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Plasticity of nutrient accumulation patterns in diapausing fall webworm pupae

Published online by Cambridge University Press:  31 March 2021

Lvquan Zhao Open the ORCID record for Lvquan Zhao [Opens in a new window] ,
Wei Wang ,
Ying Qiu  and
Alex S. Torson
Lvquan Zhao*
Affiliation:
Co-innovation Center for Sustainable Forestry in Southern China, College of Forestry, Nanjing Forestry University, Nanjing210037, China
Wei Wang
Affiliation:
Co-innovation Center for Sustainable Forestry in Southern China, College of Forestry, Nanjing Forestry University, Nanjing210037, China
Ying Qiu
Affiliation:
Co-innovation Center for Sustainable Forestry in Southern China, College of Forestry, Nanjing Forestry University, Nanjing210037, China
Alex S. Torson
Affiliation:
Department of Biology, The University of Western Ontario, London, ONN6A 5B7, Canada
*
Author for correspondence: Lvquan Zhao, Email: zhaolvquan@njfu.edu.cn
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Abstract

The accumulation of nutrients during diapause preparation is crucial because any lack of nutrition will reduce the likelihood of insects completing diapause, thereby decreasing their chances of survival and reproduction. The fall webworm, Hyphantria cunea, diapause as overwintering pupae and their diapause incidence and diapause intensity are regulated by the photoperiod. In this study, we test the hypothesis that photoperiod influences energy reserve accumulation during diapause preparation in fall webworm. We found that the body size and mass, lipid and carbohydrate content of pupae with a short photoperiod during the diapause induction phase were significantly greater than those of pupae with a relatively short photoperiod, and the efficiency of converting digested food and ingested food into body matter was greater in the short-photoperiod diapause-destined larvae than the relatively short-photoperiod diapause-destined larvae. We also observed higher lipase and amylase activities in short-photoperiod diapause-destined larvae relative to the counterparts. However, no obvious difference was found in protein and protease in the pupae with a short photoperiod during the diapause induction phase and short-photoperiod diapause-destined larvae compared with the counterparts. Therefore, we conclude that the energy reserve patterns of diapausing fall webworm pupae are plastic and that short-photoperiod diapause-destined larvae increase their energy reserves by improving their feeding efficiency and increase their lipid and carbohydrate stores by increasing the lipase and amylase activities in the midgut.

