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Article

Possible Factors of Poplar Susceptibility to Large Poplar Borer Infestation

by
Valentyna Meshkova
1,*,
Kateryna Zhupinska
2,
Oleksandr Borysenko
3,4,
Olga Zinchenko
1,
Yuriy Skrylnyk
1 and
Natalia Vysotska
5
1
Department of Entomology, Phytopathology, and Physiology, Ukrainian Research Institute of Forestry & Forest Melioration, Pushkinska 86, UA-61024 Kharkiv, Ukraine
2
Department of Agronomy and Plant Protection, State Biotechnological University, Alchevskych 44, UA-61002 Kharkiv, Ukraine
3
Department of Geoinformation Technologies and Space Monitoring of the Earth, National Aerospace University «Kharkiv Aviation Institute», Chkalov Street 17, UA-61070 Kharkiv, Ukraine
4
Department of Remote Sensing, Tartu Observatory, University of Tartu, EE-61602 Toravere, Estonia
5
Institute of Forestry and Engineering, Estonian University of Life Sciences, Fr. R. Kreutzwaldi 5, 51006 Tartu, Estonia
*
Author to whom correspondence should be addressed.
Forests 2024, 15(5), 882; https://doi.org/10.3390/f15050882
Submission received: 2 April 2024 / Revised: 27 April 2024 / Accepted: 17 May 2024 / Published: 19 May 2024
(This article belongs to the Special Issue Forest Resistance to Insect Pests)
Browse Figures
Review Reports Versions Notes

Abstract

:
Poplars (Populus spp.) are of significant ecological and economic importance. Long-term breeding efforts were aimed mainly at obtaining fast-growing and productive plants and less considered resistance to pests. This study aimed to identify patterns of susceptibility or resistance to Saperda carcharias (Linnaeus, 1758) (Coleoptera: Cerambycidae) infestation among clones of Populus hybrids and pure species, focusing on the influence of their placement, seasonal development, stem diameter, height increment, and crossing combinations. Among 34 clones of poplar species and hybrids of Ukrainian and foreign selection, in 2019–2023 S. carcharias infested 14 clones every year. Six clones (‘Ivantiivska’, ‘Kytaiska × pyramidalna’, ‘Volosystoplidna’, ‘Novoberlinska-3’, ‘Robusta’, and ‘Lada’) were the most susceptible to the infestation by S. carcharias. The clones of all presented poplar sections and their crossing combinations, except the Tacamahaca and Leucoides cross, were infested. Greater height increment promoted the infestation by S. carcharias. Ambiguous results were obtained regarding the susceptibility of Populus hybrids compared to pure species to S. carcharias infestations. Considering infestation by S. carcharias and plant placement in the site, it can be concluded that the clones ‘Sakrau45-51’, ‘Deltopodibna’, ‘Rosijska’, ‘Slava Ukrayiny’, ‘Lubenska’, ‘Rohanska’, and ‘Nocturne’ are resistant to this pest. Selecting native species clones or creating mixed clone plantations could enhance the resilience of poplar plantations to pest threats.

