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Overwintering mortality of the oak lace bug (Corythucha arcuata) in Hungary – a field survey

Overwintering mortality of the oak lace bug (Corythucha arcuata) in Hungary – a field survey The North American oak lace bug (Corythucha arcuata) was first discovered in Europe (Norhern Italy) in 2000. It started a rapid area expansion in the last decade and has been reported in 20 countries so far. Almost all European oaks are suitable hosts. On top of the host availability, abiotic factors like weather/climate may also have a decisive impact on its further spread and future outbreaks. We conducted a simple field survey within three years, at five locations to estimate the overwintering mortality of the species. Our results suggest that not even a relatively harsh winter (as 2016/2017) caused severe mortality in the overwintering populations. The average mortality of the nine year/location combinations was 30.6% (range 9.1–58.5%). Based on this, the low winter temperature is unlikely to restrict its further spread, therefore continuing area expansion can be predicted. Key words: invasive insects; area expansion; climate change; abiotic limitation; overwintering success Editor: Juraj Galko to make predictions on its further spread and expected 1. Introduction importance. Alien species are appearing at an accelerated rate world- Insects can be classified as either freeze-tolerant wide, including European countries (Roques 2010; Csóka or freeze-intolerant (or freeze-avoidant). The extracel- et al. 2010; 2012; Tuba et al. 2012; Smith et al. 2018). lular freezing is not lethal for the freeze-tolerant, they While some of them do not have any evident impact in regularly freeze between −5 to −10 °C, or at even lower the newly colonized areas, others may become invasive, temperature. After this they can be cooled to far lower rapidly expanding their area and imposing severe pres- temperatures (some species even as low as −50 °C). With sure on the invaded area’s ecosystems both from an eco- temperature increase they thaw and recover showing nor- nomic and an ecological point of view. The chance of a mal functions and development (Bale 1993). The freeze non-native species becoming invasive strongly depends intolerant (freeze-avoidant) insect may avoid freezing on the suitability of the environmental conditions includ- by lowering their super cooling point (SCP). SCP is the ing availability of host plants (Csóka et al. 2019; Paulin lower lethal temperature for the freeze-avoidant, since et al. 2020), effects of native natural enemies (Csóka et the ice formation is intracellular (Sinclair et al. 2015). al. 2009; Panzavolta et al. 2018; Kos et al. 2020). The On top of the extreme low temperature many other fac- weather and climate may also be decisive factors from tors may have significant effect on the insects’ survival the point of the establishment and the future of the (Sinclair et al. 2003). established populations. Different weather parameters The North American oak lace bug (Corythucha may have different impacts on the different life stages arcuata (Say 1832) – Heteroptera: Tingidae) is a recent of insects (Neuvonen & Virtanen 2015). Among many invader in Europe, first discovered in Italy in 2000 (Ber- others, overwintering success is an extremely important nardinelli et al. 2000). In the last decade, it showed an issue (Leather et al. 1993; Marshall et al. 2020; Vétek et al. 2020). Cold winter temperatures have both lethal and explosive area expansion and has been reported from 20 European countries (Paulin et al. 2020). As almost sub-lethal impacts on overwintering insects (Turnock & all native deciduous oaks are suitable hosts for the oak Fields 2005; Scaccini et al. 2020). Any information on the overwintering success of a new non-native insect is vital lace bug (OLB), at least 30 million hectares of oak for- *Corresponding author. György Csóka, e-mail: csokagy@erti.hu, phone: 0036 303 050 747 M. Paulin / Cent. Eur. For. J. 