Keywords

Diapauseenergy reservesenzyme activityfeeding efficiencyLepidopteraphotoperiodplasticity
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 111 , Issue 6 , December 2021 , pp. 637 - 644
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Bernfeld, MM (1955) Amylases, a and b. In Colowick, SP and Kaplan, N (eds), Methods in Enzymology, vol. I. New York, NY, USA: Academic Press, 149–158.CrossRefGoogle Scholar
Cao, LJ, Yang, F, Tang, SY and Chen, M (2014) Development of an artificial diet for three lepidopteran insects. Chinese Journal of Applied Entomology 51, 1376–1386.Google Scholar
Carroll, NV, Longley, RW and Roe, JH (1956) Determination of glycogen in liver and muscle by use of anthrone reagent. Journal of Biological Chemistry 220, 583–593.CrossRefGoogle ScholarPubMed
Chen, YS, Chen, C, He, HM, Xia, QW and Xue, FS (2013) Geographic variation in diapause induction and termination of the cotton bollworm, Helicoverpa armigera Hübner (Lepidoptera: Noctuidae). Journal of Insect Physiology 59, 855–862.CrossRefGoogle Scholar
Chen, C, Wei, XT, Xiao, HJ, He, HM, Xia, QW and Xue, FS (2014) Diapause induction and termination in Hyphantria cunea (Drury) (Lepidoptera: Arctiinae). PLoS ONE 9, e98145. doi: 10.1371/journal.pone.0098145CrossRefGoogle Scholar
Danks, HV (1987) Insect Dormancy: An Ecological Perspective. Biological Survey of Canada (Terrestrial Arthropods).Google Scholar
Denlinger, DL (1991) Relationship between cold hardiness and diapause. In Lee, RE Jr. and Denlinger, DL (eds), Insects at Low Temperature. New York: Chapman & Hall, 174–198.CrossRefGoogle Scholar
Denlinger, DL (2002) Regulation of diapause. Annual Review of Entomology 47, 93–122.CrossRefGoogle ScholarPubMed
Denlinger, DL, Yocum, GD and Rinehart, JL (2005) Hormonal control of diapause. In Gilbert, LI, Iatrou, K and Gill, SS (eds), Comprehensive Molecular Insect Science, vol. 3. Amsterdam: Elsevier Press, 615–650.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Hahn, DA and Denlinger, DL (2007) Meeting the energetic demands of insect diapause: nutrient storage and utilization. Journal of Insect Physiology 53, 760–773.CrossRefGoogle ScholarPubMed
Hahn, DA and Denlinger, DL (2011) Energetics of insect diapause. Annual Review of Entomology 56, 103–121.CrossRefGoogle ScholarPubMed
Han, B and Denlinger, DL (2009) Mendelian inheritance of pupal diapause in the flesh fly, Sarcophaga bullata. Journal of Heredity 100, 251–255.CrossRefGoogle ScholarPubMed
Irwin, JT and Lee, RE Jr (2003) Cold winter microenvironments conserve energy and improve overwintering survival and potential fecundity of the goldenrod gall fly, Eurosta solidaginis. Oikos 100, 71–78.CrossRefGoogle Scholar
Ji, R, Xi, BY, Li, XH, Gao, ZX and Li, DM (2003) Research progress on the invasive species Hyphantria cunea. Entomological Knowledge 40, 13–18.Google Scholar
Kong, HL, Luo, LZ, Jiang, XF, Zhang, L, Yang, ZL and Hu, Y (2012) Effects of larval density on food utilization efficiency and digestive enzyme activity of the beet webworm, Loxostege sticticalis (Lepidoptera: Pyralidae). Acta Entomologica Sinica 55, 361–366.Google Scholar
Koštál, V (2006) Eco-physiological phases of insect diapause. Journal of Insect Physiology 52, 113–127.CrossRefGoogle ScholarPubMed
Liu, J, Ye, LQ, Cheng, G, Xiong, DB and Chen, ZY (2016) The occurrence of forestry pests in 2015 and its occurrence trend prediction in 2016 in Jiangsu Province. Journal of Jinling Institute of Technology 32, 64–67.Google Scholar
Loewy, K, Flansburg, AL, Grenis, K and Murphy, SM (2013) Life history traits and rearing techniques for fall webworms (Hyphantria cunea Drury) in Colorado. Journal of the Lepidopterists’ Society 67, 196–205.CrossRefGoogle Scholar
Lorenz, MW (2003) Adipokinetic hormone inhibits the formation of energy stores and egg production in the cricket Gryllus bimaculatus. Comparative Biochemistry and Physiology B 136, 197–206.CrossRefGoogle ScholarPubMed
Masaki, S, Umeya, K, Sekiguchi, Y and Kawasaki, R (1968) Biology of Hyphantria cunea Drury (Lepidoptera : Arctiidae) in Japan III. Photoperiodic induction of diapause in relation to the seasonal life cycle. Applied Entomology and Zoology 3, 55–66.CrossRefGoogle Scholar
Mole, S and Zera, AJ (1993) Differential allocation of resources underlies the dispersal-reproduction trade-off in the wingdimorphic cricket, Gryllus rubens. Oecologia 93, 121–127.CrossRefGoogle ScholarPubMed
