Among the factors contributing to the initiation of outbreaks of the Siberian moth, a dangerous pest of the coniferous forests of Northern Eurasia, it is considered important to reduce the regulatory impact of entomophages. One of the most effective regulators of the pest abundance is the egg parasitoid wasp Telenomus tetratomus (Thomson, 1861). There is an established opinion that T. tetratomus is less cold-resistant than caterpillars of the Siberian moth, and outbreaks of the pest are provoked by cold winters, during which conditions (low temperatures and low snow cover depth) are tolerated by the moth caterpillars but lead to death of the parasitoid. However, the lethal temperature for T. tetratomus was determined in an insufficiently controlled experiment more than 60 years ago. We evaluated one of the cold hardiness characteristics of T. tetratomus, the supercooling point (SCP), which had not been measured previously. Both the host and the parasitoid overwinter in a supercooled state, and freezing is lethal to both. The mean SCP of T. tetratomus (-21.2±0.2 °C) was found to be 6.3 °C lower than the SCP of Siberian moth caterpillars. Comparison of SCP distributions and mortality rates at several temperatures allows us to tentatively estimate 50% mortality temperature of the wasp – about -16 °C. The obtained result, analysis of temperatures in the litter of various types of coniferous forests, and published data indicate that the asynchronous mortality of the host and its main parasitoid during wintering, due to differences in cold hardiness, can be considered as the cause of outbreaks of the Siberian moth mass reproduction only with caution.

Dendrolimus sibiricus, lower lethal temperatures, supercooling point, surviving, West Siberia

The Siberian moth, Dendrolimus sibiricus Tschetv., is a well-known dangerous pest of coniferous forests in North Asia. In addition to the Asian part of Russia and Northern Kazakhstan, it is found in North China, Northern Mongolia and on the Korean Peninsula; its larvae infest and defoliate more than 20 species of Abies, Pinus, Larix, Picea and Tsuga (Gninenko and Orlinskii 2002). In the 20^th century, the range expansion of the pest to the west was noted; by the 1950s, this species from the Asian part of Russia had moved into the European part, and is currently found up to 51°E. Moreover, the almost uniform genetics of the continental D. sibiricus populations was shown, which suggests its rapid spread to the west of Eurasia (Kononov et al. 2016). Additionally, in recent decades, due to the observed climate change, the pest range has been expanding to the north (Kharuk et al. 2016). Currently, the Siberian moth is listed as a quarantine pest in Annex IAI of Directive 2000/29/EC.

The Siberian moth is characterized by periods of rapid reproduction, leading to a catastrophic increase in numbers (outbreaks) in local areas or on a panzonal scale (taking place in various territories simultaneously) and damage to coniferous forests. Outbreaks are poorly predicted, and opinions differ about the most important triggering and limiting factors for an outbreak. A number of researchers link the dynamics of the pest population with the dynamics of the abundance of entomophages that parasitize on eggs, caterpillars, and chrysalides (Kolomiets 1958, 1961, 1962; Chikidov 2009; Gninenko and Baranchikov 2021). Among approximately 40 species of insect parasitoids that attack Siberian moth (Baranchikov and Montgomery 2014), a special place is given to the egg parasitoid wasp Telenomus tetratomus (Thomson, 1861).

Telenomus tetratomus (=T. gracilis Mayr., T. bombus Mayr. and T. verticillatus Kieffer) (Kozlov 1967; Kozlov and Kononova 1983) is widespread in Europe, Russia, Mongolia, China, and Japan. It is considered one of the most effective regulators of pest abundance. The percentage of parasitism is more than 50% at any host abundance and by the end of outbreaks it can reach 100% (Kazansky 1928; Boldaruev 1952; Kolomiets 1962; Kondakov 2002; Baranchikov and Montgomery 2014; Gninenko and Baranchikov 2021). Since the end of the 19^th century, T. tetratomus has been proposed to control the Siberian moth by breeding and releasing it into the nascent centers of the pest’s mass reproduction. There are examples of almost complete elimination of D. sibiricus at different phases of foci formation after releasing T. tetratomus in them (Vasiliev 1905; Boldaruev 1952; Baranchikov and Montgomery 2014; Gninenko and Baranchikov 2021).