67 (2021) 108–112 ests provide acceptable hosts for it in Europe (Csóka et and locations mainly due to different spring weather al. 2019). Although there are major gaps in knowledge conditions. The main aspect was to sample before the concerning the further spread and damage of the OLB, it bugs leave the overwintering microhabitats, since the late seems potentially very dangerous both from an economic sampling would have overestimated the mortality. Loca- and an ecological point of view (Nikolic et al. 2019; Csóka tions, dates of samplings and sample sizes are provided et al. 2019; Paulin et al. 2020). in Table 1. After keeping the bugs at room temperature OLB adults stop feeding in late autumn (October/ (20–22 °C) for 24–36 hours, living and dead bugs were November) and migrate to their overwintering micro- counted. Temperature dates were obtained either from habitats. These are under raised bark, bark crevices, local meteorological stations or from the daily reports of branch forks covered by leaf litter, etc. Overwintering the Hungarian Meteorological Service. Based on these adults are rarely found on the soil surface under the leaf data, the following temperature variables were calcu- litter, but the vast majority of the overwintering bugs lated/considered: use tree trunks, branches and dead logs on the ground. – Average temperature of the period (average of the No overwintering larvae have been found in Hungary daily average temperatures). so far. They finish overwintering and climb up on the – Average of the daily minimum temperature of the trees starting from early/mid-April. It is assumed that period. the mild winters and early spring might help the further – The lowest temperature measured in period. area expansion and outbreaks. However this is not yet – Lowest 10-day running average of the daily minimum supported by scientic fi results and no published informa - temperatures in the period. tion are known on temperature demands of OLB either. The “period” always means the time window from st In order to obtain information on its overwintering December 1 until the last day prior the sampling date. st th success, we conducted a simple field survey within three For example, December 1 2016 – March 15 2017 at years at five Hungarian locations already invaded by the Gyula. Measured and calculated temperature variables OLB. The finding of the first year’s survey was already are provided in Table 2. published (Csepelényi et al. 2017), but its results have Mortality rates were correlated with the meteorologi- also been incorporated in this study. cal variables listed above. 2. Methods 3. Results Adult oak lace bugs were collected from their overwinter- Mortality rates of the 9 year/location combinations (pre- ing microhabitats in the second half of March prior to sented in Table 3) ranging from 9.1% to 58.5% show their emergence (early/mid-April). In all three years, at considerable variation. The average of all combinations all locations samples were taken from at least ten trees, merged is 30.6%. normally providing different overwintering microhabi- None of the four meteorological variables gave any tats (raised bark, bark crevices, branch forks covered by significant correlation with the mortality rates at 95% leaf litter, etc.). Sampling dates differed between years significance level. Table 1. Sample sizes (number of adult C. arcuata) and sampling dates (in bracket) in three years at five locations. Békéscsaba Gyula Mátrafüred Szarvas Szolnok 46.6728°N 21.1431°E 46.6940°N 21.3350°E 47.8308°N 19.9658°E 46.8759°N 20.5314°E 47.2042°N 20.1814°E Winter/Location 85 m a.s.l. 86 m a.s.l. 355 m a.s.l. 87 m a.s.l. 86 m a.s.l. 3,187 201 683 2016/2017 — (03.20–24) (03.16) (03.30) 1,329 386 4,929 2018/2019 — — (03.20) (03.29) (03.21) 2,582 1,816 2,519 2019/2020 — — (03.19) (03.19) (03.20) Table 2. Temperature variables within three years at five locations. Temperature variables Winter/Location Békéscsaba Gyula Mátrafüred Szarvas Szolnok 2016/2017 0.7 0.1 — 0.9 — Average of