Abstract
Invasive pentatomid Halyomorpha halys recently arrived to the Black Sea region and began damaging agricultural and ornamental plants. We studied the effects of day length and temperature on the pre-adult development and diapause induction in H. halys from Sochi (Russia) under laboratory conditions (20, 24, and 28 °C and several photoperiods). The pre-adult development of H. halys was noticeably faster under L:D 12:12 compared with L:D 15:9. The sum of effective temperatures required for the pre-adult development was ca. 530 and 590 degree days under these two conditions, respectively, whereas the lower developmental thresholds were similar (ca. 13.3 °C). Adults of H. halys demonstrated a typical long-day-type photoperiodic response of facultative winter adult diapause induction: Short days (photophases of 12–15 h) induced diapause in all adults, whereas long days (with photophases longer than 15 h) promoted reproduction. The photoperiodic responses of diapause induction of females and males were very similar. At 24 °C, the threshold of the response was between 15 and 16 h. At 20 °C, even under the very long-day conditions (L:D 18:6) about 50% of adults entered diapause. Field records suggest that H. halys likely produces two generations per year in Sochi. Short days might accelerate nymphal growth of the second generation in August and then induce winter diapause in adults. Phenological studies and monitoring are needed for a better understanding of the adaptation process of this invasive pest to new conditions.
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References
Bertelsmeier C, Keller L (2018) Bridgehead effects and role of adaptive evolution in invasive populations. Trends Ecol Evol 33(7):527–534. https://doi.org/10.1016/j.tree.2018.04.014
Bradshaw WE, Holzapfel CM (2001) Genetic shift in photoperiodic response correlated with global warming. Proc Natl Acad Sci USA 98:14509–14511. https://doi.org/10.1073/pnas.241391498
Bradshaw WE, Holzapfel CM (2008) Genetic response to rapid climate change: it’s seasonal timing that matters. Mol Ecol 17(1):157–166. https://doi.org/10.1111/j.1365-294X.2007.03509.x
Cira TM, Koch RL, Burkness EC, Hutchison WD, Venette RC (2018) Effects of diapause on Halyomorpha halys (Hemiptera: Pentatomidae) cold tolerance. Environ Entomol. https://doi.org/10.1093/ee/nvy064
ClimaTemps.com (2018) http://www.soci.climatemps.com/ Accessed 09 May 2018
Danilevsky AS (1965) Photoperiodism and seasonal development of insects. Oliver & Boyd, Edinburgh
Danks HV (1987) Insect dormancy: an ecological perspective. Biological survey of Canada, Ottawa (Monograph ser. N 1)
Esquivel JF, Musolin DL, Jones WA, Rabitsch W, Greene JK, Toews MD, Schwertner CF, Grazia J, McPherson RM (2018) Nezara viridula (L.). In: McPherson JE (ed) Invasive stink bugs and related species (Pentatomoidea): biology, higher systematics, semiochemistry, and management. CRC Press, Boca Raton, pp 351–423
Fujiie A (1985) Seasonal life cycle of Halyomorpha mista. Bull Chiba Agric Exp Stn 26:87–93
Gapon DA (2016) First records of the brown marmorated stink bug Halyomorpha halys (Stål, 1855) (Heteroptera, Pentatomidae) in Russia, Abkhazia, and Georgia. Entomol Rev 96:1086–1088. https://doi.org/10.1134/S001387381608011X
Gariepy TD, Fraser H, Scott-Dupree CD (2014) Brown marmorated stink bug (Hemiptera: Pentatomidae) in Canada: recent establishment, occurrence, and pest status in southern Ontario. Can Entomol 146:579–582. https://doi.org/10.4039/tce.2014.4
