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Effects of long-term cold storage on maternal and progeny fitness of laboratory-reared Harmonia axyridis adults

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Abstract

Long-term cold storage is a commonly used technique in mass rearing of natural enemies, but it brings a diversity of negative effects, especially for the laboratory-reared biocontrol agents. Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) is an important natural enemy of aphids. In this study, the laboratory-reared H. axyridis adults were stored at 6 °C for up to 120 days, and the accompanying effects on maternal and progeny fitness were evaluated and compared with the non-stored beetles (control). Before storage, the newly emerged adults were fed with β-carotene-amended artificial diet for ten days and then acclimated at 15 °C for two days. The mass and trehalose content of the beetle were inversely proportional to the storage duration. The survival rates of the cold-stored beetles decreased as the storage duration increased. However, the survival rates were still above 50% after 120 days in storage (DIS-120). The DIS-120 beetles had a similar fecundity but a significantly longer pre-oviposition period than the control beetles. The egg hatch rates of the DIS-120 beetles were above 60% during the first six days and then dramatically decreased to near zero after day 13. However, the egg viability of the fertility-reduced beetles could be partially restored to approximately 40% by re-mating with non-stored partners. The F1 offspring of the DIS-120 beetles also had a sustained high fecundity but significantly lower egg hatch rate than the F1 offspring of the control beetles. This study demonstrated that the laboratory-reared H. axyridis could be cold stored for approximately 120 days, and their reproductive capability was still acceptable.

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Data availability

The datasets generated and analyzed during the current study are available in the fgshare repository. https://doi.org/10.6084/m9.figshare.13663613

Code availability

Not applicable.

References

  • Awad M, Kalushkov P, Nedvedova T, Nedved O (2013) Fecundity and fertility of ladybird beetle Harmonia axyridis after prolonged cold storage. BioControl 58:657–666

    Article  Google Scholar 

  • Benelli M, Tóth F, Dindo ML (2018) Low-temperature storage of Exorista larvarum puparia as a tool for assisting parasitoid production. Ent Exp Appl 166:914–924

    CAS  Google Scholar 

  • Berkvens N, Bale JS, Berkvens D, Tirry L, De Clercq P (2010) Cold tolerance of the harlequin ladybird Harmonia axyridis in Europe. J Insect Physiol 56:438–444

    Article  CAS  PubMed  Google Scholar 

  • Brown PMJ, Thomas CE, Lombaert E, Jeffries DL, Estoup A, Handley LJL (2011) The global spread of Harmonia axyridis (Coleoptera: Coccinellidae): distribution, dispersal and routes of invasion. BioControl 56:623–641

    Article  Google Scholar 

  • Bueno VHP, Carvalho LM, van Lenteren JC (2014) Performance of Orius insidiosus after storage, exposure to dispersal material, handling and shipment processes. Bull Insectol 67:175–183

    Google Scholar 

  • Camacho-Cervantes M, Ortega-Iturriaga A, Del-Val E (2017) From effective biocontrol agent to successful invader: the harlequin ladybird (Harmonia axyridis) as an example of good ideas that could go wrong. Peerj 5:e3296

    Article  PubMed  PubMed Central  Google Scholar 

  • Chang YF, Tauber MJ, Tauber CA (1996) Reproduction and quality of F1 offspring in Chrysoperla carnea: differential influence of quiescence, artificially-induced diapause, and natural diapause. J Insect Physiol 42:521–528

    Article  CAS  Google Scholar 

  • Chen WL, Leopold RA, Harris MO (2008a) Cold storage effects on maternal and progeny quality of Gonatocerus ashmeadi Girault (Hymenoptera: Mymaridae). Biol Control 46:122–132

    Article  Google Scholar 

  • Chen WL, Leopold RA, Boetel MA (2008b) Cold storage of adult Gonatocerus ashmeadi (Hymenoptera: Mymaridae) and effects on maternal and progeny fitness. J Econ Entomol 101:1760–1770

    Article  PubMed  Google Scholar 

  • Davis JR, Kirkland RL (1982) Physiological and environmental factors related to the dispersal flight of the convergent lady beetle, Hippodamia convergens (Guerin-Meneville). J Kansas Entomol Soc 55:187–196

    Google Scholar 

  • Deng DA (1982) Experiments on feeding with artificial diets and cold storage of Harmonia axyridis Pallas. Insect Knowl 19:11–12

    Google Scholar 

  • Denlinger DL, Lee RE (1998) Physiology of cold sensitivity. In: Hallman GJ, Denlinger DL (eds) Temperature sensitivity in insects and application in integrated pest management. Westview Press, Boulder, pp 55–96

    Google Scholar 

  • Du WM, Sun GZ, Zang LS, Wang XM, Ruan CC, Liu XJ (2016) Effect of long-term cold storage on fecundity of pre-wintering Harmonia axyridis (Pallas) and the fitness of its progeny. J Environ Entomol 38:286–292

