hibernation, the A. rosana L. overwinters and lays eggs in a single layer on the smooth bark of the lower part of an apple tree trunk or in the crutches of large branches in the Trans-Ili Alatau region.Larvae come out when the average daily temperature reaches 12-14 • C.Under the conditions of the Trans-Ili Alatau, this happens in the first half of April.The emergence of larvae from diapauses begins during the bud swelling period (Figure 5).

Phenology of Archips Rosana L.
During hibernation, the A. rosana L. overwinters and lays eggs in a single layer on the smooth bark of the lower part of an apple tree trunk or in the crutches of large branches in the Trans-Ili Alatau region.Larvae come out when the average daily temperature reaches 12-14 °C.Under the conditions of the Trans-Ili Alatau, this happens in the first half of April.The emergence of larvae from diapauses begins during the bud swelling period (Figure 5).Larvae of 1-2 ages feed on young swelling buds and shoots, and larvae of 2-3 ages penetrate into flower buds eating pistils and stamens.The rosebush leaf roller has the longest larvae stage, lasting from 11-15 April to 16-20 May, and this is due to the fact that this type of leaf roller has five development ages within the stage.Pupation begins on 21-25 May, lasting for about 10-14 days, then it passes into the adult imago stage from 26-30 May to 1-5 August.Females come out with a certain amount of matured eggs.Egg-laying begins 3-5 days after the flight of moths.By early August, a decline in imago is observed, and embryonic development begins [32].The stage at which pests are most vulnerable is the first stage, the appearance of larvae during April-May.According to our observations, pest flight outbreaks occur after precipitation.The adult rose leaf rollers emerge from their cocoons in the summer, after around two weeks in the pupal stage.The adult moths are small, light brown in color, and have a wingspan of about 1-1.5 cm.After mating, the female moth lays eggs on rosebush leaves, and the cycle starts again.In some regions, there can be up to three generations of rose leaf rollers per year [33].

Phenology of Cacoecia Crataegana Hb.
C. crataegana Hb. hibernate as eggs and then continue their development from April 21-25.Larvae hatch in the first stage, starting in May, at an average daily air temperature above 15-17 °C, which coincides with the budding phase of apple trees, and sprawl all over the crown.At the 1-3 instars, they damage unfolding buds, burgeons, and flowers or stay under curled edges of leaves.At the age of four, they build shelters by folding leaves along the main vein and fastening the edges with cocoon silk, not twisting the leaf-like rosebush leaf roller larvae do.Larvae of the last age live in leaf lumps at the tops of shoots.Most larvae accumulate in the outer part of the apple tree crown, in its middle and upper parts (Figure 6).Larvae of 1-2 ages feed on young swelling buds and shoots, and larvae of 2-3 ages penetrate into flower buds eating pistils and stamens.The rosebush leaf roller has the longest larvae stage, lasting from 11-15 April to 16-20 May, and this is due to the fact that this type of leaf roller has five development ages within the stage.Pupation begins on 21-25 May, lasting for about 10-14 days, then it passes into the adult imago stage from 26-30 May to 1-5 August.Females come out with a certain amount of matured eggs.Egg-laying begins 3-5 days after the flight of moths.By early August, a decline in imago is observed, and embryonic development begins [32].The stage at which pests are most vulnerable is the first stage, the appearance of larvae during April-May.According to our observations, pest flight outbreaks occur after precipitation.The adult rose leaf rollers emerge from their cocoons in the summer, after around two weeks in the pupal stage.The adult moths are small, light brown in color, and have a wingspan of about 1-1.5 cm.After mating, the female moth lays eggs on rosebush leaves, and the cycle starts again.In some regions, there can be up to three generations of rose leaf rollers per year [33].