daily average temperatures 2018/2019 — 2.4 2.0 — 2.8 2019/2020 — 3.1 2.4 — 4.3 2016/2017 −2.8 −3.3 −2.8 Average of the daily minimum temperatures 2018/2019 — −1.2 −1.3 — −0.9 2019/2020 — −0.8 −0.7 — 1.1 2016/2017 −19.0 −18.0 — −19.0 The lowest temperature measured 2018/2019 — −7.7 −9.3 — −13.0 2019/2020 — −9.5 −10.1 — −8.0 2016/2017 −8.1 −7.5 −7.5 Lowest 10 days running average of the daily minimum temperatures 2018/2019 — −3.1 −6.6 — −3.9 2019/2020 — −3.1 −2.5 — −1.2 109 M. Paulin et al. / Cent. Eur. For. J. 67 (2021) 108–112 Table 3. Percentage of dead C. arcuata in samples collected in three years at five locations. Winter/Location Békéscsaba Gyula Mátrafüred Szarvas Szolnok Average 2016/2017 21.4% 51.7% — 44.1% — 39.1% 2018/2019 — 58.5% 18.7% — 44.6% 40.6% 2019/2020 — 13.0% 9.1% — 14.4% 12.2% Average — 41.7% 13.9% — 29.5% 30.6% large contiguous territories. In this situation, the majority 4. Discussion of the population either starved or had to feed on other Bernardinelli (2006) compared the climatic conditions of secondary hosts (Rubus, Acer, etc.). But even so, the the OLB’s native range (Eastern USA and Canada) and mortality rates remained relatively low. This may mean Europe and concluded that most of Europe’s climate may that winter low winter temperature itself is unlikely to allow the further spread of the species. Zielinska & Lis restrict the further spread to the East, North and West. (2020) concluded that the climate in Southern Poland is Jun et al. (2010) studied the supercooling point (SCP) suitable for the OLB, and the presence/abundance of oak and the cold hardiness of the closely related Corythuca forests may also increase the chance of its establishment. ciliata in China, where this species is an invasive pest Our results seem to support their conclusions. of Platanus trees. The average SCP was −11.49 °C for The mortality rates did not show significant correla- males and −9.54 °C for females. They found C. ciliata tion with our four meteorological variables. The 9 data freeze-intolerant, but chill-tolerant, tolerating subzero points is likely not enough to reveal correlations if they temperatures by supercooling. It worth mentioning that are any. But it is already evident that the mortality rates supercooling points of a given species’ individuals may are rather low, even during a relatively harsh winter show considerable variation geographically, monthly (2016/2017). and inter annually as it was demonstrated by Vétek el al. It is clear that the overwintering mortality rates are (2020) for the invasive Aproceros leucopoda (Hymenop- influenced by many factors other than the extremely low tera: Argidae). No similar information is known yet for winter air temperature. The state of the overwintering the OLB, although our related cooperative experiments microhabitats (tree exposure, thickness of bark, etc.), are already in progress. number of thaw-freeze transitions, rate of temperature change, cumulative chill injury might be very different, resulting in different chances of survival (Sinclair et al. 5. Conclusions 2003). The availability and quality of the pre-overwintering Based on the results, the low winter temperatures them- food quality also have important roles, both in the suc- selves do not seem to restrict the further area expansion cess of overwintering and the post-overwintering per- of the oak lace bug towards North, West or East. How- formance, as demonstrated by Zvereva (2002) for the ever, many factors other than winter temperature can leaf beetle, Chrysomela lapponica and by Trudeau et al. influence the overwintering mortality of the oak lace (2010) for Malacosoma disstria. bug. Additional studies (both in field and laboratory) In warm periods during overwintering, insects may are needed to clarify the potential climatic limitation of use their energy sources and this can have negative the further spread. impacts on them on the longer term (Hahn & Denlinger 2011; Sinclair 2015). It can be particularly important for insects starting