1. Introduction

Poplar trees (Populus spp.) play a crucial role ecologically and economically due to their rapid growth and versatility in various applications, including timber production, bioenergy, and environmental remediation [1,2,3,4,5]. However, the Short Rotation Woody Crops (SRWC) yields are often reduced by a range of interacting environmental stressors, including frost [6], drought [7], salinity [8], pathogens [9], and phytophagous insects [10]. With climate change and increasing ecological pressures, understanding the complex interplay between insect herbivory resistance and the tolerance mechanisms to these abiotic stressors has become paramount. Dozens of species of phytophagous insects feed and develop in all organs of poplar, causing various effects on tree viability, growth rate, and wood quality [9,11,12]. The damage level depends on insect biological traits, population density, plant susceptibility, and environmental conditions [13,14,15,16,17].
Breeding efforts have historically focused on obtaining fast-growing and productive plants [18,19,20,21,22,23,24,25,26]. However, these plants had various responses to stress induced by abiotic factors of the environment and activities of living organisms within the environment. Particularly, as susceptibility to insect damage varies widely among clones, the limited genetic diversity of poplar in large SRWC areas may heighten the risk of pest-related losses or abiotic disasters [10].
Most studies of insect resistance in poplar hybrids and clones have focused on defoliators [12,13,17,27] because the foliage damage is visible and easy to quantify, and these insects can be controlled by spraying with an insecticide [9,11,28]. At the same time, phloem-boring or xylophagous insects at SRWC can, at high population densities, weaken trees in several ways. The first is adults feeding on leaves. The second is gnawing the galleries in trunks, branches, and roots. The third is actively or passively vectoring the pathogens, or promoting their penetration through entrance holes and development in weakened trees [14,15,29,30,31,32]. Some insects of this group have relatively low prevalence and harmfulness in forests but increase their population density at a single-species plantation, particularly Cryptorhynchus lapathi (Linnaeus, 1758) (Coleoptera: Curculionidae: Cryptorhynchinae), Saperda carcharias (Linnaeus, 1758) (Coleoptera: Cerambycidae), Cossus cossus (Linnaeus, 1758) (Lepidoptera: Cossidae), Paranthrene tabaniformis (Rottemburg, 1775) (Lepidoptera: Sesiidae) [9,11,12], and Anoplophora glabripennis Motschulsky, 1853 (Coleoptera: Cerambycidae) [32]. In eastern Ukraine, ten of 72 investigated xylophagous poplar species were rated as the most dangerous. However, most of them are highly harmful in the case of inhabiting over 60% of trees [14,15].
The large poplar longhorn beetle S. carcharias is one of the most dangerous poplar pests because it inhabits only living, healthy trees regardless of age [33,34], damages foliage and the bark of new growth at adult feeding [35,36], and promotes pathogen invasion [37] causing physiological harm [14]. The larva excavates a long and wide gallery deep into the wood [33,38], causing technical harm. The timber of damaged trees may be used for paper, pulp, or match production but not for saw timber, furniture, and veneering [39]. The life cycle of S. carcharias lasts 2 to 4 years, according to climatic conditions [40,41,42]. Even within the same tree, larvae develop in the upper part of the trunk for 2 years, and in the base of the trunk for 3–4 years [35,36]. The larvae pupate starting in May, depending on the instars of the hibernating individuals, and due to the heterogeneous temperature regime both within the plantation and in one tree, the emergence of adults and the colonization of new trees continues until September [40,41,42].
Since detecting the xylophagous insects in the early stages of tree colonization requires more effort than in the case of defoliators, and control is expensive and little effective [11], the best way to reduce negative consequences for plantation production is to increase the diversity of clones and hybrids [9].
A clone is a group of plants that reproduce vegetatively from a single parent individual (either a species or hybrid) and are genetically identical [43].
Fritz et al. [44] have suggested that clone resistance against herbivores is affected by hybridization in four different ways: 1—the same resistance of hybrids and parents, 2—intermediate resistance of hybrids compared to the parents, 3—hybrid susceptibility, and 4—hybrid resistance is close to either the more susceptible or more resistant parent. Responses of different insect species may vary widely to the same hybrid host. This indicates diverse genetic effects of interspecific hybridization on resistance.
The resistance of parental forms as a result of long-term coevolution may be one of the important factors of resistance to pests. For example, Manchurian ash (Fraxinus mandshurica Rupr.) coevolved with the emerald ash borer, Agrilus planipennis Fairmaire, 1888 (Coleoptera: Buprestidae), and is more resistant than North American or European ash species [45]. Usually, clones with the same parents have similar resistance. However, the progeny of P. trichocarpa is generally more resistant to caterpillar-like damage [17]. Research has shown that the cultivar ‘Robusta’ (Populus deltoides × P. nigra), obtained about 1910, is more susceptible to some insects than other P. deltoides × P. nigra crosses of more recent origin. At the same time, P. deltoides × P. nigra hybrids were damaged more intensively than P. trichocarpa (Torr. & Gray) clones [17].
In Ukraine, numerous studies have been carried out with hybrids P. deltoides, P. × euramericana, P. trichocarpa, P. laurifolia, and P. lasiocarpa, primarily focusing on growth [1,20,45,46,47,48] and biology [21,49,50,51]. However, modern studies on the resistance of poplar hybrids to insects are only starting in eastern Ukraine.
We assumed that the success of S. carcharias infestation depends not only on the clone features (for example, the beginning and end of the growing season, or growth intensity), but also on tree placement, management activity, etc.
This article aims to identify patterns of susceptibility or resistance to Saperda carcharias (Linnaeus, 1758) (Coleoptera: Cerambycidae) infestation among clones of Populus hybrids and pure species, focusing on the influence of their placement, seasonal development, stem diameter, height increment, and crossing combinations.

2. Materials and Methods

2.1. Study Region and Tested Poplar Clones

The experimental site is located on the territory of the State Enterprise “Kharkiv Forest Research Station”, 15 km from Kharkiv, in the Kharkiv region, Ukraine (50°05′01″ N, 36°18′25″ W, 156 m a.s.l.) (Figure 1). This area falls under the Forest-Steppe zone as per comprehensive forestry zoning [52]. Climate data obtained from ClimateCharts.net (Zepner et al., 2020) indicate an average annual temperature of +8.8 °C and an average annual rainfall of 535.2 mm for the period 2001–2020 [53]. The climate is classified as temperate continental (Dfb) according to the Köppen classification system [54].
Research was carried out in the collection of poplar (Populus sp.) and willow (Salix sp.) clones. The plot is flat, with a slight slope to the north. On the northern and western sides, it is bordered by deciduous forests, which include mainly Quercus robur L., Acer platanoides L., Tilia cordata Mill., and Ulmus laevis Pall. The rows of plants on the plantation are arranged from south to north. The distance between rows is 2 m, and between plants in a row, 2 m.
The cuttings, rooted the previous summer in an open field nursery and dormant for the winter, were planted in the spring of 2014. The plot encompasses 690 plants of 34 poplar clones, representing species and hybrids selected from the Aigeiros, Tacamahaca, and Leucoides sections (Table 1).
Inspection of poplars was carried out in 2019–2021 and 2023. In 2021, part of the trees on the plantation were cut to assess the biomass obtained from individual clones. In 2022, access to the plantation was impossible due to military operations. In 2023, it was discovered that the crowns of the pruned plants had been restored.

2.2. Weather Data Analysis

Mean monthly air temperature and precipitation for 1990–2020 for Kharkiv were taken from the ClimateCharts.net web platform [53], and respective weather indicators for the years of field research were taken from the website [55].
To compare the weather conditions of individual years, the following indicators were evaluated: average air temperature for a year (1) and vegetation period (period with air temperature over 10 °C) (2); the sum of precipitation for a year (3) and vegetation period (4); the dates of stable transition of temperature over 5 °C (5) and 10 °C (6); and hydrothermal index (HTI) (7).
The dates of stable transition of temperature over 5 and 10 °C were evaluated according to a method by V. Meshkova [56]. The G. T. Selyaninov hydrothermal index (HTI) was calculated as
H T I = 10 × ∑ P ∑ t
where ΣP is precipitation for a period with mean monthly air temperature over 10 °C, mm; Σt is the sum of daily air temperature for the same period, °C [57].

