Development of defoliating insects and their preferences for host plants under varying temperatures in a subtropical evergreen forest in eastern China

Abstract

The aim of this work was to understand the development of defoliating insects and their preferences for host plants under varying temperatures in a subtropical evergreen broad-leaved forest in China. We measured the main developmental parameters of three typical defoliating insects (i.e., Ourapteryx ebuleata szechuana, Biston marginata, and Euproctis angulata) and their preferences for five host plants at temperatures from 16°C to 31°C at 3°C intervals in the Tiantong National Forest Research station in eastern China. The results showed the following. 1) An appropriate rise in temperature increases the survival rate with an increase in the number of offspring. The developmental durations for these three insects were shortened, and pupal weight increased with an increase in temperature. 2) A shift in the preference for host plants for these three insects was observedat elevated temperatures. They all preferred to feed on Schima superba and Castanopsis sclerophylla at elevated temperatures, showing an opposite response to the other three plants. The daily leaf consumption of the three insects was positively correlated with their feeding preference, with more leaves being consumed from the plants they preferred. 3) For O. ebuleata szechuana larvae, daily leaf consumption initially increased and then decreased with increasing temperatures. In contrast, Biston marginata and Euproctis angulata larvae consumed more leaves at elevated temperatures. The feeding preferences of O. ebuleata szechuana and Biston marginata were more sensitive to changing temperatures than that of Euproctis angulata laevae. We concluded that increased numbers of offspring and generations, pupal weights, and a shift in preference to two plants for these three defoliating insects might lead to severe damage to these two plants which would enhance the fragmentation and decrease the stability of the forest communities under changing temperatures. Meanwhile, the variations in the responses of defoliating insects to the changing temperatures should be taken into consideration for the pest management of forests to adapt to the changing climate.

Keywords

defoliating insects / elevated temperature / development dynamics / feeding behavior / subtropical evergreen forest

References

[1] Agrawal A A, Fishbein M (2006). Plant defense syndromes. Ecology, 87(sp7): S132–S149

[2] Bidart-Bouzat M G, Imeh-Nathaniel A (2008). Global change effects on plant chemical defenses against insect herbivores. J Integr Plant Biol, 50(11): 1339–1354

[3] Borchert R, Robertson K, Schwartz M D, Williams-Linera G (2005). Phenology of temperate trees in tropical climate. Int J Biometeorol, 50(1): 57–65

[4] Calixto E S, Lange D, Del-Claro K (2015). Foliar anti-herbivore defenses in Qualea multiflora Mart. (Vochysiaceae): changing strategy according to leaf development. Flora, 212: 19–23

[5] Chen Y, Ma C S (2010). Effect of global warming on insect: a literature review. Acta Ecol Sin, 30(8): 2159–2172

[6] Chuine I, Morin X, Bugmann H (2010). Warming photoperiods and tree phenology. Science, 329(5989): 277–278

[7] Chung M Y, Moon M O, López-Pujol J, Chung I M, Chung M G (2013). Genetic diversity in the two endangered endemic species Kirengeshoma koreana (Hydrangeaceae) and Parasenecio pseudotaimingasa (Asteraceae) from Korea: Insights into population history and implications for conservation. Biochem Syst Ecol, 51: 60–69.

[8] Coley P D, Barone J A (1996). Herbivory and plant defenses in tropical forests. Annu Rev Ecol Syst, 27(1): 305–335

[9] Cribb B W, Hanan J, Zalucki M P, Perkins L E (2010). Effects of plant micro-environment on movement of Helicoverpa armigera (Hübner) larvae and the relationship to a hierarchy of stimuli. Arthropod-Plant Interact, 4(3): 165–173

[10] Dardeau F, Pointeau S, Ameline A, Laurans F, Cherqui A, Lieutier F, Salle A (2014). Host manipulation by a herbivore optimizes its feeding behavior. Anim Behav, 95: 49–56

[11] Davidson D W ,Mckey D (1993). Ant-plant symbioses: Stalking the chuyachaqui.Trends Ecol Evol , 8(9): 326–332.

[12] Delaney K J (2012). Nerium oleander indirect leaf photosynthesis and light harvesting reductions after clipping injury or Spodoptera eridania herbivory: high sensitivity to injury. Plant Sci, 185 ‒ 186: 218–226

[13] Denis D, Pierre J S, van Baaren J, van Alphen J J M (2012). Physiological adaptations to climate change in pro-ovigenic parasitoids. J Theor Biol, 309: 67–77

[14] Dielaman W I J, Venter M, Ramachandra A, Krockenberger A K, Bird M I (2013). Soil carbon stocks vary predictably with altitude in tropical forests: Implications for soil carbon storage. Geoderma, 204-205: 59–67.