    Google Scholar 

  • Elnagdy S, Majerus MEN, Handley LJL (2011) The value of an egg: resource reallocation in ladybirds (Coleoptera: Coccinellidae) infected with male-killing bacteria. J Evol Biol 24:2164–2172

    Article  CAS  PubMed  Google Scholar 

  • Elnagdy S, Majerus MEN, Gardener M, Lawson Handley LJ (2013) The direct effects of male killer infection on fitness of ladybird hosts (Coleoptera: Coccinellidae). J Evol Biol 26:1816–1825

    Article  CAS  PubMed  Google Scholar 

  • Etzel L, Legner E (1999) Culture and colonisation. Academic Press, London

    Google Scholar 

  • Flanders SE (1938) The effect of cold storage on reproduction of parasitic Hymenoptera. J Econ Entomol 31:633–634

    Google Scholar 

  • Ghazy NA, Ohyama K, Amano H, Suzuki T (2014) Cold storage of the predatory mite Neoseiulus californicus is improved by pre-storage feeding on the diapausing spider mite Tetranychus urticae. Biocontrol 59:185–194

  • Hackermann J, Rott AS, Tschudi-Rein K, Dorn S (2008) Cold stored ectoparasitoid of Cydia fruit moths released under different temperature regimes. BioControl 53:857–867

    Article  Google Scholar 

  • Hance T, van Baaren J, Vernon P, Boivin G (2007) Impact of extreme temperatures on parasitoids in a climate change perspective. Annu Rev Entomol 52:107–126

    Article  CAS  PubMed  Google Scholar 

  • Hanna AD (1935) Fertility and toleration of low temperature in Euchalcidia carybori Hanna (Hymenoptera: Chalcidinae). Bull Entomol Res 26:315–322

    Article  Google Scholar 

  • Heath JJ, Cipollini DF, Stireman JO III (2013) The role of carotenoids and their derivatives in mediating interactions between insects and their environment. Arthropod-Plant Interact 7:1–20

    Article  Google Scholar 

  • Hurst GD, Jiggins FM (2000) Male-killing bacteria in insects: mechanisms, incidence, and implications. Emerg Infect Dis 6:329–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koch RL (2003) The multicolored Asian lady beetle, Harmonia axyridis: a review of its biology, uses in biological control, and non-target impacts. J Insect Sci 3:32

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lalouette L, Williams CM, Hervant F, Sinclair BJ, Renault D (2011) Metabolic rate and oxidative stress in insects exposed to low temperature thermal fluctuations. Comp Biochem Phys A 158:229–234

    Article  CAS  Google Scholar 

  • Lombaert E, Malausa T, Devred R, Estoup A (2008) Phenotypic variation in invasive and biocontrol populations of the harlequin ladybird, Harmonia axyridis. BioControl 53:89–102

    Article  Google Scholar 

  • R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.r-project.org/

  • Rathee M, Ram P (2014) Effect of cold storage of Aenasius bambawalei Hayat (Hymenoptera: Encyrtidae) during pupal stage on its key biological characteristics. J Bio Control 28:11–17

    Google Scholar 

  • Rathee M, Ram P (2018) Impact of cold storage on the performance of entomophagous insects: an overview. Phytoparasitica 46:421–449

    Article  Google Scholar 

  • Reznik SY, Vaghina NP (2013) Effects of photoperiod and diet on diapause tendency, maturation and fecundity in Harmonia axyridis (Coleoptera: Coccinellidae). J Appl Entomol 137:452–461

    Article  Google Scholar 

  • Reznik SY, Ovchinnikov AN, Dolgovskaya MY, Belyakova NA (2015) Interspecific variation in photoperiodic effect on the rate of preimaginal development in Harmonia axyridis (Pallas) (Coleoptera, Coccinellidae). Entmol Rev 95:15–27

    Article  Google Scholar 

  • Rojas RR, Leopold RA (1996) Chilling injury in the housefly: evidence for the role of oxidative stress between pupariation and emergence. Cryobiology 33:447–458

    Article  Google Scholar 

  • Ruan CC, Du WM, Wang XM, Zhang JJ, Zang LS (2012) Effect of long-term cold storage on the fitness of pre-wintering Harmonia axyridis (Pallas). BioControl 57:95–102

    Article  Google Scholar 

  • Sakaki S, Jalali MA, Kamali H, Nedved O (2019) Effect of low-temperature storage on the life history parameters and voracity of Hippodamia variegata (Coleoptera: Coccinellidae). Eur J Entomol 116:10–15

    Article  Google Scholar 

  • Sano H (2002) DNA methylation and Lamarckian inheritance. Proc Jpn Acad Sci 78B:293–298

    Article  CAS  Google Scholar 

  • Shi Z, Liu X, Xu Q, Qin Z, Wang S, Zhang F, Wang S, Tang B (2016) Two novel soluble trehalase genes cloned from Harmonia axyridis and regulation of the enzyme in a rapid changing temperature. Comp Biochem Phys B 198:10–18

    Article  CAS  Google Scholar 

  • Sun YX, Hao YN, Liu CZ, Wang SS (2019) Artificial diet is fruitful pre-storage nutrition for long-term cold storage of laboratory-reared Harmonia axyridis (Pallas) adults. Biol Control 139:104075