2.3. Field Data

Surveys of the distribution of phytophagous insects on plantations and assessment of the condition of clones were carried out in 2019–2021 and 2023. Each tree was labeled. When examining each plant, the stem diameter at the lower part was measured with a caliper. Plant condition (healthy, dead) and the presence of pest infestation were recorded (Figure 2, Table S1).
Particular attention was paid to identifying S. carcharias infestation. Characteristic signs of tree infestation by this pest differ from other wood borers, particularly Sesiidae or Cossidae [11,12]. Its presence at the site was evidenced by characteristic frass and foliage damage as a result of adult feeding of the adults (Figure 3a,b).
The frass of young larvae is white or light yellow because these larvae gnaw phloem. The frass of larvae after hibernation is dark and brown because those larvae gnaw sapwood. Therefore, we can distinguish fresh infestation. Usually, larvae overwinter once in our region. When the beetle flies out, a large exit hole is seen surrounded by frass. If the larva has died, no fresh frass is visible at the base of the trunk.
Galleries of this longhorn beetle inside the stem could be seen only after cutting the plant (Figure 3c,d).
Poplar infestation by S. carcharias was calculated as the ratio of infested and all plants of each clone expressed as a percentage. The error of this indicator was calculated considering the number of plants in a given clone, and the comparison of infestation for different clones was assessed using criterion Z [58,59]. Poplar infestation by S. carcharias was calculated as the ratio of infested and all plants of each clone expressed as a percentage of the number of inspected plants of a particular clone and year.
The rate of poplar foliage development was assessed on 10 plants of each clone by the following scoring scheme: 1—leaf buds completely enveloped by the scales; 2—bud swelling with scales slightly diverging showing a narrow yellow margin; the presence of one or more droplets of balsam; 3—bud sprouting, with tips of the small leaves emerging out of the scales; 4—buds completely opened with leaves still clustered together; scales still present; 5—leaves diverging with their blades still rolled up; scales may be present or absent; 6—leaves completely unfolded (but smaller in size than mature ones); lengthening of the axis of the shoot evident; scales absent [60].
The average score on the day of recording was calculated. Considering the preliminary assessment of the seasonal development of the clones, the arithmetic mean score of each clone, obtained from the assessment on April 20, was used for comparison. The clones with foliage in phase ≤ 3 were considered as late, 3.1–4 as medial, and 4.1–5 as early.
The annual growth of 10 plants of each clone was measured on 15 October 2019, using a pole, when the height of the trees did not exceed 3 m.
The stem diameter of all trees was measured in 2019, 2020, 2021, and 2023 at the end of vegetation.

2.4. Data Processing

All data were organized using the software Excel 2019. Software Open-source Python libraries (Pandas, NumPy, and Matplotlib) (Python 3.13.0) [61] and PAST: Paleontological Statistics Software Package for Education and Data Analysis [62] were used for data analysis and visualization.
The infestations of different clones or cut and uncut plants were compared using z-test in the two proportions comparisons [63,64]. Inputs were the proportions of infested clones, and outputs were z (observed value), |z| (critical value at significance level alpha = 0.05), and p-value (two-tailed). As the computed p-value was greater than the significance level alpha = 0.05, one cannot reject the null hypothesis H0 (the difference between the proportions is equal to 0). In another case, the difference between the proportions is different from 0 (hypothesis Ha).
The Cochran–Armitage trend test (the trend on proportions test) [65,66] was used to evaluate the dependence of poplar infestation by S. carcharias on tree placement (row, tree number in the row) site and year of research. Input data were the values of poplar infestation by S. carcharias for different scores of time or place. Output data were z (observed value), |z| (critical value at significance level alpha = 0.05), and p-value (two-tailed). As the computed p-value was greater than the significance level alpha = 0.05, one cannot reject the null hypothesis H0 (the difference between the proportions is equal to 0). In another case, the difference between the proportions is different from 0 (hypothesis Ha).

3. Results

3.1. Clones Infestation by S. carcharias Depending on Placement in Plantation

S. carcharias was the main stem pest in inspected poplar plantations in all years of research. Only two trees were infested by Saperda populnea (Linnaeus, 1758), and four trees by Sesia apiformis (Clerck, 1759) (Lepidoptera: Sesiidae).
Clone infestation by S. carcharias was uneven (Figure 2, Table 2).
Figure 2 shows that S. carcharias-infested trees on the site unevenly, and infestation was absent after the 20th row. Calculation of the average proportion of infested trees in each row and Cochran–Armitage trend test confirmed the decrease in poplar infestation by S. carcharias with row number (zobserved was −3.277 and −7.776, and p-value was 0.001 and <0.0001 in 2020 and 2023, respectively (z0.05 = 1.96)). At the same time, a high infestation occurred in rows 4, 6–7, 10–11, and 14–15, and in all rows in 2023 it is higher than in 2020 (Figure 4).
The proportion of trees infested by S. carcharias in different parts of the row varied from 15 to 30% (Figure 5), but Cochran–Armitage trend test did not confirm the dependence of this parameter on the tree number in the row (zobserved = 0.971; p = 0.331, which is greater than the significance level alpha = 0.05).

3.2. Effect of Cutting on S. carcharias Infestation

In 2021, S. carcharias had already infested 12% of poplars in plantations. After cutting in 2021 and restoring the crowns, in the survey of 2023, uncut trees amounted to 32.5%; trees after cutting with restored crowns—57.6%. S. carcharias was found in 18.8% and 26.3% of cut and uncut trees, respectively, which is not significant (z-observed =1.17; z0.05 = 1.96) (Figure 6).
Infestation of uncut and cut groups of trees by S. carcharias was higher in 2023 compared with 2021 (zobserved = 3.00; z0.05 = 1.96 and zobserved =2.93; z0.05 = 1.96, respectively); however, it was significantly greater in uncut trees (zobserved =2.12; z0.05 = 1.96) (see Figure 6).

