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Short Communication
On cold hardiness of the egg parasitoid wasp Telenomus tetratomus (Thomson, 1861) (Hymenoptera, Scelionidae) – a population regulator of the Siberian moth
expand article infoNina A. Bulakhova, Zoya A. Zhigulskaya, Lyudmila P. Gashkova§, Daniil I. Berman
‡ Institute of Biological Problems of the North, Far Eastern Branch of the Russian Academy of Science, Magadan, Russia
§ Siberian Federal Scientific Center of Agro-Bio Technologies, Russian Academy of Sciences, Siberian Research Institute of Agriculture and Peat, Tomsk, Russia
Open Access

Abstract

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.

Keywords

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

Introduction

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 20th 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 19th 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.

Materials and methods

Sampling sites

Siberian moth eggs affected by T. tetratomus were collected at the end of August 2018 in one of the sites with high pest abundance (Bakcharsky district of the Tomsk region) on the northeastern spur of the Great Vasyugan mire in the basin of the Gavrilovka River (56.85°N, 82.69°E). In the studied mire, pine-shrub-sphagnum plant communities represent vegetation. The tree stratum is dominated by the stunted Pinus sylvestris, up to 4 m high (Fig. 1A), Pinus sibirica up to 5 m high is found singly. Projective cover of the grass-shrub stratum (height of 30–40 cm) is 70%; dominants are Vaccinium uliginosum (30%) and Chamaedaphne calyculata (20%), as well as Rhododendron tomentosum, Andromeda polifolia, Rubus chamaemorus. Among the herbs, Eriophorum vaginatum predominates (less than 10%), others are found singly. The basis of the moss-lichen cover is Sphagnum fuscum (70%) with an admixture of Sphagnum divinum, Sphagnum angustifolium, Sphagnum balticum, Polytrichum strictum, Pleurozium schreberi, and Dicranum polysetum. Lichens are represented by species of the genera Usnea and Cladonia.

Animal sampling

Collected shoots (20–30 cm) of Pinus sibirica and P. sylvestris (Fig. 1B) with Siberian moth egg clutches were packed in non-woven bags or in cardboard boxes, moistened and placed in polyethylene bags, which were stored in the laboratory at temperatures of 15–18 °C. By the time the eggs were collected, most of T. tetratomus had already hatched, which was noticeable both by the holes in the eggshells (Fig. 1B) and by the number of egg parasitoid wasps collected from the shoots in the laboratory. Since only fertilized females of T. tetratomus hibernate, in order to minimize the use in experiments of males that die shortly after hatching (Boldaruev 1952; Baranchikov and Montgomery 2014), animals were caught after a week in the laboratory. The dead individuals were not used in experiments. Mobile T. tetratomus from needles, bag walls, and Siberian moth eggs were collected with an exhauster and placed 10–20 individuals in 20 or 50 ml test tubes with moist filter paper and a bunch of needles inside. The proportion of eggs damaged by parasitoids was determined using identification keys (Kolomiets 1962). Taxonomic identification of T. tetratomus (Kozlov and Kononova 1983; Kononova 2014) was carried out by A.V. Timokhov (Moscow State University, Russia); specimens are deposeitd in Zoological Museum of Lomonosov Moscow State University (ZMMU) (No USNMENT009903625USNMENT009903629) and in the Biocenology Laboratory of the IBPN FEB RAS (Magadan).

Figure 1. 

A partially defoliated pines B egg-laying and C Siberian moth pupal cocoon at the collection site (photo by L. Gashkova).

Acclimation and determination of cold hardiness

The egg parasitoid wasps in test tubes were acclimated and cooled in test chambers WT 64/75 (Weiss Umwelttechnik GmbH, Reiskirchen-Lindenstruth, Germany), gradually (at a rate of 1 °C/day) lowering the temperature and keeping at a temperature of 5 °C for a month, 10 days at 1 °C, 20 days at 0 °C, 20 days at -5 °C, and 31–36 days at -6 °C. The temperatures were additionally monitored with preliminarily calibrated temperature loggers (iButton DS1922L, Scientific and Technical Laboratory “ElIn”, Moscow, Russia).