overwintering with low energy reserve. In Acknowledgment other words, insects starving before overwintering will This study is supported by the Ministry of Agriculture and the have a lower chance to survive and even if they survive, OTKA 128008 research project sponsored by the National they will have less resource to use for post-wintering Research, Development and Innovation Office. activities (dispersal, mating, etc.). The relative impor- tance of this aspect is likely becoming more important as warmer periods during winters are becoming more References frequent. Bale, J. S., 1993: Classes of Insects Cold hardiness. Func- In case of the OLB, the pre-overwintering starvation tional Ecology, 7:751–753. seems likely for location/year combinations we studied Bernardinelli, I., 2000: Distribution of the oak lace bug (except Mátrafüred 2018/2019). The abundance of the Corythucha arcuata (Say) in northern Italy (Heterop- OLB was always high enough for overexploitation of tera Tingidae). Redia, LXXXIII:157–162. food sources by late summer or early autumn, resulting in a uniform discoloration and desiccation of foliage on 110 M. Paulin / Cent. Eur. For. J. 67 (2021) 108–112 Bernardinelli, I., 2006: European host plants and poten- N i k o l i ć , N . , P i l i p o v i ć , A . , D r e k i ć , M . , K o j i ć , D . , tial distribution of Corythucha arcuata (Say) (Heter- Poljaković-Pajnik, L., Orlović, S. et al., 2019: Physi- optera: Tingidae). In: Csóka, Gy., Hirka, A., Koltay, ological responses of pedunculate oak (Quercus A. (eds): Biotic damage in forests. Proceedings of robur L.) to Corythucha arcuata (Say, 1832) attack. the IUFRO Symposium (WP 7.03.10 “Methodolgy Archives of Biological Sciences, 71:167–176. of forest pest and disease survey in Central Europe“) Panzavolta, T., Croci, F., Bracalini, M., Melika, G., held in Mátrafüred, Hungary, September 12–16, Benedettelli, S., Tellini Florenzano, G. et al., 2018: 2004. Budapest, Hungarian Forest Research Insti- Population Dynamics of Native Parasitoids Associ- tute, p. 10–17. ated with the Asian Chestnut Gall Wasp (Dryocosmus Csepelényi, M., Hirka, A., Mikó, Á., Szalai, Á., Csóka, kuriphilus) in Italy. Psyche: A Journal of Entomology, G., 2017: Overwintering success of the oak lace bug 2:1–13. (Corythucha arcuata) in 2016/2017 at South-Eastern Paulin, M., Hirka, A., Eötvös, C. B., Gáspár, C., Fürjes- Hungary. Növényvédelem, 53:285–288. Mikó, Á., Csóka, G., 2020. Known and predicted Csóka, G., Hirka, A. Lakatos, F., 2010: Már a spájzban impacts of the invasive oak lace bug (Corythucha vannak… Növényvédelem, 46:547–550. arcuata) in European oak ecosystems – a review. Csóka, G., Hirka, A., Szőcs, L., 2012: Rovarglobalizáció a Folia Oecologica, 47:130–138. magyar erdőkben. Erdészettudományi Közlemények, Roques, A., 2010: Taxonomy. time and geographic pat- 2:187–198. terns. In: Roques, A., Kenis, M., Lees, D., Lopez, C., Csóka, G., Hirka, A., Mutun, S., Glavendekic, M., Mikó, Vaamonde, W., Rabitsch, Y-V., Roy. D. B. (eds): Á., Szőcs, L. et al., 2019: Spread and potential host Alien terrestrial arthropods of Europe. BioRisk, range of the invasive oak lace bug [Corythucha arcu- 4:11–26. ata (Say. 1832) – Heteroptera: Tingidae] in Eurasia. Scaccini, D., Luka Vanishvili L., Tirello P., Walton, V.M., Agricultural and Forest Entomology, 22:61–74. Carlo Duso, C., 2020: Lethal and sub-lethal effects Csóka, G., Pénzes, Z., Hirka, A., Mikó, I., Matosevic, of low-temperature exposures on Halyomorpha D., Melika, G., 2009: Parasitoid assemblages of two halys (Hemiptera: Pentatomidae) adults before and invading black locust leaf miners. Phyllonorycter after overwintering. Scientific Reports, available on robiniella (Clemens. 1859) and Parectopa robiniella https://doi.org/10.1038/s41598-020-72120-5 (Clemens. 1859) in Hungary. Periodicum Biologo- Sinclair, B. J., 2015: Linking energetics and overwinter- rum, 111:405–411. ing in temperate insects. Journal of Thermal Biology, Hahn, D. A., Denlinger, D. L., 2011: Energetics of insect 54:5–11. diapause. Annual Review of Entomology, 56:103– Sinclair, B. J., Coello Alvarado, L. E., Ferguson, L. V., 121. 