3.3. Dynamics of Poplar Clones Infestation by S. carcharias

Infestation by S. carcharias increased for the years of assessment averaging from 6% in 2019 to 19.3% of all assessed plants in 2023. The trend of the infestation growth (Figure 7) was confirmed by Cochran–Armitage trend test (zobserved = 7.63; p-value < 0.0001; z0.05 = 1.96).
The increase in poplar infestation could be due to an increase in tree diameter and favorable weather conditions in these years. However, the differences in the diameter of infested and non-infested trees have not been confirmed statistically (Figure 8; zobserved = 0.006; p = 0.995; z0.05 = 1.96), although this parameter increased for 2019–2023 (p < 0.001).
In all years of the study, the annual air temperature in the plantation area exceeded long-term data: from 2.1 °C (by 23.7%) in 2019 to 0.4 °C (by 4.6%) in 2021 (Table 3). However, the temperature of the growing season exceeded long-term data to a lesser extent: from 1.8 °C (by 10.1%) in 2019 to 0.3 °C (by 1.9%) in 2021. The date of stable temperature transition over 5 °C was earlier by 10 days in 2019, 20 days in 2020, and 13 days in 2023. In 2021, this date was 4 days later than long-term data. However, the date of stable temperature transition over 10 °C was earlier than long-term data only in 2019 and 2023 (by 7 and 6 days, respectively), and in 2020 and 2021 it occurred 8 and 7 days later, respectively.
The annual precipitation in 2019–2021 was lower than long-term data (in 2019—by 180.1 mm, or by 34.5%). However, in 2023 it exceeded long-term data by 171.7 mm (32.9%). Precipitation for the growing season was almost twice less than the long-term values. In 2020, it was almost the same as the long-term values, and in 2023 it exceeded them by 23.3%. The hydrothermal index in 2019 was almost two times less than the long-term value, in 2020 it was almost equal to the long-term value, and in 2023 it even exceeded it (Table 3). Of the weather parameters considered, the highest positive correlation with the percentage of infested poplars is calculated for precipitation for year (r = 0.90) and growing season (r = 0.83) and for HTI (r = 0.82), but these values are not significant because of short observation period.
With a general trend towards an increase in infestation of trees by S. carcharias during the years of study, continuous growth in it was found only for 14 clones (Figure 8).
The increase in infestation over the years is statistically confirmed only for six clones (p < 0.05; particularly for two clones, p < 0.0001) (Table 4).
Three clones (‘Perspektyvna’, ‘Sakrau79’, and ‘Addita’ were infested only in 2023. In each of ‘Pioner’ and ‘Versia’, only one infested tree was found. Sixteen clones were not infested by S. carcharias at all.
To reveal the possible causes of various infestation levels of clones, some of their traits were analyzed.
The score of spring foliage development for poplar clones on April 20 did not differ for clones with S. carcharias presence and absence (zobserved = 1.57; Z0.05 = 1.96; p = 0.12). The average phase score on this data was 3.8 and 3.7 points for infested and non-infested clones, respectively. Early clones with a maximal score of spring foliage development (5 points) were present in both groups of clones. Minimal values of (clones with late spring development) were 2.9 and 2.2 for infested and non-infested clones, respectively.
The proportion of infested trees increased in the clones with the largest height increment (zobserved = 4.37; Z0.05 = 1.96; p < 0.0001). Average height increment of infested and non-infested clones was 97.8 and 74.8 cm, respectively, with maximums of 139.7 and 115.6 cm and minimums of 65.7 and 45.8 cm, respectively.

3.4. Infestation of Poplars by S. carcharias Depending on Clone Origin and Crossing Combination

S. carcharias infested clones of all tested poplar sections and their combinations, except T × L (Figure 9).
However, within each of the four susceptible combinations of sections, there were hybrids with high or low resistance to infestation by this pest (Figure 10). Among the hybrids from section Aigeiros, those with a maternal plant of American origin (P. deltoides) exhibited significantly higher susceptibility to infestation by S. carcharias compared with hybrids with a maternal plant of European origin (P. nigra) (Figure 10a).
Maternal plants of crossing combination A × L were also of American origin, and paternal (P. lasiocarpa) were of Asian origin. Although the S. carcharias infestation of the presented hybrids differed almost twice, the differences were not statistically confirmed (Figure 10b). In the A × L hybrid group, the clones with a maternal plant of Asian origin (P. suaveolens, P. simonii) were considerably more heavily infested compared with clones of European maternal lineage. However, the hybrid P. deltoides × P. balsamifera, descending from two American parents, showed no infestation (Figure 10c). P. trichocarpa plants were the most infested (44.2%) in the Tacamahaca section. Only 3.4% of plants having an American maternal and Asian paternal (P. trichocarpa × P. laurifolia) lineage were infested by S. carcharias, and the third member of this group having Asian origin (P. simonii f. fastigiata) was not infested at all (Figure 10d).
The data on clones infestation by S. carcharias in 2019–2023 and the influence of plant placement in the site allow for considering the clones ‘Sakrau45-51’, ‘Deltopodibna’, ‘Rosijska’, ‘Slava Ukrayiny’, ‘Lubenska’, ‘Rohanska’, and ‘Nocturne’ as conditionally resistant to this pest.