There is a widespread opinion that outbreaks of the Siberian moth are initiated by a decrease or disappearance of the regulatory impact of T. tetratomus as a result of its mass death during cold winters with little snow, since the parasitoid is less cold-resistant than its host (Kolomiets 1958, 1961, 1962; Chikidov 2009; Gninenko and Baranchikov 2021). However, studies on the cold hardiness of the wintering stages of these species, Siberian moth caterpillars and adult T. tetratomus, examined different characteristics. For the moth caterpillars, the supercooling point (SCP) was determined, and for T. tetratomus mortality was evaluated during short-term exposure to some negative temperatures (Kolomiets 1961). At the same time, while SCP of the Siberian moth (-14.9±1.5 °C) was studied in the laboratory by the instrumental method (cooling with thermocouples), the temperature limits tolerated by T. tetratomus and its mortality rate were determined in the course of an insufficiently controlled half-nature experiment. It is described as follows: “Several thousand parasitic wasps were placed in a Dewar vessel and stored in natural cooling conditions (between window frames) to determine their frost-resistance. The environmental air temperature was monitored with a minimum thermometer. After exposure to varying degrees of cooling, the parasitic wasps were brought into a warm room for vitalization” (Kolomiets 1961, p. 119). As can be seen from the above quotation, temperature conditions of the experiment were poorly controlled, and assessment of the wasp survival was approximate, which could significantly distort the true picture of the dependence of mortality on temperature.

Currently, there are two different ideas about lower lethal temperatures of T. tetratomus: according to Kolomiyets (1961), the mortality of females begins at -7 ... -9 °C, and already at -9 to -12 °C, 98% of individuals die, while 100% die at -14.7 °C. According to other authors, temperatures below -4 °C are lethal for this species (Baranchikov and Montgomery 2014). Comparison of the above characteristics of cold hardiness of the host and the parasitoid underlies one of the key ideas about population dynamics of the Siberian moth: before the onset of an outbreak, in the wintering sites of both species, there are temperature conditions under which caterpillars survive, while parasitic wasps die due to freezing. Despite the emergence of more accurate laboratory instruments in the 60 years since the experiment of Kolomiets (1961), the study of cold hardiness of T. tetratomus has not been refined. Due to the exceptional economic importance of the Siberian moth, its high potential for range expansion and the important role of T. tetratomus in regulation of the pest population, biological characteristics of the parasitoid must be carefully studied. Therefore, data on its cold hardiness need to be verified.

We determined the supercooling point of T. tetratomus, which had not been studied previously. SCP characterizes the ability of organisms to tolerate sub-zero temperatures without the freezing of body fluids. We could not fully assess the second characteristic, the lethal temperature for the survival of the species during long-term exposure, due to a technical failure (at temperatures below -6 °C). Also, the outbreak stopped in areas accessible for the parasitoid collection, which did not allow us to continue the work. However, comparison of the SCP values ​obtained by us and the known levels of mortality at several temperatures (Kolomiets 1961) do not support the idea of insufficient cold hardiness of T. tetratomus. Based on the leading role of this species of parasitic wasps in regulating the abundance of the dangerous pest and the possibility of introducing T. tetratomus into foci that appear in new territories with climatic conditions other than those in the native range, we considered it necessary to publish the results of our studies to draw the attention of colleagues to the need for a comprehensive study of its biological parameters, including cold hardiness.

Coniferous forests in the Tomsk region periodically suffer from outbreaks of the Siberian moth, the last of which was observed in 2016–2018. This outbreak was part of a panzonal outbreak that engulfed many regions of Asian Russia. In the year of our research, the outbreak in the Tomsk region was in the eruptive phase. However, in 2019, the number of Siberian moths decreased sharply and the vast majority of the local outbreaks disappeared. According to forest pathologists, this was facilitated by a high level of parasitoid infection of eggs, caterpillars and chrysalides in 2018 and weather conditions in 2019. In most of the region’s territories, as in our studies, more than 90% of Siberian moth eggs were infested with parasitoids, of which the most common was T. tetratomus (Denisova et al. 2020). These observations once again confirm the significant role of parasitoids in regulating the abundance of the Siberian moth.