2015: An invitation to measure insect cold tolerance: Kos, K., Lacković, N., Melika, G. et al., 2020: Diversity methods, approaches, and workflow. Journal of and surge in abundance of native parasitoid commu- Thermal Biology, 53:180–197. nities prior to the onset of Torymus sinensis on the Sinclair, B. J., Vernon, P., Klok, J. C., Chown, S. L., 2003: Asian chestnut gall wasp (Dryocosmus kuriphilus) Insects at low temperatures: an ecological perspective. in Slovenia, Croatia and Hungary. Journal of For- Trends in Ecology and Evolution, 18:257–362. est Research, available on https://doi.org/10.1007/ Smith, R. M., Baker, R. H. A., Collins, D. W., Korycinska, s11676-020-01197-5 A., Malumphy, C. P., Ostojá-Starzewski, J. C. et al., Jun, R-T., Wang, F., Xiao, Y-Y., 2010: Supercooling 2018: Recent trends in non-native, invertebrate, plant Capacity and Cold Hardiness of the Adults of the pest establishments in Great Britain, accounting for Sycamore Lace Bug, Corythucha ciliata (Hemiptera: time lags in reporting. Agricultural and Forest Ento- Tingidae). Cryo Letters, 31:445–453 mology, 20:496–504. Leather, S., Walters, K., Bale, J., 1993: The Ecology of Trudeau, M., Mauffette, Y., Rochefort, S., Hans, E., Insect Overwintering. Cambridge University Press, Bauce, E., 2010: Impact of Host Tree on Forest Tent 255 p. Caterpillar Performance and Offspring Overwinter- Marshall, E. K., Gotthard, K., Williams, C. M., 2020: ing Mortality. Environmental Entomology, 39:49– Evolutionary impacts of winter climate change on 504. insects. Current Opinion in Insect Science 2020, Tuba, K., Horváth, B., Lakatos, F., 2012: Inváziós rova- 41:54–62. rok fás növényeken. Nyugat-magyarországi Egyetem Neuvonen, S., Virtanen, T., 2015: Abiotic factors, climate Kiadó, 120 p. variability of forest insect pests. In: Björkman, C., Turnock, W. J., Fields, P. G., 2005: Winter climates and Niemalä, P.: Climate change and insect pests. CABI coldhardiness in terrestrial insects. European Journal climate change series, 7:154–172. of Entomology, 102:561–576. 111 M. Paulin et al. / Cent. Eur. For. J. 67 (2021) 108–112 Vétek, G., Fekete, V., Ladányi, M., Cargnus, E., Zan- Zielińska, A., Lis, B., 2020: Ocena możliwości potenc- digiacomo, P., Oláh, R. et al., 2020: Cold tolerance jalnej ekspansji prześwietlika dębowego Corythucha strategy and cold hardiness of the invasive zigzag elm arcuata (Say, 1832), inwazyjnego gatunku z rodziny sawy fl Aproceros leucopoda (Hymenoptera: Argidae). Tingidae (Hemiptera: Heteroptera), na tereny Polski. Agricultural and Forest Entomology, 22:231–237. Heteroptera Poloniae – Acta Faunistica, 14:175–180. Zvereva, E. L., 2002: Effects of host plant quality on overwintering success of the leaf beetle Chrysomela lapponica (Coleoptera: Chrysomelidae). European Journal of Entomology, 99:189–195. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Forestry Journal de Gruyter

Overwintering mortality of the oak lace bug (Corythucha arcuata) in Hungary – a field survey

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Publisher
de Gruyter
Copyright
© 2021 Márton Paulin et al., published by Sciendo
ISSN
0323-1046
eISSN
2454-0358
DOI
10.2478/forj-2020-0024
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See Article on Publisher Site

Abstract

The North American oak lace bug (Corythucha arcuata) was first discovered in Europe (Norhern Italy) in 2000. It started a rapid area expansion in the last decade and has been reported in 20 countries so far. Almost all European oaks are suitable hosts. On top of the host availability, abiotic factors like weather/climate may also have a decisive impact on its further spread and future outbreaks. We conducted a simple field survey within three years, at five locations to estimate the overwintering mortality of the species. Our results suggest that not even a relatively harsh winter (as 2016/2017) caused severe mortality in the overwintering