Raubenheimer, D and Simpson, SJ (1992) Analysis of covariance: an alternative to nutritional indices. Entomologia Experimentalis et Appicata 62, 221–231.CrossRefGoogle Scholar
Rehnberg, BG (2006) Temperature profiles inside webs of the fall webworm, Hyphantria cunea (Lepidoptera: Arctiidae): influence of weather, compass orientation, and time of day. Journal of Thermal Biology 31, 274–279.CrossRefGoogle Scholar
Schulte, PM, Healy, TM and Fangue, NA (2011) Thermal performance curves, phenotypic plasticity, and the time scales of temperature exposure. Integrative and Comparative Biology 51, 691–702.CrossRefGoogle ScholarPubMed
Shin, SM, Akram, W and Lee, JJ (2012) Effect of body size on energy reserves in Culex pipiens pallens females (Diptera: Culicidae). Entomological Research 42, 163–167.CrossRefGoogle Scholar
Sinclair, BJ (2015) Linking energetics and overwintering in temperate insects. Journal of Thermal Biology 54, 5–11.CrossRefGoogle ScholarPubMed
Sinclair, BJ and Marshall, KE (2018) The many roles of fats in overwintering insects. Journal of Experimental Biology 221, jeb161836.CrossRefGoogle ScholarPubMed
Tan, QQ, Feng, L, Liu, W, Zhu, L, Lei, CL and Wang, XP (2016) Differences in the pre-diapause and pre-oviposition accumulation of critical nutrients in adult females of the beetle Colaphellus bowringi. Entomologia Experimentalis et Applicata 160, 117–125.CrossRefGoogle Scholar
Tanaka, S (1991) De-alation and its influences on egg production and flight muscle histolysis in a cricket (Velarifictorus parvus) that undergoes inter-reproductive migration. Journal of Insect Physiology 37, 517–523.CrossRefGoogle Scholar
Tanaka, S and Zhu, DH (2008) Geographic variation of embryonic diapause, cold-hardiness and life cycles in the migratory locust, Locusta migratoria (Orthoptera: Acrididae), in China. Entomological Science 11, 327–339.CrossRefGoogle Scholar
Tanaka, S, Arai, T and Tanaka, K (1999) Nymphal development, diapause and cold-hardiness in a nymph-overwintering cricket. Entomological Science 2, 173–182.Google Scholar
Tauber, MJ, Tauber, CA and Masaki, S (1986) Seasonal Adaptations of Insects. New York: Oxford University Press, 411.Google Scholar
Wei, XT, Xiao, HJ, Yang, D, Wu, SH and Xue, FS (2006) Several important biological characters in the fall webworm, Hyhandria cunea. Plant Quarantine 1, 14–17.Google Scholar
Weidlich, S, Huster, J, Hoffmann, KH and Woodring, J (2012) Environmental control of trypsin secretion in the midgut of the two-spotted field cricket, Gryllus bimaculatus. Journal of Insect Physiology 58, 1477–1484.CrossRefGoogle ScholarPubMed
Weidlich, S, Müller, S, Hoffmann, KH and Woodring, J (2013) Regulation of amylase, cellulase and chitinase secretion in the digestive tract of the two-spotted field cricket, Gryllus bimaculatus. Archives of Insect Biochemistry and Physiology 83, 69–85.CrossRefGoogle ScholarPubMed
Williams, CM, Chick, WD and Sinclair, BJ (2015) A cross-seasonal perspective on local adaptation: metabolic plasticity mediates responses to winter in a thermal-generalist moth. Functional Ecology 29, 549–561.CrossRefGoogle Scholar
Williams, CM, Marshall, KE, MacMillan, HA, Dzurisin, JDK, Hellmann, JJ, et al. (2012) Thermal variability increases the impact of autumnal warming and drives metabolic depression in an overwintering butterfly. PLoS ONE 7, e34470. doi: doi: 10.1371/journal.pone.0034470CrossRefGoogle Scholar
Woodring, J, Hoffmann, K and Lorenz, M (2007) Activity, release and flow of digestive enzymes in the cricket, Gryllus bimaculatus. Physiological Entomology 32, 56–63.CrossRefGoogle Scholar
Yang, HZ, Tu, XY, Xia, QW, He, HM, Chen, C and Xue, FS (2014) Photoperiodism of diapause induction and diapause termination in Ostrinia furnacalis (Lepidoptera: Crambidae). Entomologia Experimentalis et Applicata 153, 34–46.CrossRefGoogle Scholar
Zhao, LQ, Liao, HY, Zeng, Y, Wu, HJ and Zhu, DH (2017) Food digestion capability and digestive enzyme activity in female adults of the wing-dimorphic cricket Velarifictorus ornatus. Entomologia Experimentalis et Applicata 163, 35–42.CrossRefGoogle Scholar
Zhao, LQ, Wang, W, Qiu, Y and Torson, AS. Physiological mechanisms of variable nutrient accumulation patterns between diapausing and non-diapausing fall webworm (Lepidoptera: Arctiidae) pupae (unpublished).Google Scholar