We have estimated the supercooling point of T. tetratomus for the first time. The significant survival rate of T. tetratomus, which were at negative temperatures for about 2 months (down to -6 °C), and 100% death after freezing on thermocouples (i.e. at temperatures below SCP) indicate that they are not freeze-resistant, and therefore are only able to overwinter in a supercooled state, like many other hymenopteran parasitoids (Carrillo et al. 2005; Hanson et al. 2013; Santacruz et al. 2017). The real ecological value of SCP for freeze intolerant species is ambiguous. Though SCP is often criticized as a poor indicator of cold hardiness, it is used in many studies because it provides crucial information on the lower lethal temperature of freeze intolerant species of non-tropical invertebrates and constitutes a convenient comparative index (Bale 1987; Renault et al. 2002). Together with the lower lethal temperatures, it gives an idea of cold hardiness of a species that can be obtained from laboratory studies.

Our average T. tetratomus SCP values (-21.2±0.2 °C) were found to be 6.3 °C lower than the average moth caterpillar SCP values (-14.9±1.5 °C) (Kolomiets 1961). Such a large difference in the average SCP of these species living together and hibernating in a supercooled state casts doubt on the established opinion about the greater cold hardiness of the Siberian moth compared to the parasitoid.

The statistical distribution of T. tetratomus SCP (Fig. 2) and SCP cumulative curve (Fig. 3) have shapes typical of many small invertebrate species studied, including Hymenoptera (Block 1982; Berman et al. 2010; Berman and Leirikh 2019). However, the construction of the T. tetratomus cumulative mortality curve according to Kolomiets (1961) and its comparison with the cumulative SCP curve that we obtained raise a number of questions (Fig. 3).

Figure 3. 

Cumulative values of supercooling points and mortality at negative temperatures of Telenomus tetratomus. The black line is the mortality at different temperatures (according to: Kolomiets 1961), open circles indicate the SCP obtained in our experiments, the gray dashed line indicates our predicted mortality.

First, none of the more than 20 species of invertebrates that we have previously studied wintering in a supercooled state are characterized by such a narrow (only 3 °C) diapason of lethal temperatures. Such examples from the literature are also unknown to us. In the experiments of Kolomiets (1961), T. tetratomus females only began to die at -9 °C, and when it reached -12 °C, already 98% of individuals from a sample of several thousand animals were dead. Indeed, the death of the least prepared individuals for wintering in different species usually occurs at slightly subzero temperatures (-3 ... -5 °C); as temperatures decrease, mortality increases, and the most cold-resistant individuals die at temperatures close to the minimum SCP (Berman et al. 2010; Santacruz et al. 2017; Berman and Leirikh 2019). Thus, death occurs in a large temperature interval, significantly greater than 3 °C (from negative near zero temperatures to those comparable to minimum SCP values). Usually, this interval reaches 10–25 °C (Fig. 4).

Figure 4. 

Cold hardiness characteristics of several ant species (plotted according to: Berman et al. 2010, Berman and Leirikh 2019). Black lines indciate SCP cumulative curves, gray dashed lines indicate cumulative mortality curves upon exposure to the indicated temperatures for 1 day A Formica sanquinea B Myrmica angulinodis C Camponotus herculeanus D Formica execta E Myrmica kamtschatica F Formica gagatoides.

Second, the temperature of 100% mortality of T. tetratomus (-14.7 °C) revealed by Kolomiyets (1961) was found to be higher than the results of our experiments, with the SCP of the least cold-resistant individual at -15.7 °C (Fig. 3). This situation is not typical for species living in temperate seasonally cold latitudes and is probably typical only for tropical species (Renault 2002).