4. Discussion

In our research, 34 clones of poplar species and hybrids of Ukrainian and foreign selection from the Aigeiros, Tacamahaca, and Leucoides sections were tested in 2021 and 2023 for sustainability or resistance to infestation by S. carcharias in the plantation created in 2014 in Eastern Ukraine (Figure 1, Table 1).
Analysis of the scheme of infested poplar placement at the experimental plot (Figure 2) showed the necessity to evaluate the dependence of infestation by S. carcharias on row number and the placement of trees in the rows.
The decrease in the percentage of infested trees with row number was confirmed statistically (Figure 4). Clones in rows 18–25 were non-infested by S. carcharias. Of the 17th row, only one tree in each of ‘Pioner’ and ‘Versia’ was infested. At the same time, non-infested clones were also found in rows 5 (‘Nocturne’), 6 (‘Rosijska’), 7 (‘Deltopodibna’), 9 (‘Slava Ukrayiny’), 12 (‘Rohanska’), 14 (‘Sakrau45-51’) and 16 (‘Lubenska’).
The effect of plant placement within a row on infestation by S. carcharias has not been statistically confirmed (Figure 5). Among the poplars growing at the beginning and at the end of the row, both infested and non-infested clones were represented.
Infestation of uncut and cut trees by S. carcharias was higher in 2023 compared with 2020; however, it was significantly greater in uncut trees (Figure 6). This may be because after cutting, a part of the trunk was left with insufficient height for the galleries of S. carcharias. However, the plants were cut at a height of about 40 cm, and the length of the galleries in the dissected plants from which the adults emerged did not exceed 17 cm (our unpublished data). It is possible also that wood moisture decreased after cutting, which was unfavorable for larvae development [67].
Fourteen clones were infested by S. carcharias throughout the years, and its number increased over the years, which was confirmed statistically (Figure 7). In all years of assessment, the clone ‘Ivantiivska’ was the most infested by S. carcharias. Three more clones (‘Kytaiska × pyramidalna’, ‘Karolinska 162’, and ‘Volosystoplidna’) had over 50% infestation in 2023.
We assumed the increase in poplar infestation was due to an increase in tree diameter and favorable weather conditions. It is known [16,33,34,35,36] that S. carcharias infests trees of different ages and diameters, and it even colonizes the same tree with enough diameter several times. However, the differences in diameter increase in infested and non-infested trees were not confirmed statistically (Figure 8). At the same time, the infestation of clones with greater height increments was confirmed, which is consistent with data on the attractiveness of larger trees for S. carcharias [16,68] because the plants with greater height increments usually have greater radial increments [52] and sufficient wood volume for larvae development [39].
In all years of the study, the annual air temperature in the plantation area exceeded long-term data, but the dates of the stable temperature transition over 10 °C occurred earlier than long-term data in 2019 and 2023 by 7 and 6 days, respectively (Table 3). Such variations could affect the attractiveness, suitability, and susceptibility of poplars to S. carcharias and larvae development inside the trunk. This warrants further investigation into their role in pest infestation dynamics. In our research, the precipitation and hydrothermal index in 2019–2021 were inferior to long-term data, and in 2023 exceeded them (see Table 3). Lack of precipitation usually promotes phytophagous insect development, while its increase promotes tree resistance [56,69,70,71]. Since the development length of S. carcharias larvae in the poplar trunk varies depending on locality and year, this aspect is also advisable for further study in different clones. However, of the weather parameters considered, the high positive correlation of the percentage of infested poplars with precipitation and HTI (r > 0.9) was not significant because of short observation period.
The high reliability of the increase in infestation over the years was confirmed only for six clones (p < 0.05; particularly for two clones, p < 0.0001) (Table 4). Sixteen clones were not infested by S. carcharias at all.
In Canada, poplar clones resistant to Cryptorhynchus lapathi (L.) (Coleoptera: Curculionidae) were flushed approximately three weeks earlier than the susceptible clones [72]. However, C. lapathi larvae mine in the bark while developing through three instars, and then move into the xylem, while S. carcharias larvae immediately gnaw a gallery to the sapwood [11,12]. We suggested that S. carcharias prefers the plants with earlier leaf development due to the availability of the foliage for adult feeding, which then becomes able to mate and lay eggs on nearby trees. However, the difference in the rate of spring foliage development for infested and non-infested poplar clones was not confirmed statistically in our research, which may be related to a relatively short period of research.
S. carcharias showed a wide capacity to infest clones across all presented poplar sections and their crossing combinations, except the Tacamahaca and Leucoides cross (Figure 9 and Figure 10). Within each crossing combination, there was a discernible variation in susceptibility levels. This variation underscores the complex nature of hybrid resistance, suggesting that neither clone origin nor crossing combination alone can predict susceptibility to S. carcharias.
The studies have provided mixed results regarding the susceptibility of Populus hybrids compared to pure species in the face of pest infestations. In Sweden, Christersson [18] found that hybrids P. trichocarpa and P. deltoides were more prone to pest attacks, unlike their pure P. trichocarpa counterparts which were largely spared. In Canada, Kalischuk et al. [73] reported that poplar hybrids suffered severe infestations by poplar bud gall mites, and no trees were severely infested in areas where pure poplars grew.
Contrary to these findings, in Latvia, in the study by Zeps et al. [37], infestations of hybrid and European aspen by poplar borer and rots have no significant differences. In Finland, Välimäki and Heliövaara’s [38] research indicates no significant difference in poplar borer larval galleries between aspens and hybrid aspens. A study by Moore and Wilson [74] in Michigan found no discernible preference by S. inornata for hybrid over pure Populus species, despite attacking a substantial proportion of the population. This lack of preference challenges the notion that Populus hybrids are inherently more vulnerable to pests.
Among the hybrids from section Aigeiros, those with a maternal plant of American origin (P. deltoides) exhibited higher susceptibility to infestation. Conversely, hybrids with a maternal plant of European origin (P. nigra) showed significantly lower infestation levels. This pattern suggests a pivotal role of maternal lineage in determining hybrid susceptibility to pest attacks.
For the crossing combinations of Aigeiros and Leucoides, P. deltoides × P. lasiocarpa showed a significantly high infestation rate, while P. × canadensis cv. ‘Regenerata’ × P. lasiocarpa had a lower infestation rate, suggesting variability in pest resistance even within specific crossing combinations.
In the Aigeiros and Tacamahaca hybrid group, clones with a maternal plant of Asian origin (P. suaveolens, P. simonii) were more heavily infested, while those with European maternal lineage were less affected. Interestingly, the hybrid P. deltoides × P. balsamifera, descending from two American parents, showed no infestation, highlighting the complexity of genetic influences on pest resistance. The experience of Hannon et al. [29] suggests that hybrids with P. deltoides × P. nigra parentage are more resistant to stem borers than with P. trichocarpa × P. deltoides or P. trichocarpa × P. nigra parentage.
Among the representatives of section Tacamahaca, P. trichocarpa were significantly more susceptible to S. carcharias infestation. However, a genome-wide association study (GWAS) conducted by Sepúlveda et al. [31] on P. trichocarpa provenances revealed three SNP markers significantly associated with resistance to S. calcarata. This discovery indicates that P. trichocarpa employs a sophisticated machinery of genetic expression and metabolite production to fend off S. calcarata attacks in different conditions. Another representative with an American maternal and Asian paternal (P. trichocarpa × P. laurifolia) lineage exhibited low infestation rates. The third representative, of Asian origin (P. simonii f. fastigiata), was not infested, suggesting a potential genetic basis for resistance.
At the same time, as was shown above, in addition to the genetic properties of clones, environmental factors play an important role in tree resistance to infestation by S caecharias, in particular, related to location on the plantation (see Table 2). Thus, when comparing clones with the same crossing combinations located in different rows, it was found that ‘Perspektyvna’ was not inhabited in the 20th row and was single-inhabited in the eighth row. ‘Robusta’ was populated in the 10th row and not populated in the 25th row. ‘Novoberlinska-3’ was in the fourth row and was not populated in the 17th row. However, ‘Sakrau45-51’ was not populated either in rows 14 or 20, and ‘Sakrau79’ was populated singly in row 8. At the same time, ‘Ivantiivska’ in row 7 was the most populated in all years of assessment.
The data on clones infestation by S. carcharias in 2019–2023 and the influence of plant placement in the site allow for considering the clones ‘Sakrau45-51’, ‘Deltopodibna’, ‘Rosijska’, ‘Slava Ukrayiny’, ‘Lubenska’, ‘Rohanska’, and ‘Nocturne’ as conditionally resistant to this pest.
The findings underscore the importance of considering both maternal lineage and specific hybrid genetic makeup and of environmental factors in poplar breeding to enhance resistance to pest infestations. It is necessary to take into account that the resistance of the same clones to insects of different ecological groups (defoliators, xylophages, pests of reproductive organs) and species, as well as to pathogens and unfavorable environmental factors (frost, drought, and salinity), is different. Therefore, the influence of these factors needs to be studied in complex research for creating mixed clone plantations [9].