populations. The average mortality of the nine year/location combinations was 30.6% (range 9.1–58.5%). Based on this, the low winter temperature is unlikely to restrict its further spread, therefore continuing area expansion can be predicted. Key words: invasive insects; area expansion; climate change; abiotic limitation; overwintering success Editor: Juraj Galko to make predictions on its further spread and expected 1. Introduction importance. Alien species are appearing at an accelerated rate world- Insects can be classified as either freeze-tolerant wide, including European countries (Roques 2010; Csóka or freeze-intolerant (or freeze-avoidant). The extracel- et al. 2010; 2012; Tuba et al. 2012; Smith et al. 2018). lular freezing is not lethal for the freeze-tolerant, they While some of them do not have any evident impact in regularly freeze between −5 to −10 °C, or at even lower the newly colonized areas, others may become invasive, temperature. After this they can be cooled to far lower rapidly expanding their area and imposing severe pres- temperatures (some species even as low as −50 °C). With sure on the invaded area’s ecosystems both from an eco- temperature increase they thaw and recover showing nor- nomic and an ecological point of view. The chance of a mal functions and development (Bale 1993). The freeze non-native species becoming invasive strongly depends intolerant (freeze-avoidant) insect may avoid freezing on the suitability of the environmental conditions includ- by lowering their super cooling point (SCP). SCP is the ing availability of host plants (Csóka et al. 2019; Paulin lower lethal temperature for the freeze-avoidant, since et al. 2020), effects of native natural enemies (Csóka et the ice formation is intracellular (Sinclair et al. 2015). al. 2009; Panzavolta et al. 2018; Kos et al. 2020). The On top of the extreme low temperature many other fac- weather and climate may also be decisive factors from tors may have significant effect on the insects’ survival the point of the establishment and the future of the (Sinclair et al. 2003). established populations. Different weather parameters The North American oak lace bug (Corythucha may have different impacts on the different life stages arcuata (Say 1832) – Heteroptera: Tingidae) is a recent of insects (Neuvonen & Virtanen 2015). Among many invader in Europe, first discovered in Italy in 2000 (Ber- others, overwintering success is an extremely important nardinelli et al. 2000). In the last decade, it showed an issue (Leather et al. 1993; Marshall et al. 2020; Vétek et al. 2020). Cold winter temperatures have both lethal and explosive area expansion and has been reported from 20 European countries (Paulin et al. 2020). As almost sub-lethal impacts on overwintering insects (Turnock & all native deciduous oaks are suitable hosts for the oak Fields 2005; Scaccini et al. 2020). Any information on the overwintering success of a new non-native insect is vital lace bug (OLB), at least 30 million hectares of oak for- *Corresponding author. György Csóka, e-mail: csokagy@erti.hu, phone: 0036 303 050 747 M. Paulin / Cent. Eur. For. J. 67 (2021) 108–112 ests provide acceptable hosts for it in Europe (Csóka et and locations mainly due to different spring weather al. 2019). Although there are major gaps in knowledge conditions. The main aspect was to sample before the concerning the further spread and damage of the OLB, it bugs leave the overwintering microhabitats, since the late seems potentially very dangerous both from an economic sampling would have overestimated the mortality. Loca- and an ecological point of view (Nikolic et al. 2019; Csóka tions, dates of samplings and sample sizes are provided et al. 2019; Paulin et al. 2020). in Table 1. After keeping the bugs at room temperature OLB adults stop feeding in late autumn (October/ (20–22 °C) for 24–36 hours, living and dead bugs were November) and migrate to their overwintering micro- counted. Temperature dates were obtained either from habitats. These are