Gomi T (1997) Geographic variation in critical photoperiod for diapause induction and its temperature dependence in Hyphantria cunea Drury (Lepidoptera: Arctiidae). Oecologia 111:160–165. https://doi.org/10.1007/s004420050220
Gomi T, Nagasaka M, Fukuda T, Nagihara H (2007) Shifting of the life cycle and life-history traits the fall webworm in relation to climate change. Entomol Exp Appl 125:179–184. https://doi.org/10.1111/j.1570-7458.2007.00616.x
Goryshin NI, Tyshchenko GF (1972) Experimental analysis of photoperiodic induction of diapause in insects. Trudy Biologicheskogo instituta Leningraskogo gosudarstvennogo universiteta [Proc of the Biol Inst Leningrad State Univ] 21:68–89
Hamilton GC, Ahn JJ, Bu W, Leskey TC, Nielsen AL, Park Y-L, Rabitsch W, Hoelmer KA (2018) Halyomorpha halys (Stål). In: McPherson JE (ed) Invasive stink bugs and related species (Pentatomoidea): biology, higher systematics, semiochemistry, and management. CRC Press, Boca Raton, pp 243–292
Haye T, Abdallah S, Gariepy T, Wyniger D (2014) Phenology, life table analysis, and temperature requirements of the invasive brown marmorated stink bug, Halyomorpha halys, in Europe. J Pest Sci 87:407–418. https://doi.org/10.1007/s10340-014-0560-z
Haye T, Gariepy T, Hoelmer K, Rossi J-P, Streito J-C, Tassus X, Desneux N (2015) Range expansion of the invasive brown marmorated stinkbug, Halyomorpha halys: an increasing threat to field, fruit and vegetable crops worldwide. J Pest Sci 88(4):665–673. https://doi.org/10.1007/s10340-015-0670-2
Hoffman WE (1931) A pentatomid pest of growing beans in south China. Peking Nat Hist Bull 5:25–27
Hulme PE (2009) Trade, transport and trouble: managing invasive species pathways in an era of globalization. J Appl Ecol 46(1):10–18. https://doi.org/10.1111/j.1365-2664.2008.01600.x
Kiritani K (2007) The impact of global warming and land use change on the pest status of rice and fruit bugs (Heteroptera) in Japan. Global Change Biol 13:1586–1595. https://doi.org/10.1111/j.1365-2486.2007.01397.x
Lee D-H (2015) Current status of research progress on the biology and management of Halyomorpha halys (Hemiptera: Pentatomidae) as an invasive species. Appl Entomol Zool 50(3):277–290. https://doi.org/10.1007/s13355-015-0350-y
Lee D-H, Short BD, Joseph SV, Bergh JC, Leskey TC (2013) Review of the biology, ecology and management of Halyomorpha halys (Hemiptera: Pentatomidae) in China, Japan and the Republic of Korea. Environ Entomol 42:627–641. https://doi.org/10.1603/EN13006
Leskey TC, Nielsen AL (2018) Impact of the invasive brown marmorated stink bug in North America and Europe: History, biology, ecology, and management. Annu Rev Entomol 63:599–618. https://doi.org/10.1146/annurev-ento-020117-043226
Leskey TC, Hamilton GC, Nielsen AL et al (2012) Pest status of the brown marmorated stink bug, Halyomorpha halys (Stål), in the USA. Outlooks on Pest Management 23(5):218–226
McPherson JE (ed) (2018) Invasive stink bugs and related species (Pentatomoidea): biology, higher systematics, semiochemistry, and management. CRC Press, Boca Raton, pp. 497–564
Milonas PG, Partsinevelos GK (2014) First report of brown marmorated stink bug Halyomorpha halys Stål (Hemiptera: Pentatomidae) in Greece. EPPO Bull 44(2):183–186. https://doi.org/10.1111/epp.12129
Mityushev IM (2016) The first record of Brown marmorated stink bug in Russia. Zashita i Karantin Rasteniy [Prot Quar Plants] 3:48
