Abstract
Diet quality influences arthropod performance under changing environments. However, little is known about how host plant species may influence the responses of polyphagous insects to climate stressors despite their exploitation of different plant species within and across seasons. Against this background, we examined the effects of host plant species (Zea mays L. and Sorghum bicolor L. Moench) on the thermal tolerance of Chilo partellus (Swinhoe) (Lepidoptera: Crambidae) measured as lower and upper thermal activity limits, chill coma recovery time and heat knockdown time. Experiments were conducted on field-collected larvae and laboratory-reared F1 larval offspring from each of the two host species. Our results showed significant host plant effects on both cold and heat tolerance. Insects from sweet sorghum showed higher thermal resilience (cold and heat) relative to those from maize as indicated by their low lower thermal activity limits (0.73 and 0.02 °C magnitude, respectively) and high upper thermal activity limits (0.5 and 0.28 °C magnitude, respectively). Both field and F1 larval populations from sweet sorghum recovered faster from chill coma and also took longer to be knocked down by acute heat stress, further affirming their superior thermal tolerance to those that fed on maize. These results therefore indicate that host plant species may potentially mediate thermal fitness of C. partellus. Despite wide adoption of sweet sorghum as a climate resilient crop owing to its drought tolerance and perennial nature, our findings suggest this may come at a cost of enhanced C. partellus performance and pest pressure under changing temperature environments.
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References
Andersen LH, Kristensen TN, Loeschcke V, Toft S, Mayntz D (2010) Protein and carbohydrate composition of larval food affects tolerance to thermal stress and desiccation in adult Drosopohila melanogaster. J Insect Physiol 56:336–340
Bale JS (2002) Insects and low temperatures: from molecular biology to distributions and abundance. Philos Trans R Soc B 357:849–862
Berger A (1992) Larval movement of Chilo partellus (Lepidoptera: Pyrallidae) within and between plants: timing, density responses and survival. Bull Entomol Res 82:441–448
Boardman L, Grout T, Terblanche JS (2012) False codling moth Thaumatotibia leucotreta (Lepidoptera: Tortricidae) larvae are chill-susceptible. Insect Sci 19:315–328
Bowler K, Terblanche JS (2008) Insect thermal tolerance: what is the role of ontogeny, ageing and senescence. Biol Rev 83:339–355
Buckley LB, Huey RB (2016) How extreme temperatures impact organisms and the evolution of their thermal tolerance. Integr Comp Biol 56:98–109
Chidawanyika F, Terblanche JS (2011) Rapid thermal responses and thermal tolerance in adult codling moth Cydia pomonella (Lepidoptera: Totricidae). J Insect Physiol 57:108–117
Chidawanyika F, Nyamukondiwa C, Strathie L, Fischer K (2017) Effects of thermal regimes, starvation and age on heat tolerance of the Parthenium Beetle Zygogramma bicolorata (Coleoptera: Chrysomelidae) following dynamic and static protocols. PLoS ONE 12:e0169371. https://doi.org/10.1371/journal.pone.0169371
Chown SL, Terblanche JS (2007) Physiological diversity in insects: ecological and evolutionary contexts. Adv Insect Physiol 33:50–152
Chown SL, Huiskes AH, Gremmen NJ, Lee JE, Terauds A, Crosbie K, Frenot Y, Hughes KA, Imura S, Kiefer K, Lebouvier M (2012) Continent-wide risk assessment for the establishment of nonindigenous species in Antarctica. Proc Natl Acad Sci USA 109:4938–4943
