Abstract
Lower development threshold temperatures (LDT) of gall midges (Diptera: Cecidomyiidae) were directly determined by comparing developmental stages before and after incubation of galls for a definite period under a range of temperatures sufficient to cover the borders of the linear response. The LDT was determined to be 15 and 17 °C, respectively, for the soybean-pod gall midge, Asphondylia yushimai Yukawa and Uechi, and the ampelopsis fruit-gall midge, A. baca Monzen. They are host-alternating multivoltine species, but their LDT did not differ between generations on winter–spring and summer–autumn hosts, supporting the hypothesis that the value of LDT is stable and species specific. Based on the LDT and the 50 % emergence dates (ET50) of an overwintered generation, we estimated the thermal constants from first instars to adults to be 47.4 day-degrees for A. yushimai and 164.9 day-degrees for A. baca. The estimated thermal constant enables A. yushimai to repeat many generations annually, which may support the possibility that the gall-midge infestation range expands every summer and autumn from southern to northern Honshu, where winter–spring hosts have never been detected. The larval development of A. yushimai and A. baca, as well as those of two other univoltine congeners, A. aucubae Yukawa and Ohsaki and A. sphaera Monzen, was delayed at temperatures of 26, 28, or 29 °C. Global warming, when it becomes more prominent, will reduce the number of generations and the survival rate of multivoltine gall midges that spend summer without diapause.
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Bale JS, Masters GJ, Hodkinson ID, Wmack CA, Bezemer TM, Brown VK, Butterfield J, Buse A, Coulson JC, Farrar J, Good JEG, Harrington R, Hartley S, Jones TH, Lindroth RL, Press MC, Symrnioudis I, Watt AD, Whittaker JB (2002) Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Glob Change Biol 8:1–16
Baxendale FP, Teetes GL, Sharpe PJH, Wu H (1984) Temperature-dependent model for development of nondiapausing sorghum midges (Diptera: Cecidomyiidae). Environ Entomol 13:1572–1576
Bergant K, Trdan S (2006) How reliable are thermal constants for insect development when estimated from laboratory experiments? Entomol Exp Appl 120:251–256
Craig RR, Oscar EL (2010) Pupation and emergence of blueberry gall midge, Dasineura oxycoccana (Diptera: Cecidomyiidae), under varying temperature conditions. Fla Entomol 93:283–290
Foster JE, Taylor PL (1975) Thermal-unit requirements for development of the hessian fly under controlled conditions. Environ Entomol 4:195–202
Hellqvist S (2001) Phenology of the blackcurrant leaf midge (Dasineura tetensi) in Northern Sweden. Acta Agr Scand B 51:84–90
Hinz H (1998) Life history and host specificity of Rhopalomyia n. sp. (Diptera: Cecidomyiidae), a potential biological control agent of scentless chamomile. Environ Entomol 27:1537–1547
Hodek I, Honěk A (1996) Ecology of Coccinellidae. Kluwer Acad Pub, London
Hokkaido Plant Protection Office (2013) Plant diseases and pests newly found in Hokkaido from 1991 to 2014. www.agri.hro.or.jp/boujosho/sinhassei/index.htm (in Japanese)
Honěk A (1996) The relationship between thermal constants for insect development: a verification. Acta Soc Zool Bohem 60:115–152
Kim W, Matsunaga K, Gyoutoku N, Matsuo L, Minami T, Yukawa J (2015) Life history strategy and adult and larval behavior of Macrodiplosis selenis (Diptera: Cecidomyiidae), a species that induces leaf-margin fold galls on deciduous Quercus (Fagaceae). Entomol Sci 18:470–478
Kingsolver JG, Diamond SE, Buckley LB (2013) Heat stress and the fitness consequences of climate change for terrestrial ectotherms. Funct Ecol 27:1–9
Kiritani K (1997) The low developmental threshold temperature and the thermal constant in insects, mites and nematodes in Japan. Mis Pub Natl Inst Agro Environ Sci 21:72
Kiritani K (2010) Heat stress on and minimum development temperature of insects with future prospects for Nezara viridula. In: Kiritani K, Yukawa J (eds) Effects of global warming on insects. Zenkoku Nôson Kyôiku Kyôkai, Tokyo, pp 300–308 (in Japanese)
Kiritani K (2011) Impacts of global warming on Nezara viridula and its native congeneric species. J Asia Pac Entomol. 14:221–226
Kiritani K (2012) The low development threshold temperature and the thermal constant in insects and mites in Japan (2nd edition). Bull Natl Inst Agro Environ Sci 31:1–74 (in Japanese with English summary)
Kiritani K, Yamashita H (2008) Phenology of reproduction and the lower development threshold in Carabus lewisianus Breuning. Jpn J Appl Entomol Zool 52:77–86 (in Japanese with English abstract)
Kiritani K, Yukawa J (eds.) (2010) Effects of global warming on insects. Zenkoku Nôson Kyôiku Kyôkai, Tokyo (in Japanese)
Ladányi M, Horváth L (2010) A review of the potential climate change impact on insect populations—general and agricultural aspects. Appl Ecol Env Res 8:143–152
Mason L, Strait CA (1998) Stored product integrated pest management with extreme temperatures. In: Hallman GJ, Denlinger DL (eds) Temperature sensitivity in insects and application in integrated pest management. Westview Press, Oxford, pp 141–177