[15] Du Y L, Guo H M, Sun S L, Zhang M Z, Zhang A H, Wang J B, Qin L (2012). Effects of temperature on the development and reproduction of the yellow peach moth, Conogethes punctiferalis (Lepidoptera: Pyralidae). Acta Entomol Sin, 55(5): 561–569

[16] Everatt M J, Bale J S, Convey P, Worland M R, Hayward S A L (2013). The effect of acclimation temperature on thermal activity thresholds in polar terrestrial invertebrates. J Insect Physiol, 59(10): 1057–1064

[17] Feeny P P (1970). Seasonal changes in Oak leaf tannins and nutrients as a cause of spring feeding by winter moth caterpillars. Ecology, 51(4): 565–581

[18] Fleurat-Lessard F, DupuisS A(2010). Comparative analysis of upper thermal tolerance and co2 production rate during heat stock in two different European strains of Sitophilus zeamais (Coleoptera: Curculionidae). J Stored Prod Res, 46(1): 20–27

[19] Ge F (2011). Challenges facing entomologists in a changing global climate. Chin J Appl Entomol, 48(5): 1117–1122

[20] Giffard B, Jactel H, Corcket E, Barbaro L (2012). Influence of surrounding vegetation on insect herbivory: a matter of spatial scale and herbivore specialization. Basic Appl Ecol, 13(5): 458–465

[21] Gomi T, Adachi K, Shimizu A, Tanimoto K, Kawabata E, Takeda M (2009). Northerly shift in voltinism watershed in Hyphantria cunea (Drury) (Lepidoptera: Arctiidae) along the Japan sea coast: Evidence of global warming? Appl Entomol Zool (Jpn), 44(3): 357–362

[22] Hódar J A, Castro J, Zamora R (2003). Pine processionary caterpillar Thaumetopoea pityocampa as a new threat for relict Mediterranean Scots pine forests under climatic warming. Biol Conserv, 110(1): 123–129

[23] IPCC (2013). Climate Change 2013: The physical Science Basis. In: Solomon S D, Qin M, Manning Z, Chen M, Marquis K B, Averyt M, Tignor H L Miller, eds. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change.Cambridge and New York: Cambridge University Press

[24] Jermy T, Hanson F E, Dethier V G (1968). Introduction of specific food preference in lepidopterous larvae. Entomol Exp Appl, 11(2): 211–230

[25] Karageorgou P, Buschmann C, Manetas Y (2008). Red leaf color as a warning signal against insect herbivory: honest or mimetic? Flora, 203(8): 648–652

[26] Kardol P, Campany C E, Souza L, Norby R J, Weltzin J F, Classen A T (2010). Climate change effects on plant biomass alter dominance patterns and community evenness in an experimental old-field ecosystem. Glob Change Biol, 16(10): 2676–2687

[27] Lemoine N P, Drews W A, Burkepile D E, Parker J D (2013). Increased temperature alters feeding behavior of a generalist herbivore. Oikos, 122(12): 1669–1678

[28] Liu Z G (2011). Defense syndromes of young leaves against insect herbivores in subtropical evergreen broad-leaved forests. East China Normal University, Shanghai.

[29] Liu ZG, Cai YL, Fang Y, Jing J, Li K. Induced response in Schima superba: Effects of early season herbivory on leaf traits and subsequent insect attack [J]. Afr J Biotechnol, 2010, 9(51): 8731–8738

[30] Nyamukondiwa C, Weldon C W, Chown S L, le Roux P C, Terblanche J S (2013). Thermal biology, population fluctuations and implications of temperature extremes for the management of two globally significant insect pests. J Insect Physiol, 59(12): 1199–1211

[31] Peters K, Breitsameter L, Gerowitt B (2014). Impact of climate change on weeds in agriculture: a review. Agron Sustain Dev, 34(4): 707–721

[32] Porter J (1995). The effects of climate change on the agricultural environments for crop insect pests with particular reference to the European corn borer and grain maize. In: Harrington R, Stork NE, eds. Insect in a Changing Environment. New York: Academic Press. 93–123