Colinet H, Renault D (2014) Dietary live yeast alters metabolic profiles, protein biosynthesis and thermal stress tolerance of Drosophila melanogaster. Comp Biochem Physiol A Mol Integr Physiol 170:6–14
Deutsch CA, Tewksbury JJ, Huey RB, Sheldon KS, Ghalambor CK, Haak DC, Martin PR (2008) Impacts of climate warming on terrestrial ectotherms across latitude. Proc Natl Acad Sci USA 105:6668–6672
Findsen A, Pedersen TH, Petersen AG, Nielsen OB, Overgaard J (2014) Why do insects enter and recover from chill coma? Low temperature and high extracellular potassium compromise muscle function in Locusta migratoria. J Exp Biol 217:1297–1306
Garcia-Robledo C, Charlotten-Silva M, Cruz C, Kuprewicz EK (2018) Low quality diet and challenging temperatures affect vital rates, but not thermal tolerance in a tropical insect expanding its diet to an exotic plant. J Therm Biol 77:7–13
Geister TL, Lorenz MW, Hoffmann KH, Fischer K (2008) Adult nutrition and butterfly fitness: effects of diet quality on reproductive output, egg composition, and egg hatching success. Front Zool 5:10
Gray EM, Bradley TJ (2005) Physiology of desiccation resistance in Anopheles gambiae and Anopheles arabiensis. Am J Trop Med Hyg 73:553–559
Hoffmann AA, Sørensen JG, Loeschcke V (2003) Adaptation of Drosophila to temperature extremes: bringing together quantitative and molecular approaches. J Therm Biol 28:175–216
Holopainen JK, Virjamo V, Ghimire RP, Blande JD, Julkunen-Tiitto R, Kivimäenpää M (2018) Climate change effects on secondary compounds of forest trees in the Northern Hemisphere. Front Plant Sci. https://doi.org/10.3389/fpls.2018.01445
Hosler JS, Burns JE, Esch HE (2000) Flight muscle resting potential and species-specific differences in chill coma. J Insect Physiol 46:621–627
Ju RT, Zhu HY, Gao L, Zhou XH, Li B (2015) Increases in both temperature means and extremes likely facilitate invasive herbivore outbreaks. Sci Rep 5:15715
Kawahigashi H, Kasuga S, Okuizumi H, Hiradate S, Yonemaru JI (2013) Evaluation of brix and sugar content in stem juice from sorghum varieties. Grassl Sci 59:11–19
Khadioli N, Tonnang ZEH, Muchugu E, Ong’amo G, Achia T, Kipchirchir I, Kroschel J, Le Ru B (2014) Effect of temperature on the phenology of Chilo partellus (Swinhoe) (Lepidoptera: Crambidae), simulation and visualization of the potential future distribution of C. partellus in Africa under warmer temperatures through the development of life-table parameters. Bull Entomol Res 104:809–822
Kleynhans E, Conlong D, Terblanche JS (2014) Host plant-related variation in thermal tolerance if Eldana saccharina. Entomol Exp Appl 150:113–122
Kristensen TN, Henningsen AK, Aastrup C, Bech-Hansen M, Bjerre LB, Carlsen B, Hagstrup M, Jensen SG, Karlsen P, Kristensen L, Lundsgaard C (2016) Fitness components of Drosophila melanogaster developed on a standard laboratory diet or a typical natural food source. Insect Sci 23:771–779
Kulamarva AG, Sosle VR, Raghavan GV (2009) Nutritional and rheological properties of sorghum. Int J Food Prop 12:55–69
Ma FZ, Lü ZC, Wang R, Wan FH (2014) Heritability and evolutionary potential in thermal tolerance traits in the invasive Mediterranean cryptic species of Bemisia tabaci (Hemiptera: Aleyrodidae). PLoS ONE 9:e103279. https://doi.org/10.1371/journal.pone.0103279
MacMillan HA, Andersen JL, Davies SA, Overgaard J (2015) The capacity to maintain ion and water homeostasis underlies interspecific variation in Drosophila cold tolerance. Sci Rep 5:18607. https://doi.org/10.1038/srep18607