The supercooling point (SCP) of T. tetratomus was assessed approximately 5 months after the individuals were collected and kept in the laboratory at the above temperatures. SCP is the temperature at which ice begins to form within the body fluids. Crystallization is accompanied by a surge of heat output and a peak on the temperature diagram. Cooling specimens to SCP and then evaluating survival after the rewarming gives an idea of ​​the state, either frozen or supercooled, in which the specimens are able to tolerate freezing temperatures. SCP was determined in living specimens stored at -6 °C (n = 73), which, when manipulated, weakly moved their limbs. The standard methodology for SCP determination, which has been tested on many invertebrate species, was used (Berman et al. 2010; Berman and Leirikh 2019). The temperature was measured with manganin–constantan thermocouples (wire diameter 0.12 mm). The thermocouple signal was converted using an analog–digital board (ADC LA-TK5) via a DC voltage amplifier and recorded on a computer. The egg parasitoid wasps were fixed on the working junctions of thermocouples with a thin layer of vaseline. The thermocouples with attached insects were cooled in a cooling chamber at a rate of 1 °C/minute. After passing the peak of the freezing onset, the temperatures were lowered by 0.2–7 °C to guarantee freezing of the samples. After that, the wasps were warmed and kept for several hours at 4 °C, then at room temperature, and then the survival was checked.

Winter temperatures in habitats

The temperatures in forest litter in the places where Siberian moth eggs were collected were not determined due to their remoteness. However, they were estimated in typical habitats of the Siberian moth and T. tetratomus at a site located approximately 90 km from the egg collection area, in the vicinity of the Podgornoye village (57.79°N, 82.69°E), according to our archival data. In 2008–2009, in this area, a large-scale study of temperatures in soils and forest litter was carried out in various biotopes, including several types of coniferous forests: at a pine-shrub-sphagnum bog (similar to the one at which Siberian moth eggs with egg parasitoid wasps were collected); in a mature dark coniferous (cedar and fir) forest with high crown density on a river side of the Iksa River; in plantations of pine and in a narrow snow-protective spruce-pine belt. The temperature loggers (DS1922L) recorded temperature 6 times a day in typical T. tetratomus wintering places, forest litter or moss cover at three depths: at the surface (0–2 cm) and at 10 or 20 cm (depending on the cover thickness). Data on air temperatures and snow depth were obtained at the meteorological station in the Podgornoe village, located no more than 7 km from the places where the temperature loggers were positioned and at the meteorological station in the Bakchar village, located about 40 km from the place where the animals were collected for experiments.

Results

Observations in nature

At the end of August, pupal cocoons and eggs of the Siberian moth were found on trees in the studied bog (Fig. 1B, C). Among the several hundred collected eggs examined in the laboratory, no more than 3% had signs of caterpillars emerging (brownish color of the shells, a large irregularly shaped hole with uneven edges). The vast majority of eggs had traces of parasitoids in them, among which T. tetratomus predominated (gray shells, one hole of small diameter with smooth edges, see Fig. 1B). In the summer of 2019, during an inspection of this territoty, as well as forests damaged by the Siberian moth in the Chainsky and Tomsk regions, caterpillars, butterflies or eggs of the moths were not found, i.e., the year of the Siberian moth egg collection (2018) was the last year of the three-year pest outbreak.

Cold hardiness of Telenomus tetratomus

The majority of T. tetratomus (85% of the sample) cooled in the laboratory to -6 °C survived: when they were transferred to positive temperatures, they began to move after a few minutes. SCP values ranged from -15.7 to -26.2 °C, with an average of -21.2±0.2 °C (Fig. 2). None of the animals cooled by another 0.2–7 °C after reaching SCP, including those that spent only a few seconds in the frozen state, survived after a long period at positive temperatures.

Figure 2. 

Histogram of Telenomus tetratomus SCP distribution.

Minimum temperatures in winter habitats of Telenomus tetratomus

In the winter preceding the time of collecting Siberian moth eggs (2017–2018), the minimum air temperature was -40.9 °C, and the maximum snow depth was 73 cm (according to data from the meteorological station in the Bakchar village). In the area of ​​soil temperature measurements (surrounding the Podgornoe village), the minimum air temperature was the same (-41 °C), with a slightly lower snow cover depth (69 cm). Under these conditions, the minimum temperature in the ground cover in different types of coniferous forests varied greatly. In the upper 2 cm of the litter, it was the lowest (-25 °C) in the pine-shrub-sphagnum bog with sparse low-growing pines and cedars and in the mature dark coniferous forest with high crown density on the river side (-15 °C). However, in the plantations of pine and in the narrow snow-protective spruce-pine belt, the temperatures were much higher (-7 and -9.5 °C, respectively). At a depth of 10 cm in the litter in both areas of pine plantations, the minimum temperatures were 1–2.5 °C higher than at the surface (-6.2 and -7 °C), respectively. In the litter in the dark coniferous forest, even at a depth of 10 cm, temperatures dropped to -12.8 °C. It was also cold on the raised bog in the depths of the thick and loose moss-grass-shrub cover – temperatures of -7 °C were recorded no closer than 20 cm from the surface.

Discussion

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.

Conclusions

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.

Acknowledgements

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.

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