Third, the curves of the cumulative SCP and cumulative mortality turned out to be almost parallel and separated from each other by 10–11 °C throughout the entire length (Fig. 3). An analysis of literature data and our results of studying the cold hardiness of various groups of invertebrates in temperate latitudes wintering in a supercooled state (ants, beetles, butterflies, mollusks, etc.) suggests that such a disposition between the mortality curve and the SCP curve is an atypical situation (Berman et al. 2010; Berman and Leirikh 2019). In the vast majority of species, these two curves converge strongly with decreasing temperature, as, for example, in ants (Fig. 4A–D). Examples of parallel arrangement of the two curves are less common. At the same time, the curves of mortality and SCP in such cases are separated from each other by no more than 2–3 °C (Fig. 4E, F).

Considering all of the above, we can conclude that the high (more than 90%) mortality of T. tetratomus in the temperature interval from -9 to -12 °C is most likely the result of an incorrect conduction of the experiment and the lack of proper control of the temperatures at which the insects were held. Using a graphical method, 50% mortality temperature for T. tetratomus can be estimated at about -16 °C (Fig. 3), which is at least 5 °C lower than indicated by Kolomiyets (1961) and more than 10 °C lower than indicated by Baranchikov and Montgomery (2014).

For a number of invertebrates, including Hymenoptera, geographical variation in cold hardiness due to climatic differences has been shown: the average SCP of individuals in southern populations (with higher temperature) is higher than in northern ones (Block 1982; Turnock and Fields 2005; Santacruz et al. 2017). However, an analysis of temperatures in the wintering places of T. tetratomus (in the litter of coniferous forests) showed that, despite the more southerly position of the Tuvan population (52°N), which was studied by Kolomiets (1961), compared to the one studied by us, the temperatures in the wintering places of the parasitoid in Tuva are lower. In a coniferous forest, in the litter and under the moss cover at a depth of almost 20 cm, Kolomiets (1961) estimated the minimum temperatures as -18 °C due to the thin snow layer (20–22 cm) and low air temperatures (down to -48 °C). In the habitats that we studied, even at half the depth in the litter (10 cm), the minimum temperatures were higher (from -6.2 °C to -12.8 °C). The winter in which we measured the temperatures was slightly colder than usual and the minimum temperature reached -41 °C (against an average of -39.5 °C for the last 10 years) and with a slightly lower snow depth (69 cm against 73 cm on average for the last 10 years). So, it can be assumed that the forest litter was somewhat colder than usual. But even in relatively cold winters, the temperatures in the litter turned out to be higher than in the studied Tuva habitats. Thus, the comparison of winter temperature conditions in the wintering sites of T. tetratomus does not confirm the climatic conditionality of the obtained differences in cold hardiness of this species.

Our study of cold hardiness of T. tetratomus and the analysis of temperatures in the places of its overwintering indicate that the causes of Siberian moth outbreaks need further study. Both the host and its parasitoid overwinter in a supercooled state, and freezing is lethal to both. The average T. tetratomus SCP values ​​(-21.2±0.2 °C) turned out to be 6.3 °C lower than the average Siberian moth caterpillar SCP values (-14.9±1.5 °C) obtained in the experiments by Kolomiets (1961). Such a large difference in average SCP casts doubt on two well-established positions: firstly, about the greater cold hardiness of the Siberian moth compared to its parasitoid; secondly, that one of the main reasons for the beginning of an increase in number of the Siberian moth is the death of T. tetratomus population during cold winters with little snow, while the host safely overwinters (Kolomiets 1961, 1962; Chikidov 2009).

The analysis of SCP distribution and T. tetratomus mortality allows concluding that 50% mortality temperature can be estimated at about 5 °C lower than indicated by Kolomiets (1961) and more than 10 °C lower than indicated by Baranchikov and Montgomery (2014), at about16 °C. The presented results undoubtedly require determination of T. tetratomus mortality at several temperatures with simultaneous SCP measurements. We hope that the present research will stimulate colleagues to conduct a full-scale study of cold hardiness of T. tetratomus and other parasitoids, which will provide an adequate understanding of the possible ways of regulating the Siberian moth abundance not only within the existing range, but also with its possible expansion into Europe, and the prospects for introduction of parasitoids into cold regions.

The authors thank A.V. Timokhov for determining the species of Telenomus tetratomus, without which this work would not have been possible; E.N. Meshcheryakova – for help in setting up the measuring equipment.