Mathur S, Umakanth AV, Tonapi VA, Sharma R, Sharma MK (2017) Sweet sorghum as biofuel feedstock: recent advances and available resources. Biotechnol Biofuels 10:146
Mbande A, Tedder M, Chidawanyika F (2019) Differential life-history responses in Neolema abbreviata, a biological control agent for Tradescantia fluminensis under water and nitrogen gradients. Arthropod Plant Interact 13:57–70
Meehl GA, Tebaldi C (2004) More intense, more frequent, and longer lasting heat waves in the 21st century. Science 305:994–997
Mevi-Schütz J, Erhardt A (2003) Larval nutrition affects female nectar amino acid preference in the map butterfly (Araschnia levana). Ecology 84:2788–2794
Milton CC, Partridge L (2008) Brief carbon dioxide exposure blocks heat hardening but not cold acclimation in Drosophila melanogaster. J Insect Physiol 54:32–40
Moeng E, Mutamiswa R, Conlong DE, Assefa Y, Le Ru BP, Goftishu M, Nyamukondiwa C (2018) Diversity and distribution of lepidopteran stemborer species and their host plants in Botswana. Arthropod Plant Interact 12:733–749
Moolman J, Van den Berg J, Conlong D, Cugala D, Siebert S, Le Ru B (2014) Species diversity and distribution of lepidopteran stem borers in South Africa and Mozambique. J Appl Entomol 138:52–66
Morey AC, Venette RC, Nystrom Santacruz EC, Mosca LA, Hutchison WD (2016) Host-mediated shift in the cold tolerance of an invasive insect. Ecol Evol 6:8267–8275
Mutamiswa R, Chidawanyika F, Nyamukondiwa C (2017) Dominance of spotted stemborer Chilo partellus (Swinhoe) (Lepidoptera: Crambidae) over indigenous stemborer species in Africa's changing climates: ecological and thermal biology perspectives. Agric For Entomol 19:344–356
Mutamiswa R, Chidawanyika F, Nyamukondiwa C (2018a) Superior basal and plastic thermal responses to environmental heterogeneity in invasive exotic stemborer Chilo partellus Swinhoe over indigenous Busseola fusca (Fuller) and Sesamia calamistis Hampson. Physiol Entomol 43:108–119
Mutamiswa R, Machekano H, Chidawanyika F, Nyamukondiwa C (2018b) Thermal resilience may shape population abundance of two sympatric congeneric Cotesia species (Hymenoptera: Braconidae). PLoS ONE 13:e0191840
Mutamiswa R, Chidawanyika F, Nyamukondiwa C (2018c) Comparative assessment of the thermal tolerance of spotted stemborer, Chilo partellus Swinhoe (Lepidoptera: Crambidae) and its larval parasitoid, Cotesia sesamiae Cameron (Hymenoptera: Braconidae). Insect Sci 25:847–860
Mutamiswa R, Machekano H, Chidawanyika F, Nyamukondiwa C (2019) Life-stage related responses to combined effects of acclimation temperature and humidity on the thermal tolerance of Chilo partellus (Swinhoe) (Lepidoptera: Crambidae). J Therm Biol 79:85–94
Nyamukondiwa C, Terblanche JS (2009) Thermal tolerance in adult Mediterranean and Natal fruit flies (Ceratitis capitata and Ceratitis rosa): effects of age, gender and feeding status. J Therm Biol 34:406–414
Nyamukondiwa C, Terblanche JS (2010) Within-generation variation of critical thermal limits in adult Mediterranean and Natal fruit flies Ceratitis capitata and Ceratitis rosa: thermal history affects short-term responses to temperature. Physiol Entomol 35:255–264
Ong’amo GO, Le Ru B, Dupas S, Moyal P, Muchugu E, Calatayud PA, Silvain JF (2006) The role of wild host plants in the abundance of lepidopteran stem borers along altitude gradient in Kenya. Ann Soc Entomol Fr 42:363–370
Oyen KJ, Dillon ME (2018) Critical thermal limits of bumblebees (Bombus impatiens) are marked by stereotypical behaviors and are unchanged by acclimation, age or feeding status. J Exp Biol 221:jeb165589. https://doi.org/10.1242/jeb.165589
Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42
Piyaphongkul J, Pritchard J, Bale J (2012) Heat stress impedes development and lowers fecundity of the Brown Planthopper, Nilaparvata lugens (Sta°l). PLoS ONE 7:e47413. https://doi.org/10.1371/journal.pone.0047413
Ries L, Fletcher RJ Jr, Battin J, Sisk TD (2004) Ecological responses to habitat edges: mechanisms, models, and variability explained. Annu Rev Ecol Evol Syst 35:491–522
Scharf I, Braf H, Ifrach N, Rosenstein S, Subach A (2015) The effects of temperature and diet during development, adulthood, and mating on reproduction in the red flour beetle. PLoS ONE 10:e0136924
Schittenhelm S, Schroetter S (2014) Comparison of drought tolerance of maize, sweet sorghum and sorghum-sudangrass hybrids. J Agron Crop Sci 200:46–53
Schou MF, Loeschcke V, Kristensen TN (2015) Strong costs and benefits of winter acclimatization in Drosophila melanogaster. PLoS ONE 10:e0130307
Sinclair BJ, Coello Alvarado LE, Ferguson LV (2015) An invitation to measure insect cold tolerance: Methods, approaches, and workflow. J Therm Biol 53:180–197
Sisodia S, Singh BN (2012) Experimental evidence for nutrition regulated stress resistance in Drosophila ananassae. PLoS ONE 7:e46131
Smalley J, Blake M, Chavez SJ, DeBoer WR, Eubanks MW, Gremillion KJ, Katzenberg MA, Oyuela-Caycedo A, Pearsall D, Piperno DR, Tykot RH (2003) Sweet beginnings: stalk sugar and the domestication of maize. Curr Anthropol 44:675–703
Stathers T, Lamboll R, Mvumi BM (2013) Postharvest agriculture in changing climates: its importance to African smallholder farmers. Food Secur 5:361–392
Tsuchihashi N, Goto Y (2004) Cultivation of sweet sorghum (Sorghum bicolor (L.) Moench) and determination of its harvest time to make use as the raw material for fermentation, practiced during rainy season in dry land of Indonesia. Plant Prod Sci 7:442–448
Valtonen TM, Kangassalo K, Pölkki M, Rantala MJ (2012) Transgenerational effects of parental larval diet on offspring development time, adult body size and pathogen resistance in Drosophila melanogaster. PLoS ONE 7:e31611
Weldon CW, Terblanche JS, Chown SL (2011) Time-course for attainment and reversal of acclimation to constant temperature in two Ceratitis species. J Therm Biol 36:479–485
Yerushalmi GY, Misyura L, Donini A, MacMillan HA (2016) Chronic dietary salt stress mitigates hyperkalemia and facilitates chill coma recovery in Drosophila melanogaster. J Insect Physiol 95:89–97
Zilic S, Milasinovic M, Terzic D, Barac M, Ignjatovic-Micic D (2011) Grain characteristics and composition of maize specialty hybrids. Span J Agric Res 9:230–241
Acknowledgements
The authors appreciate valuable support from University of the Free State to RM and FC, Botswana International University of Science and Technology (BIUST) to RM, HM and CN. Our gratitude also goes to several anonymous referees for the critical and constructive comments on an earlier version of this manuscript.
Funding
The study was funded through the University of the Free State (UFS) Research Office Grant and postdoctoral fellowship to RM. Funding was provided by Universiteit van die Vrystaat (Grant No. 1-119-B53568).
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Mutamiswa, R., Machekano, H., Nyamukondiwa, C. et al. Host plant-related responses on the thermal fitness of Chilo partellus (Swinhoe) (Lepidoptera: Crambidae). Arthropod-Plant Interactions 14, 463–471 (2020). https://doi.org/10.1007/s11829-020-09762-9
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DOI: https://doi.org/10.1007/s11829-020-09762-9