5. Conclusions

In 2019–2023, S. carcharias infested every year 14 poplar clones of 34 inspected clones of poplar species and hybrids of the Ukrainian and foreign selection in the plantation created in 2014 in Eastern Ukraine. Six clones (‘Ivantiivska’, ‘Kytaiska × pyramidalna’, ‘Volosystoplidna’, ‘Novoberlinska-3’, ‘Robusta’, and ‘Lada’) were the most susceptible to the infestation by S. carcharias, for which the increase in infestation over the years was statistically confirmed. Greater height increment promoted the infestation by S. carcharias. The clones of all presented poplar sections and their crossing combinations, except the Tacamahaca and Leucoides cross, were infested. However, the data on the susceptibility of Populus hybrids compared to pure species to S. carcharias infestations were ambiguous. The influence of plant placement in the site on infestation by S. carcharias was confirmed statistically. The data obtained allow for considering the clones ‘Sakrau45-51’, ‘Deltopodibna’, ‘Rosijska’, ‘Slava Ukrayiny’, ‘Lubenska’, ‘Rohanska’, and ‘Nocturne’ as conditionally resistant to this pest.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/f15050882/s1, Table S1: Database of tested clones’ health condition.

Author Contributions

Conceptualization, V.M.; methodology, V.M. and N.V.; software, O.B. and N.V.; validation, O.B. and N.V.; formal analysis, V.M., N.V. and Y.S.; investigation, V.M., N.V., Y.S., K.Z. and O.Z.; data curation, K.Z., O.Z. and Y.S.; writing—original draft preparation, V.M. and N.V.; writing—review and editing, V.M., N.V. and Y.S.; visualization, O.B. and N.V.; supervision, V.M. All authors have read and agreed to the published version of the manuscript.

Funding

The paper was prepared by the authors in the framework of a research plan of URIFFM (grant 0120U101891), which was supported by the State Forest Resources Agency of Ukraine.

