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The influence of temperature, photoperiod, and diet on development and reproduction in the four-spot lady beetle Harmonia quadripunctata (Pontoppidan) (Coleoptera, Coccinellidae)

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Abstract

This is the first report on the effects of temperature (from 17 to 30°C), photoperiod (from 10 to 16 h of light), and diet (the wheat aphid Schizaphis graminum and the green peach aphid Myzus persicae) on preimaginal developmental rates, adult body mass, preoviposition period, and female fecundity of the predatory lady beetle Harmonia quadripunctata (Pontoppidan) under the laboratory conditions. A constant temperature of 30°C was lethal to the embryos. Judging from the data obtained at 17, 20, and 25°C, the lower temperature threshold for total egg-to-adult development equaled 12.0°C and the respective sum of effective temperatures was 274 degree-days. Preimaginal development was somewhat faster under short-day conditions, the threshold for this quantitative photoperiodic response being approximately 14 h at the rearing temperatures of 20 and 25°C. At a temperature of 25°C, the mean body mass of newly emerged adults was greater for those individuals that during the larval stage had been fed on the green peach aphid (16.4 mg in males and 18.4 mg in females) than in those fed with the wheat aphid (13.8 mg in males and 15.3 mg in females). The preoviposition period (measured from adult emergence to the first egg laid) also depended on temperature and had a lower threshold of 13.4°C and a sum of effective temperatures of 152 degree-days. Maximum fecundity was observed at 25°C and 16-h day length; under these conditions, the oviposition period lasted over 100 d, and the average lifetime fecundity was about 800 eggs per female. Under short-day conditions, females of H. quadripunctata entered reproductive diapause. The photoperiodic threshold for this qualitative response at the temperatures of 20 and 25°C was about 14 h when fed on the peach aphid and 15 h when fed on the wheat aphid. Relatively small body size, low fecundity, and a strong photoperiodic response that hinders rapid adaptation to novel climates probably explain the fact that H. quadripunctata, in contrast to H. axyridis, has not become an aggressive invader.

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References

  1. Abrams, P.A., Leimar, O., Nylin, S., and Wiklund, C., “The Effect of Flexible Growth Rates on Optimal Sizes and Development Times in a Seasonal Environment,” The American Naturalist 147 (3), 381–395 (1996).

    Article  Google Scholar 

  2. Alhmedi, A., Haubruge, É., and Francis, F., “Intraguild Interactions Implicating Invasive Species: Harmonia axyridis as a Model Species,” Biotechnology, Agronomy, Society and Environment 14 (1), 187–201 (2010).

    Google Scholar 

  3. Aslan, M.M. and Uygun, N., “The Aphidophagous Coccinellid (Coleoptera: Coccinellidae) Species in Kahramanmaraş, Turkey,” Turkish Journal of Zoology 29 (1), 1–8 (2005).

    Google Scholar 

  4. Atkinson, D., “Temperature and Organism Size: a Biological Law for Ectotherms?” Advances in Ecological Research 25, 1–58 (1994).

    Article  Google Scholar 

  5. Barševskis, A. and Lazdāns, D., “Catalogue of Ladybirds (Coleoptera: Coccinellidae) of Latvia,” Acta Biologica Universitatis Daugavpiliensis 10 (2), 89–100 (2010).

    Google Scholar 

  6. Belyakova, N.A. and Pazyuk, I.M., “Selection of Entomophages for Greenhouses,” Zashchita i Karantin Rastenii 7, 28–30 (2007).

    Google Scholar 

  7. Belyakova, N.A. and Reznik, S.Ya., “First Record of the Harlequin Ladybird, Harmonia axyridis, in the Caucasus,” European Journal of Entomology 110 (4), 699–702 (2013).

    Article  Google Scholar 

  8. Benelli, M., Simon, R., Francati, S., Marchetti, E., and Dindo, M.L., “Effect of Two Temperatures on Biological Traits and Susceptibility to a Pyrethroid Insecticide in an Exotic and Native Coccinellid Species,” Bulletin of Insectology 68 (1), 23–29 (2015).