Musolin DL, Numata H (2003a) Photoperiodic and temperature control of diapause induction and colour change in the southern green stink bug Nezara viridula. Physiol Entomol 28(2):65–74. https://doi.org/10.1046/j.1365-3032.2003.00307.x
Musolin DL, Numata H (2003b) Timing of diapause induction and its life-history consequences in Nezara viridula: is it costly to expand the distribution range? Ecol Entomol 28(6):694–703. https://doi.org/10.1111/j.1365-2311.2003.00559.x
Musolin DL, Saulich AKh (1997) Photoperiodic control of nymphal growth in true bugs (Heteroptera). Entomol Rev 77(6):768–780
Musolin DL, Saulich AH (1999) Diversity of seasonal adaptations in terrestrial true bugs (Heteroptera) from the temperate zone. Entomol Sci 2(4):623–639
Musolin DL, Saulich AKh (2018) Diapause in Pentatomoidea. In: McPherson JE (ed) Invasive stink bugs and related species (Pentatomoidea): biology, higher systematics, semiochemistry, and management. CRC Press, Boca Raton, pp 497–564
Musolin DL, Konjević A, Karpun NN, Procenko VYe, Ayba LYa, Saulich AKh (2018) Invasive brown marmorated stink bug Halyomorpha halys (Stål) (Heteroptera: Pentatomidae) in Russia, Abkhazia, and Serbia: history of invasion, range expansion, early stages of establishment, and first records of damage to local crops. Arthropod-Plant Interact 12(4):517–529. https://doi.org/10.1007/s11829-017-9583-8
Nakamura K, Numata H (1997) Seasonal life cycle of Aelia fieberi (Heteroptera: Pentatomidae). Ann Entomol Soc Am 90:625–630. https://doi.org/10.1093/aesa/90.5.625
Nielsen AL, Hamilton GC (2009) Life history of the invasive species Halyomorpha halys (Hemiptera: Pentatomidae) in Northeastern United States. Ann Entomol Soc Am 102(4):608–616. https://doi.org/10.1603/008.102.0405
Nielsen AL, Hamilton GC, Matadha D (2008) Developmental rate estimation and life table analysis for Halyomorpha halys (Hemiptera: Pentatomidae). Environ Entomol 37:348–355. https://doi.org/10.1093/ee/37.2.348
Nielsen AL, Chen S, Fleischer SJ (2016) Coupling developmental physiology, photoperiod, and temperature to model phenology and dynamics of an invasive heteropteran, Halyomorpha halys. Front Physiol 7:165. https://doi.org/10.3389/fphys.2016.00165
Nielsen AL, Fleischer S, Hamilton GC et al (2017) Phenology of brown marmorated stink bug described using female reproductive development. Ecol Evol 7:6680–6690. https://doi.org/10.1002/ece3.3125
Niva CC (2003) Molecular and neuroendocrine mechanisms of photoperiodism in Halyomorpha halys (Heteroptera: Pentatomidae). Ph.D. Dissertation, Kobe University
Niva CC, Takeda M (2003) Effects of photoperiod, temperature and melatonin on nymphal development, polyphenism and reproduction in Halyomorpha halys (Heteroptera: Pentatomidae). Zool Sci 20:963–970. https://doi.org/10.2108/zsj.20.963
Pyšek P, Bacher S, Chytrý M et al (2010) Contrasting patterns in the invasions of European terrestrial and freshwater habitats by alien plants, insects and vertebrates. Glob Ecol Biogeogr 19(3):317–331. https://doi.org/10.1111/j.1466-8238.2009.00514.x
Rice KB, Bergh JC, Bergmann EJ et al (2014) Biology, ecology, and management of brown marmorated stink bug (Halyomorpha halys). J Integr Pest Manag 5:1–13. https://doi.org/10.1603/IPM14002
Ruberson JR, Kring TJ, Elkassabany N (1998) Overwintering and the diapause syndrome of predatory Heteroptera. In: Coll M, Ruberson JR (eds) Predatory Heteroptera: their ecology and use in biological control. Thomas Say Publications in Entomology, Entomological Society of America, Lanham, pp 49–69