Phenology of Cacoecia crataegana Hb.
C. crataegana Hb. hibernate as eggs and then continue their development from 21-25 April.Larvae hatch in the first stage, starting in May, at an average daily air temperature above 15-17 • C, which coincides with the budding phase of apple trees, and sprawl all over the crown.At the 1-3 instars, they damage unfolding buds, burgeons, and flowers or stay under curled edges of leaves.At the age of four, they build shelters by folding leaves along the main vein and fastening the edges with cocoon silk, not twisting the leaf-like rosebush leaf roller larvae do.Larvae of the last age live in leaf lumps at the tops of shoots.Most larvae accumulate in the outer part of the apple tree crown, in its middle and upper parts (Figure 6).
The larvae are active from the first half of May to the end of June.The hatching of larvae basically coincides with the apple tree budding phase.Larvae are passive migrants that spread on cocoon silk by winds over a considerable distance; therefore, they are often found in nurseries and orchards with the complete absence of clutches on fruit trees.Pupation occurs from 6 to 10 June.Moths fly from mid-June to mid-August, with the maximum flight occurring in mid-July during twilight hours and at night.Moths begin laying eggs 2-4 days later and continue to do so throughout their flight period.The entire life cycle takes about 6-8 weeks, and there can be multiple generations in a year depending on the climate and location.Control measures for hawthorn leaf rollers include pruning and removing infested plant parts, using insecticides, and promoting natural predators such as birds and parasitic wasps [34,35].The larvae are active from the first half of May to the end of June.The hatching of larvae basically coincides with the apple tree budding phase.Larvae are passive migrants that spread on cocoon silk by winds over a considerable distance; therefore, they are often found in nurseries and orchards with the complete absence of clutches on fruit trees.Pupation occurs from 6 to 10 June.Moths fly from mid-June to mid-August, with the maximum flight occurring in mid-July during twilight hours and at night.Moths begin laying eggs 2-4 days later and continue to do so throughout their flight period.The entire life cycle takes about 6-8 weeks, and there can be multiple generations in a year depending on the climate and location.Control measures for hawthorn leaf rollers include pruning and removing infested plant parts, using insecticides, and promoting natural predators such as birds and parasitic wasps [34,35].
Results of the experiments on the effect of temperature on the development of insects are presented in the graph below (Figure 7), which shows the main outbreaks of mass flight of imago at a temperature of 15-20 °C in mid-June and July.The larvae are active from the first half of May to the end of June.The hatching of larvae basically coincides with the apple tree budding phase.Larvae are passive migrants that spread on cocoon silk by winds over a considerable distance; therefore, they are often found in nurseries and orchards with the complete absence of clutches on fruit trees.Pupation occurs from 6 to 10 June.Moths fly from mid-June to mid-August, with the maximum flight occurring in mid-July during twilight hours and at night.Moths begin laying eggs 2-4 days later and continue to do so throughout their flight period.The entire life cycle takes about 6-8 weeks, and there can be multiple generations in a year depending on the climate and location.Control measures for hawthorn leaf rollers include pruning and removing infested plant parts, using insecticides, and promoting natural predators such as birds and parasitic wasps [34,35].
Results of the experiments on the effect of temperature on the development of insects are presented in the graph below (Figure 7), which shows the main outbreaks of mass flight of imago at a temperature of 15-20 °C in mid-June and July.

Figure 1 .
Figure 1.Map of the Ile-Alatau state national park location.

Figure 2 .
Figure 2. The study area.The Sievers apple trees in the Trans-Ili Alatau.

Figure 2 .
Figure 2. The study area.The Sievers apple trees in the Trans-Ili Alatau.

Figure 2 .
Figure 2. The study area.The Sievers apple trees in the Trans-Ili Alatau.

Figure 3 .
Figure 3. Phenograms of the development of the main representatives of Lepidoptera, damaging M.sieversii in the conditions of the Trans-Ili Alatau (data from the field seasons 2018-2019):

Figure 6 .
Figure 6.Stages of development of hawthornleaf roller (C.crataegana Hb.) in laboratory.(a) larvae, (b) pupae, (c) imago (Photos: Gulzhanat Tanabekova).Results of the experiments on the effect of temperature on the development of insects are presented in the graph below (Figure7), which shows the main outbreaks of mass flight of imago at a temperature of 15-20 • C in mid-June and July.

3. 5 .
The Effect of Temperature on the Development of Y. malinellus Zell.The emergence of larvae from hibernation under conditions of middle altitudes begins at an average daily temperature of 17 • C. The pupal stage lasts for about 10-14 days at an average temperature of 21 • C. Mass pupation takes place in the third week of May at an average daily temperature of 20-25 • C. Adult hatching occurs from late May to early August, with the massive flight of moths occurring in the second half of June at an average daily temperature of 28 • C. The life of an adult lasts between 8 and 30 days.By early August, there is a gradual decline in imago.Laying eggs begins in the third week (26 June 2019) at an average daily temperature of 30 • C.

Table 1 .
Geographic coordinates of the monitoring sites.

Table 2 .
Dominant species causing epiphytotic and economic loss, as well as their species breeding mass.

Table 3 .
Percentage damage to leaf blades and percentage damage to trees by dominant pests.