    Google Scholar 

  9. Berkvens, N., Bonte, J., Berkvens, D., Tirry, L., and De Clercq, P., “Influence of Diet and Photoperiod on Development and Reproduction of European Populations of Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae),” BioControl 53 (1), 211–221 (2008).

    Article  Google Scholar 

  10. Brown, P.M.J., Roy, H.E., Rothery, P., Roy, D.B., Ware, R.L., and Majerus, M.E., “Harmonia axyridis in Great Britain: Analysis of the Spread and Distribution of a Non-native Coccinellid,” BioControl 53 (1), 55–67 (2008).

    Article  Google Scholar 

  11. Brown, P.M.J., Thomas, C.E., Lombaert, E., Jeffries, D.L., Estoup, A., and Handley, L.-J.L., “The Global Spread of Harmonia axyridis (Coleoptera: Coccinellidae): Distribution, Dispersal and Routes of Invasion,” BioControl 56 (4), 623–641 (2011).

    Article  Google Scholar 

  12. Chen, J., Qin, Q.J., Liu, S., and He, Y.Z., “Effect of Six Diets on Development and Fecundity of Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae),” African Entomology 20 (1), 85–90.

  13. Danilevskii, A.S., Photoperiodism and Seasonal Development of Insects (Oliver & Boyd, Edinburgh, 1965). 283 p.

    Google Scholar 

  14. de Oliveira Ramos, T., dos Santos-Cividanes, T.M., Cividanes, F.J., and dos Santos, L.D.C., “Harmonia axyridis Pallas (Coleoptera: Coccinellidae): Biological Aspects and Thermal Requirements,” Advances in Entomology 2 (1), 42–46 (2014).

    Article  Google Scholar 

  15. Hemptinne, J.L., Magro, A., Evans, E.W., and Dixon, A.F.G., “Body Size and the Rate of Spread of Invasive Ladybird Beetles in North America,” Biological Invasions 14 (3), 595–605 (2012).

    Article  Google Scholar 

  16. Hodek, I., “Diapause/Dormancy,” in Ecology and Behaviour of the Ladybird Beetles (Coccinellidae), Ed. by Hodek, I., van Emden, H.F., and Honěk, A. (Wiley-Blackwell, Chichester, 2012), pp. 275–342.

    Chapter  Google Scholar 

  17. Isayev, A.Yu. and Yegorov, L.V. “On the Fauna of Some Groups of the Superfamily Cucujoidea (Coleoptera) of the Forest-Steppe of the Lower Volga region. Communication 1. Families Erotylidae, Endomychidae, and Coccinellidae,” Kavkazskii Entomol. Byull. 2 (1), 65–72 (2006).

    Google Scholar 

  18. Karaca, G., Karaca, I., Yardimci, N., Demirözer, O., Aslan, B., and Kiliç, H.Ç., “Investigations on Pests, Diseases and Present Early Warning System of Apple Orchards in Isparta, Turkey,” African Journal of Biotechnology 9 (6), 834–841 (2010).

    Google Scholar 

  19. Kawauchi, S., “Effects of Photoperiod on the Induction of Diapause, the Live Weight of Emerging Adult, and the Duration of Development of Three Species of Aphidophagous Coccinellids (Coleoptera, Coccinellidae),” Kontyû 53 (3), 536–546 (1985).

    Google Scholar 

  20. Kenis, M., Roy, H.E., Zindel, R., and Majerus, M.E., “Current and Potential Management Strategies Against Harmonia axyridis,” BioControl 53 (1), 235–252 (2008).

    Article  CAS  Google Scholar 

  21. Kingsolver, J.G. and Huey, R.B., “Size, Temperature, and Fitness: Three Rules,” Evolutionary Ecology Research, 10 (2), 251–268 (2008).