Data Availability Statement

Data are available upon email request to the corresponding author.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Location of study plot in the map of Kharkiv region (Ukraine).
Figure 1. Location of study plot in the map of Kharkiv region (Ukraine).
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Figure 2. Placement of alive, dead, cut, and infested by S. carcharias plants at the experimental plot in 2020 (before cutting) and in 2023 (after cutting) (0—S. carcharias is absent; 1—S. carcharias is present).
Figure 2. Placement of alive, dead, cut, and infested by S. carcharias plants at the experimental plot in 2020 (before cutting) and in 2023 (after cutting) (0—S. carcharias is absent; 1—S. carcharias is present).
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Figure 3. Signs of S. carcharias in plantation: (a) frass at the base of the trunk, chips, and streaks are visible; (b) adult feeding of an adult; (c) a gallery inside the stem; (d) cross-section in the lower part of infested poplar stem.
Figure 3. Signs of S. carcharias in plantation: (a) frass at the base of the trunk, chips, and streaks are visible; (b) adult feeding of an adult; (c) a gallery inside the stem; (d) cross-section in the lower part of infested poplar stem.
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Figure 4. Percentage of poplar trees infested by S. carcharias in different rows of trees in 2020 and 2023.
Figure 4. Percentage of poplar trees infested by S. carcharias in different rows of trees in 2020 and 2023.
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Figure 5. Percentage of poplar trees infested by S. carcharias in different parts of rows (grouped by 5 trees).
Figure 5. Percentage of poplar trees infested by S. carcharias in different parts of rows (grouped by 5 trees).
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Figure 6. Percentage of poplar trees infested by S. carcharias in 2021 (before cutting) and 2023 (after cutting). The infestation of groups of trees with the same letters in parentheses has no significant difference at p = 0.05.
Figure 6. Percentage of poplar trees infested by S. carcharias in 2021 (before cutting) and 2023 (after cutting). The infestation of groups of trees with the same letters in parentheses has no significant difference at p = 0.05.
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Figure 7. The percentage of trees infested by S. carcharias in poplar clones in 2019–2023 (clones are sorted by descending order of infestation by S. carcharias in 2023; non-infested clones are not shown). Bars—stand. errors. Clones abbr. and full names: Iv—‘Ivantiivska’, Kp—‘Kytaiska × pyramidalna’, Ka—‘Karolinska 162’, Vo—‘Volosystoplidna’, Lv—‘Lvivska’, N3—‘Novoberlinska-3’, Rob—‘Robusta’, La—‘Lada’, Tr—‘Tronco’, Udv—‘Udyvytelnaya’, Ve—‘Veryla’, St—‘Strilopodibna’, Cn—‘Constanta’, Bh—‘Bachelieri’.
Figure 7. The percentage of trees infested by S. carcharias in poplar clones in 2019–2023 (clones are sorted by descending order of infestation by S. carcharias in 2023; non-infested clones are not shown). Bars—stand. errors. Clones abbr. and full names: Iv—‘Ivantiivska’, Kp—‘Kytaiska × pyramidalna’, Ka—‘Karolinska 162’, Vo—‘Volosystoplidna’, Lv—‘Lvivska’, N3—‘Novoberlinska-3’, Rob—‘Robusta’, La—‘Lada’, Tr—‘Tronco’, Udv—‘Udyvytelnaya’, Ve—‘Veryla’, St—‘Strilopodibna’, Cn—‘Constanta’, Bh—‘Bachelieri’.
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Figure 8. Diameter of trees in poplar clones infested by S. carcharias (2019-1, 2020-1. 2021-1, 2023-1) and non-infested (2019-0, 2020-0. 2021-0, 2023-0) in different years (whiskers—minimum and maximum, box—first and third quartiles, central line is median; points—outliers).
Figure 8. Diameter of trees in poplar clones infested by S. carcharias (2019-1, 2020-1. 2021-1, 2023-1) and non-infested (2019-0, 2020-0. 2021-0, 2023-0) in different years (whiskers—minimum and maximum, box—first and third quartiles, central line is median; points—outliers).
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Figure 9. Proportion of poplar clones infested by S. carcharias, depending on the group of sections. The columns with the same letters have no significant difference at p = 0.05. Sections: A—Aigeiros, T—Tacamahaca, and L—Leucoides.
Figure 9. Proportion of poplar clones infested by S. carcharias, depending on the group of sections. The columns with the same letters have no significant difference at p = 0.05. Sections: A—Aigeiros, T—Tacamahaca, and L—Leucoides.
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Forests 15 00882 g010aForests 15 00882 g010b
Figure 10. The proportion of poplar clones infested by S. carcharias, depending on crossing combinations in the groups of sections: (a)Section A; (b) A × L; (c) A × T; (d) Section T. The columns with the same letters in parentheses have no significant difference at p = 0.05. The abbreviations of crossing combinations are mentioned in Table 1.
Figure 10. The proportion of poplar clones infested by S. carcharias, depending on crossing combinations in the groups of sections: (a)Section A; (b) A × L; (c) A × T; (d) Section T. The columns with the same letters in parentheses have no significant difference at p = 0.05. The abbreviations of crossing combinations are mentioned in Table 1.
Forests 15 00882 g010aForests 15 00882 g010b
Table 1. Tested poplar clones.
Table 1. Tested poplar clones.
Section Abbr. *Hybrids/Crossing Combination
(Abbr. in Parentheses)		Clone Name (Abbr. and Number of Trees in Parentheses)Ref. **