under raised bark, bark crevices, local meteorological stations or from the daily reports of branch forks covered by leaf litter, etc. Overwintering the Hungarian Meteorological Service. Based on these adults are rarely found on the soil surface under the leaf data, the following temperature variables were calcu- litter, but the vast majority of the overwintering bugs lated/considered: use tree trunks, branches and dead logs on the ground. – Average temperature of the period (average of the No overwintering larvae have been found in Hungary daily average temperatures). so far. They finish overwintering and climb up on the – Average of the daily minimum temperature of the trees starting from early/mid-April. It is assumed that period. the mild winters and early spring might help the further – The lowest temperature measured in period. area expansion and outbreaks. However this is not yet – Lowest 10-day running average of the daily minimum supported by scientic fi results and no published informa - temperatures in the period. tion are known on temperature demands of OLB either. The “period” always means the time window from st In order to obtain information on its overwintering December 1 until the last day prior the sampling date. st th success, we conducted a simple field survey within three For example, December 1 2016 – March 15 2017 at years at five Hungarian locations already invaded by the Gyula. Measured and calculated temperature variables OLB. The finding of the first year’s survey was already are provided in Table 2. published (Csepelényi et al. 2017), but its results have Mortality rates were correlated with the meteorologi- also been incorporated in this study. cal variables listed above. 2. Methods 3. Results Adult oak lace bugs were collected from their overwinter- Mortality rates of the 9 year/location combinations (pre- ing microhabitats in the second half of March prior to sented in Table 3) ranging from 9.1% to 58.5% show their emergence (early/mid-April). In all three years, at considerable variation. The average of all combinations all locations samples were taken from at least ten trees, merged is 30.6%. normally providing different overwintering microhabi- None of the four meteorological variables gave any tats (raised bark, bark crevices, branch forks covered by significant correlation with the mortality rates at 95% leaf litter, etc.). Sampling dates differed between years significance level. Table 1. Sample sizes (number of adult C. arcuata) and sampling dates (in bracket) in three years at five locations. Békéscsaba Gyula Mátrafüred Szarvas Szolnok 46.6728°N 21.1431°E 46.6940°N 21.3350°E 47.8308°N 19.9658°E 46.8759°N 20.5314°E 47.2042°N 20.1814°E Winter/Location 85 m a.s.l. 86 m a.s.l. 355 m a.s.l. 87 m a.s.l. 86 m a.s.l. 3,187 201 683 2016/2017 — (03.20–24) (03.16) (03.30) 1,329 386 4,929 2018/2019 — — (03.20) (03.29) (03.21) 2,582 1,816 2,519 2019/2020 — — (03.19) (03.19) (03.20) Table 2. Temperature variables within three years at five locations. Temperature variables Winter/Location Békéscsaba Gyula Mátrafüred Szarvas Szolnok 2016/2017 0.7 0.1 — 0.9 — Average of daily average temperatures 2018/2019 — 2.4 2.0 — 2.8 2019/2020 — 3.1 2.4 — 4.3 2016/2017 −2.8 −3.3 −2.8 Average of the daily minimum temperatures 2018/2019 — −1.2 −1.3 — −0.9 2019/2020 — −0.8 −0.7 — 1.1 2016/2017 −19.0 −18.0 — −19.0 The lowest temperature measured 2018/2019 — −7.7 −9.3 — −13.0 2019/2020 — −9.5 −10.1 — −8.0 2016/2017 −8.1 −7.5 −7.5 Lowest 10 days running average of the daily minimum temperatures 2018/2019 — −3.1 −6.6 — −3.9 2019/2020 — −3.1 −2.5 — −1.2 109 M. Paulin et al. / Cent. Eur. For. J. 67 (2021) 108–112 Table 3. Percentage of dead C. arcuata in samples collected in three years at five locations. Winter/Location Békéscsaba Gyula Mátrafüred Szarvas Szolnok Average 2016/2017 21.4% 51.7% — 44.1% — 39.1% 2018/2019 — 58.5% 18.7% — 44.6% 40.6% 2019/2020 — 13.0% 9.1% — 14.4% 12.2% Average — 41.7% 13.9% — 29.5% 30.6% large contiguous territories. In this situation, the