    Google Scholar 

  22. Koch, R.L. and Galvan, T.L., “Bad Side of a Good Beetle: the North American Experience with Harmonia axyridis,” BioControl 53 (1), 23–35 (2008).

    Article  Google Scholar 

  23. Krafsur, E.S., Obrycki, J.J., and Harwood, J.D., “Comparative Genetic Studies of Native and Introduced Coccinellidae in North America,” European Journal of Entomology 102 (3), 469–474 (2005).

    Article  Google Scholar 

  24. Kutcherov, D.A., Lopatina, E.B., and Kipyatkov, V.E., “Photoperiod Modifies Thermal Reaction Norms for Growth and Development in the Red Poplar Leaf Beetle Chrysomela populi (Coleoptera: Chrysomelidae),” Journal of Insect Physiology 57 (7), 892–898 (2011).

    Article  CAS  PubMed  Google Scholar 

  25. Kuznetsov, V.N., “The Fauna and Distribution of Coccinellids (Coleoptera: Coccinellidae) in the Russian Far East,” Trudy Ross. Entomol. O-va 77, 192–199 (2006).

    Google Scholar 

  26. Labrie, G., Lucas, E., and Coderre, D., “Can Developmental and Behavioral Characteristics of the Multicolored Asian Lady Beetle Harmonia axyridis Explain Its Invasive Success?” Biological Invasions 8 (4), 743–754 (2006).

    Article  Google Scholar 

  27. Lombaert, E., Estoup, A., Facon, B., Joubard, B., Grégoire, J.C., Jannin, A., Blin, A., and Guillemaud, T., “Rapid Increase in Dispersal during Range Expansion in the Invasive Ladybird Harmonia axyridis,” Journal of Evolutionary Biology 27 (3), 508–517 (2014).

    Article  CAS  PubMed  Google Scholar 

  28. Lombaert, E., Guillemaud, T., Cornuet, J.M., Malausa, T., Facon, B., and Estoup, A., “Bridgehead Effect in the Worldwide Invasion of the Biocontrol Harlequin Ladybird,” PLoS ONE 5 (3), e9743 (2010).

    Article  Google Scholar 

  29. Lopatina, E.B., Balashov, S.V., and Kipyatkov, V.E., “First Demonstration of the Influence of Photoperiod on the Thermal Requirements for Development in Insects and in Particular the Linden-Bug, Pyrrhocoris apterus (Heteroptera: Pyrrhocoridae),” European Journal of Entomology, 104 (1), 23–31 (2007).

    Article  Google Scholar 

  30. Nedvěd, O. and Honěk, A., “Life History and Development,” in Ecology and Behaviour of the Ladybird Beetles (Coccinellidae), Ed. by Hodek, I., van Emden, H.F., and Honěk, A. (Wiley-Blackwell, Chichester, 2012), pp. 54–109.

    Chapter  Google Scholar 

  31. Nylin, S. and Gotthard, K., “Plasticity in Life-History Traits,” Annual Review of Entomology 43, 63–83 (1998).

    Article  CAS  PubMed  Google Scholar 

  32. Obrycki, J.J., and Kring, T.J., “Predaceous Coccinellidae in Biological Control,” Annual Review of Entomology 43, 295–321 (1998).

    Article  CAS  PubMed  Google Scholar 

  33. Ongagna, P. and Iperti, G., “Influence of Temperature and Photoperiod on Harmonia axyridis Pall. (Col., Coccinellidae): Rapidly Obtaining Fecund Adults or in Dormancy,” Journal of Applied Entomology 117 (3), 314–317 (1994).

    Article  Google Scholar 

  34. Orlova-Bienkowskaja, M.J., “A Dangerous Invasive Lady Beetle Species Harmonia axyridis (Pallas, 1973) (Coleoptera, Coccinellidae) in European Russia,” Rossiiskii Zh. Biol. Invazii 1, 75–81 (2013).