    Article  Google Scholar 

  • Sun YX, Hao YN, Liu CZ, Zhou JJ, Wang SS (2021) Obstructs-equipped apparatus reduces cannibalism and improves larval survival of the coccinellid, Harmonia axyridis (Coleoptera: Coccinellidae). Egypt J Biol Pest Co 31:80

    Article  Google Scholar 

  • Takahashi S, Kinoshita M, Adachi S, Seko T, Tokuda M (2019) Overwintering ability of a flightless strain of the ladybird beetle Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). BioControl 64:391–399

    Article  CAS  Google Scholar 

  • Tang B, Liu XJ, Shi ZK, Shen QD, Xu YX, Wang S, Zhang F, Wang SG (2017) Transcriptome analysis and identification of induced genes in the response of Harmonia axyridis to cold hardiness. Comp Biochem Phys D 22:78–89

    CAS  Google Scholar 

  • Tauber MJ, Tauber CA, Masaki S (1984) Adaptations to hazardous seasonal conditions: dormancy, migration and polyphenism. In: Huffaker CB (ed) Ecological entomology. Wiley, New York, pp 149–184

    Google Scholar 

  • Umina PA, Edwards O, Carson P, van Rooyen A, Anderson A (2014) High levels of resistance to carbamate and pyrethroid chemicals widespread in Australian Myzus persicae (Hemiptera: Aphididae) populations. J Econ Entomol 107:1626–1638

    Article  PubMed  Google Scholar 

  • van Handel E (1969) Metabolism of hexoses in the intact mosquito: exclusion of glucose and trehalose as intermediates. Comp Biochem Physiol 29:413–421

    Article  PubMed  Google Scholar 

  • Watanabe M (2002) Cold tolerance and myo-inositol accumulation in overwintering adults of a lady beetle, Harmonia axyridis (Coleoptera: Coccinellidae). Eur J Entomol 99:5–10

    Article  CAS  Google Scholar 

  • Wu M, Xu Q, Liu Y, Shi X, Shen Q, Yang M, Wang S, Tang B (2016) The super cooling point change of Harmonia axyridis under low temperature stress and its cold-resistance genes’ expression analysis. Sci Agric Sin 49:677–685

    CAS  Google Scholar 

  • Wu MY, Ying YY, Zhang SS, Li XG, Yan WH, Yao YC, Shah S, Wu G, Yang FL (2020) Effects of diallyl trisulfide, an active substance from garlic essential oil, on energy metabolism in male moth Sitotroga cerealella (Olivier). Insects 11:270

    Article  PubMed Central  Google Scholar 

  • Zeng B, Wang S, Li Y, Xiao Z, Zhou M, Wang S, Zhang D (2020) Effect of long-term cold storage on trehalose metabolism of pre-wintering Harmonia axyridis adults and changes in morphological diversity before and after wintering. PLoS ONE 15(3):e0230435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang T, Zhang G, Zhang L, Chen H, Wang M, Liu C, Mao J (2019) Effects of cold storage on quality of Chrysopa pallens and recovery of fecundity by insulin. Sci Rep 9:5311

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgements

We are grateful for the assistance of all staff and students in the Biocontrol Engineering Laboratory of Crop Diseases and Pests of Gansu Province, College of Plant Protection, Gansu Agricultural University, Lanzhou, China. Funding of this research was partially supported by the following Grants: the National Natural Science Foundation of China (31960561), the Funds for Fuxi Young Scientific Talents of Gansu Agricultural University (Gaufx-03Y05), the Youth Natural Science Foundation of Gansu Province (20JR5RA006), and the Program of Introducing Talents to Chinese Universities (111 Program no. D20023). The paper has benefitted greatly from the comments of editor and anonymous reviewers.

Funding

We would like to thank the funding from the National Natural Science Foundation of China (31960561) to YXS, the Funds for Fuxi Young Scientific Talents of Gansu Agricultural University (Gaufx-03Y05) to YXS, the Youth Natural Science Foundation of Gansu Province (20JR5RA006) to YXS, and the Program of Introducing Talents to Chinese Universities (111 Program no. D20023) to JJZ.

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YXS and CZL designed the research; YXS, YNH, and SSW conducted experiments and analyzed data. YXS, JJZ and YNH wrote the paper. JJZ made critical revisions and proofreading. All authors read and approved the manuscript.

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Correspondence to Yuan-Xing Sun.

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The following insects used in this study commonly occurred in the agricultural field, e.g. Harmonia axyridis, Aphis craccivora, A. pisum and Myzus persicae. The pork liver component in artificial diet was purchased from a market in China, which is a well-received food for many people.

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Handling Editor: Eric Riddick.

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Sun, YX., Hao, YN., Zhou, JJ. et al. Effects of long-term cold storage on maternal and progeny fitness of laboratory-reared Harmonia axyridis adults. BioControl 67, 395–405 (2022). https://doi.org/10.1007/s10526-022-10144-8

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