Saulich AKh, Musolin DL (2009) Seasonal development and ecology of anthocorids (Heteroptera, Anthocoridae). Entomol Rev 89(5):501–528. https://doi.org/10.1134/S0013873809050017
Saulich AKh, Musolin DL (2012) Diapause in the seasonal cycle of stink bugs (Heteroptera, Pentatomidae) from the temperate zone. Entomol Rev 92(1):1–26. https://doi.org/10.1134/S0013873812010010
Saulich AKh, Musolin DL (2018) Seasonal cycles of Pentatomoidea. In: McPherson JE (ed) Invasive stink bugs and related species (Pentatomoidea): biology, higher systematics, semiochemistry, and management. CRC Press, Boca Raton, pp 565–607
Saunders DS (1976) Insect clocks. Pergamon Press, Oxford
Shintani Y, Kato Y, Saito T, Oda Y, Terao M, Nagamine K (2018) Maladaptive photoperiodic response in an invasive alien insect, Milionia basalis pryeri (Lepidoptera: Geometridae), in southern Kyushu, Japan. Appl Entomol Zool 53(3):343–351. https://doi.org/10.1007/s13355-018-0562-z
SYSTAT 10.2 (2018) https://systat.informer.com/10.2/ Accessed 22 Dec 2018
Tauber MJ, Tauber CA, Masaki S (1986) Seasonal adaptations of insects. Oxford University Press, New York
Tyshchenko VP (1980) Signal and vital modes of action of ecological factors. Zhurnal Obshey Biologii [J General Biol] 41:655–667
Urbanski J, Mogi M, O’Donnell D, DeCotiis M, Toma T, Armbruster P (2012) Rapid adaptive evolution of photoperiodic response during invasion and range expansion across a climatic gradient. Am Nat 179:490–500. https://doi.org/10.1086/664709
Watanabe M (1979) Ecology and extermination of Halyomorpha halys. 4. The relationship between day length and ovarian development. Ann Rep Toyama Inst Health 3:33–37
Watanabe M (1980) Study of the life cycle of the brown marmorated stink bug, Halyomorpha mista. Insectarium 17:168–173
Xu J, Fonseca DM, Hamilton GC et al (2014) Tracing the origin of US brown marmorated stink bugs, Halyomorpha halys. Biol Invasion 16:153–166. https://doi.org/10.1007/s10530-013-0510-3
Yanagi T, Hagihara Y (1980) Ecology of the brown marmorated stink bug. Plant Prot 34:315–321
Zhu G, Bu W, Gao Y, Liu G (2012) Potential geographic distribution of brown marmorated stink bug invasion (Halyomorpha halys). PLoS ONE 7:e31246. https://doi.org/10.1371/journal.pone.003124
Acknowledgements
The present study was partially supported by the Russian Foundation for Basic Research (Grant No. 17-04-01486 for DLM), the EU COST Action FP1401 Global Warning (A global network of nurseries as early warning system against alien tree pests; http://www.cost.eu/COST_Actions/fps/FP1401 for DLM), the Russian state research project AAAA-A17-117030310205-9 (for MYuD and SYaR), and The Innessa Charitable Foundation (for AKhS). We sincerely thank Dr. J.F. Esquivel (USDA, ARS, SPARC), Dr. K. Tsytsulina and anonymous reviewers for critical reading of the MS and helpful comments, Dr. K. Samartsev for photographs, and T.Yu. Moskaleva for assistance with the experiments.
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Musolin, D.L., Dolgovskaya, M.Y., Protsenko, V.Y. et al. Photoperiodic and temperature control of nymphal growth and adult diapause induction in the invasive Caucasian population of the brown marmorated stink bug, Halyomorpha halys. J Pest Sci 92, 621–631 (2019). https://doi.org/10.1007/s10340-019-01080-1
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DOI: https://doi.org/10.1007/s10340-019-01080-1