    Google Scholar 

  35. Radwan, Z. and Lövei, G.L., “Distribution and Bionomics of Ladybird Beetles (Col., Coccinellidae) Living in an Apple Orchard near Budapest, Hungary,” Journal of Applied Entomology 94 (1–5), 169–175 (1982).

    Google Scholar 

  36. Reznik, S.Ya., Dolgovskaya, M.Y., and Ovchinnikov, A.N., “Effect of Photoperiod on Adult Size and Weight in Harmonia axyridis (Coleoptera: Coccinellidae),” European Journal of Entomology 112 (4), 642–647 (2015a).

    Google Scholar 

  37. Reznik, S.Ya. and Vaghina, N.P., “Dynamics of Fat Content during Induction and Termination of “Trophic Diapause” in Harmonia sedecimnotata Fabr. Females (Coleoptera, Coccinellidae),” Entomol. Obozr. 85 (1), 3–12 (2006) [Entomol. Rev. 86 (2), 125–132 (2006)].

    Google Scholar 

  38. Reznik, S.Ya. and Vaghina, N.P., “Effects of Photoperiod and Diet on Diapause Tendency, Maturation and Fecundity in Harmonia axyridis (Coleoptera: Coccinellidae),” Journal of Applied Entomology 137 (6), 452–461 (2013).

    Article  Google Scholar 

  39. Reznik, S.Ya. and Vaghina, N.P., “Photoperiodic Control of Development and Reproduction in Harmonia axyridis (Coleoptera: Coccinellidae),” European Journal of Entomology 108 (3), 385–390 (2011).

    Article  Google Scholar 

  40. Reznik, S.Ya., Dolgovskaya, M.Y., Ovchinnikov, A.N., and Belyakova, N.A., “Weak Photoperiodic Response Facilitates the Biological Invasion of the Harlequin Ladybird Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae),” Journal of Applied Entomology 139 (4), 241–249 (2015b).

    Article  Google Scholar 

  41. Reznik, S.Ya., Ovchinnikov, A.N., Dolgovskaya, M.Yu., and Belyakova, N.A., “Interspecific Variation in Photoperiodic Effect on the Rate of Preimaginal Development in Harmonia axyridis (Pallas) (Coleoptera, Coccinellidae),” Entomol. Obozr. 94 (1), 35–52 (2015c) [Entomol. Rev. 95 (1), 15–27 (2015)].

    Google Scholar 

  42. Roy, H.E. and Wajnberg, E., “From Biological Control to Invasion: the Ladybird Harmonia axyridis as a Model Species,” BioControl 53 (1), 1–4 (2008).

    Article  Google Scholar 

  43. Saulich, A.Kh. and Volkovitch, T.A., Ecology of Insect Photoperiodism (St. Petersburg Univ., St Petersburg, 2004) [in Russian].

    Google Scholar 

  44. Saunders, D.S., Steel, C.G.H., Vafopoulou, X., and Lewis, R.D., Insect Clocks (Elsevier, Amsterdam, 2002).

    Google Scholar 

  45. Semyanov, V.P., “Biology of Coccinellids (Coleoptera, Coccinellidae) from Southeast Asia: II. Harmonia sedecimnotata (F.),” Entomol. Obozr. 79 (1), 3–9 (2000) [Entomol. Rev. 80 (5), 491–496 (2000)].

    Google Scholar 

  46. Semyanov, V.P. and Vaghina, N.P., “Effect of the Trophic Diapause on the Fecundity and Longevity of a Tropical Coccinellid, Harmonia sedecimnotata (Fabr.) (Coleoptera, Coccinellidae),” Entomol. Obozr. 82 (1), 3–5 (2003) [Entomol. Rev. 83 (8), 915–916 (2003)].

    Google Scholar 

  47. Sloggett, J.J., “Harmonia axyridis Invasions: Deducing Evolutionary Causes and Consequences,” Entomological Science, 15 (3), 261–273 (2012).

