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 [
27], 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]. It 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]. 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 [
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 by maturation feeding on leaves, gnaw the galleries of different diameters and at different depths in trunks, branches, and roots, actively or passively vector the pathogens, or create conditions for the penetration of pathogens through entrance holes and promote their development by weakening the trees [
14,
15,
29,
30,
31,
32]. Some insects of this group have relatively low prevalence and harmfulness in forests but increase the 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 [
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].
Large poplar longhorn beetle
S. carcharias is one of them because it inhabits only living, healthy trees regardless of age [
33,
34], damages foliage and the bark of new growth at maturation feeding [
35,
36], and promotes the 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].
Fritz et al. [
43] have suggested that clone resistance against herbivores is affected by hybridization in four different ways: the same resistance of hybrids and parents, intermediate resistance of hybrids compared to the parents, hybrid susceptibility, and hybrid resistance is close to either more susceptible or more resistance 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 emerald ash borer,
Agrilus planipennis Fairmaire, 1888 (Coleoptera: Buprestidae) and is more resistant than North American or European ash species [
44]. 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 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, P. lasiocarpa primarily focusing on growth [
1,
20,
45,
46,
47,
48,
49,
50,
51] and biology [
21,
52]. However, modern studies on the resistance of poplar hybrids to insects are only starting in eastern Ukraine.
This article aims to identify patterns of susceptibility or resistance to Saperda carcharias (Linnaeus, 1758) (Coleoptera: Cerambycidae) infestation among Populus hybrids and pure species, focusing on the influence of their seasonal development, stem diameter, height increment, and crossing combinations.
4. Discussion
In our research, 35 clones of poplar species and hybrids of the 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.
Infestation by
S. carcharias was higher in 2023 compared with 2020 for most clones (
Figure 5). In both 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.
12 clones were not infested in both years, particularly, ‘Deltopodibna’, Gradizka’, ‘Gulliver’, ‘Kanadska × balsamichna’, ‘Lubenska’, ‘Mobilna’, ‘Nocturne’, ‘Novoberlinska-7’, ‘Robusta 16’, ‘Rohanska’, ‘Sakrau45-51’, ‘Slava Ukrayiny’. To reveal the possible causes of various infestation levels of clones, some of their traits were analyzed.
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, and occurred 8 and 7 days later it in 2020 and 2021 (see
Table 2). 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 2). Lack of precipitation usually promotes phytophagous insect development while its increase promotes tree resistance [
56]. 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.
Infestation of uncut and cut trees by
S. carcharias was higher in 2023 compared with 2020, however, it was significantly greater in uncut trees (see
Figure 4). 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.
In our research, the clones with earlier foliage development were more susceptible to infestation (see
Figure 6a), while the dates of the fall had no significant impact on
S. carcharias presence (
Figure 6b). However, in Canada, resistant to
Cryptorhynchus lapathi (L.) (Coleoptera: Curculionidae) poplar clones were flushed approximately three weeks earlier than the susceptible clones [
63]. The conflicting findings may be because
C. lapathi larvae mine in the bark while developing through three instars, and then move into the xylem, while
S. carcharias larva immediately gnaws a gallery to the sapwood. The choice of plants with earlier leaf development may be explained by the availability of foliage for
S. carcharias maturation feeding, which then becomes able to mate and lay eggs on nearby trees.
The dates of the fall have no significant impact on clone infestation by
S. carcharias because it needs foliage only for maturation feeding after adult emergence, which goes on from May to August [
35,
36].
In our research,
S. carcharias preferred colonizing clones with larger diameters (
Figure 7a) and height increments (
Figure 7b). The first may be because the larva cannot complete its development in young plants with insufficient wood volume. The second phenomenon may be because the plants with greater height increments usually have greater radial increments [
53] and sufficient wood volume for larvae development [
39].
S. carcharias showed a wide capacity to infest clones across all presented poplar sections and their crossing combinations, except the Tacamahaca and Leucoides cross. 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] has studied 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. [
64] 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, the study by Zeps et al. [
37], no significant differences in susceptibility of rot and poplar borer were found between hybrid and European aspen. 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 [
65] 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
P. trichocarpa ×
P. deltoides or
P. trichocarpa ×
P. nigra parentage.
Among the representatives of section
Tacamahaca,
P. trichocarpa was 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.
When sorting non-infested clones by parent origin, it was observed that European and American species were more prevalent by plant count, whereas European-American and European-Asian hybrids dominated by clone count. This distribution suggests a nuanced relationship between genetic background and pest resistance, warranting further exploration into the specific genetic or environmental factors that confer resilience against S. carcharias infestation. Hybrids with European maternal lineage generally exhibited lower susceptibility to pest infestations, suggesting a robust genetic basis for resistance within these lines. Hybrids derived from American maternal lineage tend to be more vulnerable to pests, necessitating careful consideration in breeding programs aiming for pest-resistant poplar cultivars. The presence of Asian maternal lineage or complex crossing combinations involving Asian lineage can result in higher susceptibility.
The findings underscore the importance of considering maternal lineage and specific hybrid genetic makeup when developing poplar breeding strategies to enhance resistance to pest infestations. Further research into the genetic and environmental interactions influencing these susceptibility patterns is crucial for advancing pest-resistant poplar cultivation.
The exploration of alternative strategies, such as the utilization of selected clones of native species or the creation of mixed clone plantations, emerges as a viable path toward the sustainable development of poplar plantations resilient to the dynamic threats of pests and pathogens. Our results corroborate the alternative strategy proposed by Biselli et al. [
9] about creating mixed clone plantations, which emerge as viable paths toward the sustainable development of poplar plantations resilient to the dynamic threats of pests and pathogens.
Insect herbivory resistance, a key trait in poplar trees, influences their ability to withstand and recover from damage caused by herbivorous insects. This resistance trait is critical for maintaining tree health and productivity. On the other hand, the ability of hybrid poplars to tolerate environmental stresses like frost, drought, and salinity can significantly affect their survival and growth in diverse ecosystems. These abiotic stressors are becoming more pronounced due to changing climate patterns and land-use practices, making it imperative to investigate how insect herbivory resistance may interact with the trees’ abilities to tolerate such stressors. Further research into the genetic and environmental interactions influencing these susceptibility patterns is crucial for advancing pest-resistant poplar cultivation.