majority 4. Discussion of the population either starved or had to feed on other Bernardinelli (2006) compared the climatic conditions of secondary hosts (Rubus, Acer, etc.). But even so, the the OLB’s native range (Eastern USA and Canada) and mortality rates remained relatively low. This may mean Europe and concluded that most of Europe’s climate may that winter low winter temperature itself is unlikely to allow the further spread of the species. Zielinska & Lis restrict the further spread to the East, North and West. (2020) concluded that the climate in Southern Poland is Jun et al. (2010) studied the supercooling point (SCP) suitable for the OLB, and the presence/abundance of oak and the cold hardiness of the closely related Corythuca forests may also increase the chance of its establishment. ciliata in China, where this species is an invasive pest Our results seem to support their conclusions. of Platanus trees. The average SCP was −11.49 °C for The mortality rates did not show significant correla- males and −9.54 °C for females. They found C. ciliata tion with our four meteorological variables. The 9 data freeze-intolerant, but chill-tolerant, tolerating subzero points is likely not enough to reveal correlations if they temperatures by supercooling. It worth mentioning that are any. But it is already evident that the mortality rates supercooling points of a given species’ individuals may are rather low, even during a relatively harsh winter show considerable variation geographically, monthly (2016/2017). and inter annually as it was demonstrated by Vétek el al. It is clear that the overwintering mortality rates are (2020) for the invasive Aproceros leucopoda (Hymenop- influenced by many factors other than the extremely low tera: Argidae). No similar information is known yet for winter air temperature. The state of the overwintering the OLB, although our related cooperative experiments microhabitats (tree exposure, thickness of bark, etc.), are already in progress. number of thaw-freeze transitions, rate of temperature change, cumulative chill injury might be very different, resulting in different chances of survival (Sinclair et al. 5. Conclusions 2003). The availability and quality of the pre-overwintering Based on the results, the low winter temperatures them- food quality also have important roles, both in the suc- selves do not seem to restrict the further area expansion cess of overwintering and the post-overwintering per- of the oak lace bug towards North, West or East. How- formance, as demonstrated by Zvereva (2002) for the ever, many factors other than winter temperature can leaf beetle, Chrysomela lapponica and by Trudeau et al. influence the overwintering mortality of the oak lace (2010) for Malacosoma disstria. bug. Additional studies (both in field and laboratory) In warm periods during overwintering, insects may are needed to clarify the potential climatic limitation of use their energy sources and this can have negative the further spread. impacts on them on the longer term (Hahn & Denlinger 2011; Sinclair 2015). It can be particularly important for insects starting overwintering with low energy reserve. In Acknowledgment other words, insects starving before overwintering will This study is supported by the Ministry of Agriculture and the have a lower chance to survive and even if they survive, OTKA 128008 research project sponsored by the National they will have less resource to use for post-wintering Research, Development and Innovation Office. activities (dispersal, mating, etc.). The relative impor- tance of this aspect is likely becoming more important as warmer periods during winters are becoming more References frequent. Bale, J. S., 1993: Classes of Insects Cold hardiness. 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Journal

Forestry Journalde Gruyter

Published: Jun 1, 2021

Keywords: invasive insects; area expansion; climate change; abiotic limitation; overwintering success

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