    Article  Google Scholar 

  48. Smaili, M.C., Blenzar, A., and Fursch, H., “First Record of New Species and Phenotypes of Ladybird (Coleoptera: Coccinellidae) in Citrus Orchards in Morocco,” Faunistic Entomology 62 (3), 103–107 (2010).

    Google Scholar 

  49. Su, N.Y., “How to Become a Successful Invader,” Florida Entomologist 96 (3), 765–769 (2013).

    Article  Google Scholar 

  50. Tauber, M.J., Tauber, C.A., and Masaki, S., Seasonal Adaptations of Insects (Oxford Univ. Press, New York, 1986).

    Google Scholar 

  51. Tyshchenko, V.P., “Physiology of Insect Photoperiodism,” Trudy Vses. Entomol. O-va 59, 1–159 (1977).

    Google Scholar 

  52. Ukrainsky, A.S. and Orlova-Bienkowskaja, M.J., “Expansion of Harmonia axyridis Pallas (Coleoptera: Coccinellidae) to European Russia and Adjacent Regions,” Biological Invasions 16 (5), 1003–1008 (2014).

    Article  Google Scholar 

  53. Ungerová, D., Kalushkov, P., and Nedvěd, O., “Suitability of Diverse Prey Species for Development of Harmonia axyridis and the Effect of Container Size,” International Organization for Biological and Integrated Control / West Palaearctic Regional Section Bulletin 58, 165–174.

  54. Whitney, K.D. and Gabler, C.A., “Rapid Evolution in Introduced Species, ‘Invasive Traits’ and Recipient Communities: Challenges for Predicting Invasive Potential,” Diversity and Distributions 14 (4), 569–580 (2008).

    Article  Google Scholar 

  55. Yu, G., Montgomery, M.E., and Yao, D., “Lady Beetles (Coleoptera: Coccinellidae) from Chinese Hemlocks Infested with the Hemlock Woolly Adelgid, Adelges tsugae Annand (Homoptera: Adelgidae),” The Coleopterists Bulletin 54 (2), 154–199 (2000).

    Article  Google Scholar 

  56. Zaslavskii, V.A., Insect Development. Photoperiodic and Temperature Control (Springer-Verlag, Berlin–Heidelberg, 1988). 187 p.

    Google Scholar 

  57. Zaslavskii, V.A., Semyanov, V.P., and Vaghina, N.P., “Food as a Cue Factor Controlling Adult Diapause in the Lady Beetle Harmonia sedecimnotata (Coleoptera, Coccinellidae),” Zool. Zh. 77 (12), 1383–1388 (1998) [Entomol. Rev. 78 (6), 774–779 (1998)].

    Google Scholar 

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Authors and Affiliations

  1. All-Russia Institute of Plant Protection, Russian Academy of Sciences, Pushkin, St. Petersburg, 196608, Russia

    N. A. Belyakova & I. M. Pazyuk

  2. Zoological Institute, Russian Academy of Sciences, St. Petersburg, 196034, Russia

    A. N. Ovchinnikov & S. Ya. Reznik

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  1. N. A. Belyakova
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  2. I. M. Pazyuk
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  3. A. N. Ovchinnikov
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  4. S. Ya. Reznik
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Original Russian Text © N.A. Belyakova, I.M. Pazyuk, A.N. Ovchinnikov, S.Ya. Reznik, 2016, published in Entomologicheskoe Obozrenie, 2016, Vol. 95, No. 1, pp. 3–18.

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Belyakova, N.A., Pazyuk, I.M., Ovchinnikov, A.N. et al. The influence of temperature, photoperiod, and diet on development and reproduction in the four-spot lady beetle Harmonia quadripunctata (Pontoppidan) (Coleoptera, Coccinellidae). Entmol. Rev. 96, 1–11 (2016). https://doi.org/10.1134/S0013873816010012

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