[33] Radchuk V, Johst K, Groeneveld J, Grimm V, Schtickzelle N (2013). Behind the scenes of population viability modeling: predicting butterfly metapopulation dynamics under climate change. Ecol Modell, 259: 62–73

[34] Régnière J, Powell J, Bentz B, Nealis V (2012). Effects of temperature on development, survival and reproduction of insects: experimental design, data analysis and modeling. J Insect Physiol, 58(5): 634–647

[35] Salin C, Renault D, Vannier G, Vernon P (2006). Critical thermal maximum and water loss in developmental stages of the lesser mealworm Alphitobius diaperinus. Acta Zool Sin, 52(1): 79–86

[36] Song Y C, Chen X Y (2007). Degradation Mechanism and Ecological Restoration of Evergreen Broad-Leaved Forest Ecosystem in East China.Beijing: Science Press, 393–405

[37] Strauss R E (2001). Cluster analysis and the identification of aggregations. Ani Behav, 61(2): 481–488.

[38] Su C, Jing J, Wang M M, Fang Y, Li K (2013). Effects of different host plants on the development and fecundity of Lemyra alikangensis (Strand) (Lepidoptera: Arctiidae). Chin J Appl Entomol, 50(6): 1614–1621

[39] Sun R Y (2001). Animal Ecology.Beijing: Beijing Normal University Press

[40] Teimouri N, Sendi J J, Zibaee A, Khosravi R (2013). Feeding indices and enzymatic activities of carob moth Ectomyelois ceratoniae(Zeller) (Lepidoptera: pyrallidae) on two commercial pistachio cultivars and an artificial diet. J Saudi Soc Agr Sci, 2–7

[41] Thomson L J, Macfadyen S, Hoffmann A A (2010). Predicting the effects of climate change on natural enemies of agricultural pests. Biol Control, 52(3): 296–306

[42] Tian Y P, Cai Y L, Wang H W, Liu Z G, Qiu Y X, Chen Z F (2007). The traits of leaf lifespan of 51 evergreen broad-leaved species and analysis on the influencing factors of Mt. Meihuashan, Fujian Province. Subtropical Plant Sci, 36(2): 4–8

[43] Unsicker S B, Kunert G, Gershenzon J (2009). Protective perfumes: the role of vegetative volatiles in plant defense against herbivores. Curr Opin Plant Biol, 12(4): 479–485

[44] van Velzen E, Etienne R L (2015). The importance of ecological costs for the evolution of plant defense against herbivory. J Theor Biol, 372: 89–99

[45] Visser M E, Holleman L J M (2001). Warmer springs disrupt the synchrony of oak and winter moth phenology. Proc Biol Sci, 268(1464): 289–294

[46] Wang H W (2007). Studies on Herbivory and Its Influencing Factors of Plants in Subtropical Evergreen Broad-leaved Forest. East China Normal University, Shanghai.

[47] Weed A S, Gassmann A, Casagrande R A (2011). Effects of leaf and root herbivory by potential insect biological control agents on the performance of invasive Vincetoxicum spp. Biol Control, 56(1): 50–58

[48] Yamanaka T, Tatsuki S, Shimada M (2008). Adaptation to the new land or effect of global warming? An age-structured model for rapid voltinism change in an alien lepidopteran pest. J Anim Ecol, 77(3): 585–596

[49] Yamazaki K, Lev-Yadun S (2015). Dense white trichome production by plants as possible mimicry of arthropod silk or fungal hyphae that deter herbivory. J Theor Biol, 364: 1–6

[50] Yao F L, You M S (2012). Impacts of global warming on the interaction between host plants, insect pests and their natural enemies. Chin J Appl Entomol, 49(3): 563–572

[51] Yuan H E, Yan S C, Tong L L, Gao L L, Wang Y J (2009). Content differences of condensed tannin in needles of Larix gmelinii by cutting needles and insect feeding. Acta Ecol Sin, 29(3): 1415–1420

Acknowledgements

This work was supported by the National Natural Science Foundation of China (Grant No. 30570329), and Key Projects of Science and Technology Commission of Shanghai Municipality (Nos. 09DZ120901 and 10QH1400700) and Shanghai Science Foundation (No. 06RTZ1412), the Open Research Fund of the State Key Laboratory of Estuarine and Coastal Research (No. SKLEC-KF201411). We are grateful to Senior Engineer Mr. Xianwei Liu for the diagnosis of insect specimens. We also thank Mr. Chao Su for field work and laboratory experiment.

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