Matsui M (1987) The developmental period of the soybean pod gall midge, Asphondylia sp. (Diptera: Cecidomyiidae). Jpn J Appl Entomol Zool 31:414–416 (in Japanese)
Musolin DL, Tougou D, Fujisaki K (2009) Too hot to handle? Phenological and life-history responses to simulated climate change of the southern green stink bug Nezara viridula (Heteropetra: Pentatomidae). Glob Change Biol 16:73–87
Nam Y, Choi W (2014) An empirical predictive model for the spring emergence of Thecodiplosis japonensis (Diptera: Cecidomyiidae): model construction and validation on the basis of 25 years of field observation data. J Econ Entomol 107:1136–1141
Noll J (1959) Über den Einfluss von Temperatur und Bodenfeuchtigkeit auf die Larven und Puppen der Kohldrehherzmücke Contarinia nasturtii (Kieffer) als Grundlage für die Vorausberechnung der ersten Schjlupftermins im Frühjahr. Arch Garten 7:362–415
Ohtani T, Yazawa Y, Yukawa J (1983) Developmental zero point of the ligustrum fruit midge, Asphondylia sphaera Monzen and the aucuba fruit midge, Asphondylia sp. (Diptera: Cecidomyiidae). Proc Assoc Pl Prot Kyushu 29:118–121 (in Japanese with English summary)
Okuda S, Yukawa J (2000) Life history strategy of Tokiwadiplosis matecola (Diptera: Cecidomyiidae) relying upon the lammas shoots of Lithocarpus edulis (Fagaceae). Entomol Sci 3:47–56
Readshaw JL (1966) The ecology of the swede midge, Contarinia nasturtii (Kieffer) (Diptera: Cecidomyiidae). 1. Life history and influences of temperature on development. B Entomol Res 56:685–700
Shibuya S (1997) Voltinism of the soybean pod gall midge, Asphondylia sp. (Diptera, Cecidomyiidae) and the prediction of its infestation. Pl Prot 51:560–564 (in Japanese)
Son Y, Lee JH, Chung YJ (2007) Temperature-dependent post-diapause development and prediction of spring emergence of the pine needle gall midge (Diptera: Cecidomyiidae). J Appl Entomol 131:674–683
Tamura I (1952) Ecological studies on the insect injury of soy bean plant. Bunkyôsha, Tokyo (in Japanese with English summary)
Uechi N, Yukawa J (2006) Life history patterns and host ranges of the genus Asphondylia (Diptera: Cecidomyiidae). In: Ozaki K, Yukawa J, Ohgushi T, Price PW (eds) Galling Arthropods and Their Associates: Ecology and Evolution. Springer-Verlag, Tokyo, pp 275–285
Uechi N, Yukawa J, Yamaguchi D (2004) Host alternation by gall midges of the genus Asphondylia (Diptera: Cecidomyiidae). In: Evenhuis NL, Kaneshiro KY (eds) In contributions to the systematics and evolution of Diptera, D. Elmo Hardy Mem, Bishop Mus Bull Entomol 12. Bishop Museum Press, Honolulu, pp 53–66
Uechi N, Yukawa J, Usuba S (2005) Discovery of an additional winter host of the soybean pod gall midge, Asphondylia yushimai (Diptera: Cecidomyiidae) in Japan. Appl Entomol Zool 40:597–607
Wise IL, Lamb RJ (2004) Diapause and emergence of Sitodiplosis mosellana (Diptera: Cecidomyiidae) and its parasitoid Macroglenes penetrans (Hymenoptera: Pteromalidae). Can Entomol 136:77–90
Yukawa J (1987) Life history strategies of univoltine gall-making Cecidomyiidae (Diptera) in Japan. Phytophaga 1:121–139
Yukawa J (2000) Synchronization of gallers with host plant phenology. Popul Ecol 42:105–113
Yukawa J, Akimoto K (2006) Influence of synchronization between adult emergence and host plant phenology on the population density of Pseudasphondylia neolitseae (Diptera: Cecidomyiidae) inducing leaf galls on Neolitsea sericea (Lauraceae). Popul Ecol 48:13–21
Yukawa J, Masuda H (1996) Insect and mite galls of Japan in colors. Zenkoku Nôson Kyôiku Kyôkai, Tokyo (in Japanese with English explanation for color plates)
Yukawa J, Uechi N, Horikiri M, Tuda M (2003) Description of the soybean pod gall midge, Asphondylia yushimai sp. n. (Diptera: Cecidomyiidae), a major pest of soybean and findings of host alternation. B Entomol Res 93:73–86
Yukawa J, Nakagawa K, Saigou T, Awa T, Fukuda T, Higashi M (2013) Adult behavior of an ambrosia gall midge Illiciomyia yukawai (Diptera: Cecidomyiidae) and synchronization between its emergence and host plant phenology. Entomol Sci 16:400–412
Acknowledgments
We express our thanks to Dr. K. Kiritani (Emeritus Researcher, NARO Institute for Agro-environmental Sciences, Japan), Dr. K. M. Harris (former Director of the International Institute of Entomology, UK), and Prof. T. Hirowatari (Kyushu University, Japan) for their critical reading of an early draft. We thank the late Mr. Y. Ariyoshi, Mr. H. Ueda (Botanical Garden of Fukuoka City), and Ms. S. Seto, Ms. A. Sugita, and Mr. D. Yamaguchi (Kyushu University) for their help in collecting, rearing, and dissecting galls. We are grateful to Dr. M. Tuda (Kyushu University) for providing us with incubators for rearing experiments.
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Yukawa, J., Ichinose, M., Kim, W. et al. Lower development threshold temperatures and thermal constants for four species of Asphondylia (Diptera: Cecidomyiidae) in Japan and their larval developmental delay caused by heat stress. Appl Entomol Zool 51, 71–80 (2016). https://doi.org/10.1007/s13355-015-0372-5
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DOI: https://doi.org/10.1007/s13355-015-0372-5