AP. × canadensis (Pc)‘Bachelieri’ (Bh; 33), ‘Constanta’ (Cn; 36), ‘Robusta’ (Rob; 17), ‘Robusta 16’ (Rob16; 8), ‘Sakrau45-51’ (Sk45; 26), ‘Sakrau79’ (Sk79; 8), ‘Tronco’ (Tr; 10), ‘Veryla’ (Ve; 28)[39,46,49]
AP. deltoides (Pd)‘Gulliver’ (Gu; 22), ‘Deltopodibna’ (De; 14), ‘Karolinska 162’ (Ka; 7)[46,49]
AP. deltoides × P. nigra cv. ‘Italica’
(Pd × PnIt)		‘Strilopodibna’ (St; 40) [47]
AP. nigra × P. deltoides (Pn × Pd)‘Gradizka’ (Gr), ‘Keliberdynska’ (Ke)[39,46]
AP. nigra × P. nigra cv. ‘Italica’
(Pn × PnIt)		‘Addita’ (Ad; 14), ‘Pioner’ (Pi; 13), ‘Rosijska’ (Ro; 12)[39,49]
AP. nigra cv. ‘Pyramidalis’ (PnPrm)‘Slava Ukrayiny’ (Sl; 17)[46]
TP. trichocarpa (Pt)‘Lada’ (La; 18), ‘Volosystoplidna’ (Vo; 30) [49]
TP. trichocarpa × P. laurifolia (Pt × Plrf)‘Druzhba’ (Dr; 29)[49]
TP. simonii f. fastigiata (PsimF)‘Rohanska’ (Rh; 32)[49]
A × LP. × canadensis cv. ‘Regenerata’ ×
P. lasiocarpa (PcRg × Pls)		‘Perspektyvna’ (Pe; 41)[46]
A × LP. deltoides × P. lasiocarpa (Pd × Pls)‘Udyvytelnaya’ (Udv; 18)[46]
A × TP. × canadensis × P. trichocarpa (Pc ×Pt)‘Lvivska’ (Lv; 27), ‘Mobilna’ (Mo; 17)[46]
A × TP. deltoides × P. balsamifera (Pd × Pbls)‘Kanadska×balsamichna’ (KB; 14)[49]
A × TP. nigra cv. ‘Italica’ × P. laurifolia (PnIt × Plrf)‘Novoberlinska-3’ (N3; 28); ‘Novoberlinska-7’ (N7; 18) [46,49]
A × TP. nigra cv. ‘Italica’ × P. trichocarpa (PnIt × Pt)‘Lubenska’ (Lu; 13)[46]
A × T(P. nigra cv. ‘Italica’ × P. nigra) × P. balsamifera (PnIt × Pn × Pbls)‘Versia’ (Vr; 24)[46]
A × TP. suaveolens ×P. × berolinensis
(Psv × Pbrl)		‘Ivantiivska’ (Iv; 20)[47,49]
A × TP. simonii × P. nigra cv. ‘Italica’
(Psim × PnIt)		‘Kytaiska × pyramidalna’ (Kp; 14)[47]
T × LP. trichocarpa × P. lasiocarpa (Pt × Pls)‘Nocturne’ (No; 17)[47,49]
Notes: * A—Aigeiros, T—Tacamahaca, L—Leucoides; ** References point to mentioning the names of clones in publications. This is especially important since most of the clones were obtained in Ukraine and have names in Ukrainian.
Table 2. Characteristics of poplar clones placement and the fact of infestation by S. carcharias.
Table 2. Characteristics of poplar clones placement and the fact of infestation by S. carcharias.
Clone NameAbbr. RowPlace in the Row *Number of PlantsInfestation **
‘Bachelieri’Bh4end331
‘Constanta’Cn5end361
‘Sakrau79’Sk798end8single
‘Robusta’Rob10end171
‘Veryla’Ve11start281
‘Tronco’Tr13start101
‘Sakrau45-51’Sk4514end70
‘Sakrau45-51’Sk4520start190
Robusta 16’Rob1625start80
‘Deltopodibna’De7start140
‘Karolinska 162’Ka10start71
‘Gulliver’Gu23start220
‘Strilopodibna’St16start401
‘Rosijska’Ro6end120
‘Addita’Ad12end14single
‘Pioner’Pi17end13single
‘Keliberdynska’Ke21start220
‘Gradizka’Gr22start110
‘Slava Ukrayiny’Sl9start170
‘Perspektyvna’Pe8start25single
‘Perspektyvna’Pe20end160
‘Udyvytelnaya’Udv9end181
‘Versia’Vr19start24single
‘Lvivska’Lv14start271
‘Mobilna’Mo24start170
‘Kanadska×balsamichna’KB18end140
‘Novoberlinska-3’N34start281
‘Novoberlinska-7’N717start180
‘Lubenska’Lu16end130
‘Kytaiska × pyramidalna’Kp11end141
‘Ivantiivska’Iv7end211
‘Rohanska’Rg12start330
‘Volosystoplidna’Vo6start301
‘Lada’La15start181
‘Druzhba’Dr18start290
‘Nocturne’ No5start170
Notes: * start—from the row beginning; end—in the half part of row, usually after 50 m from row beginning; ** 0—infestation by S. carcharias was absent in all years; 1—infestation by S. carcharias was present in all years; single—one infested tree.
Table 3. Climatic indicators for 1990–2020 and the years of field research for Kharkiv meteorological station.
Table 3. Climatic indicators for 1990–2020 and the years of field research for Kharkiv meteorological station.
Climatic Indicators *1990–20202019202020212023
Air temperature, T °C
—for year8.810.810.49.210.3
—for the growing season 17.419.217.917.818.2
Date of stable transition of temperature
—over 5 °C29/0319/039/032/0416/03
—over 10 °C16/049/0424/0423/0410/04
Precipitation, mm
—for year535.2342.3494.6399.0694.1
—for the growing season287.2159.4285.1217.8354.2
Hydrothermal index, HTI0.900.450.870.671.06
* Note: data for 2022 are not full because of military actions.
Table 4. Cochran–Armitage trend test of poplar clones infestation by S. carcharias in 2019–2023 (z0.05 = 1.96).
Table 4. Cochran–Armitage trend test of poplar clones infestation by S. carcharias in 2019–2023 (z0.05 = 1.96).
Clone NameAbbr.Zobservedp-Value (Two-Tailed)
‘Ivantiivska’Iv3.390.001
Kytaiska × pyramidalna’Kp2.660.01
‘Karolinska 162’Ka1.760.08
‘Volosystoplidna’Vo3.51<0.0001
‘Lvivska’Lv0.980.33
‘Novoberlinska-3’N33.94<0.0001
‘Robusta’Rob2.620.01
‘Lada’La2.210.03
‘Tronco’Tr1.190.24
‘Udyvytelnaya’Udv1.900.6
‘Veryla’Ve1.410.16
‘Strilopodibna’St1.280.20
‘Constanta’Cn2.190.03
‘Bachelieri’Bh1.350.18
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Meshkova, V.; Zhupinska, K.; Borysenko, O.; Zinchenko, O.; Skrylnyk, Y.; Vysotska, N. Possible Factors of Poplar Susceptibility to Large Poplar Borer Infestation. Forests 2024, 15, 882. https://doi.org/10.3390/f15050882

AMA Style

Meshkova V, Zhupinska K, Borysenko O, Zinchenko O, Skrylnyk Y, Vysotska N. Possible Factors of Poplar Susceptibility to Large Poplar Borer Infestation. Forests. 2024; 15(5):882. https://doi.org/10.3390/f15050882

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Meshkova, Valentyna, Kateryna Zhupinska, Oleksandr Borysenko, Olga Zinchenko, Yuriy Skrylnyk, and Natalia Vysotska. 2024. "Possible Factors of Poplar Susceptibility to Large Poplar Borer Infestation" Forests 15, no. 5: 882. https://doi.org/10.3390/f15050882

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