Effectiveness of ladybirds as biological control agents: Patterns and processes

Efficacité des coccinelles comme agents de lutte biologique

Abstract

Aphidophagous species of ladybirds have generally proved ineffective biocontrol agents, whereas many coccidophagous species have proved very effective, especiallyRodolia cardinalis (Caltagirone & Doutt, 1989). Two hypotheses have been proposed to account for this pattern: the optimum food utilization/satiation hypothesis (Mills, 1982) and the generation time ratio hypothesis (Kindlmann & Dixon, 1996). In this paper the extensive literature on ladybirds is used to test these hypotheses.

Résumé

Chez les coccinelles, les espèces aphidiphages se sont montrées généralement peu efficaces comme agents de lutte biologique, à l’inverse de nombreuses espèces coccidiphages qui se sont révélées très efficaces, telleRodolia cardinalis (Caltagirone & Doutt, 1989). Deux hypothèses ont été proposées pour expliquer ce phénomène : l’hypothèse de l’utilisation optimale de la proie/ satiété (Mills, 1982) et l’hypothèse du rapport des durées de développement des générations (Kindlmann & Dixon, 1996). Dans cette étude, la vaste littérature existant sur les coccinelles est utilisée pour tester ces hypothèses.

This is a preview of subscription content, log in to check access.

References

  1. Agarwala, B. K. &Bhattacharya, S. — 1994. Anholocycly in tropical aphids: population trends and influence of temperature on development, reproduction and survival of three aphid species (Homoptera: Aphidoidea). —Phytophaga, 6, 17–27.

    Google Scholar 

  2. Ball, J. C. — 1980. Development and fecundity of the white peach scale at two constant temperatures. —Fla Entomol., 63, 188–194.

    Article  Google Scholar 

  3. Bodenheimer, F. S. — 1932.Icerya purchasi Mask. undNovius cardinalis Muls. Eine Bevölkerungswissenschaftenliche Studie über die Grundlagen der biologischen Bekämpfung. —Z. angew. Entomol., 19, 514–543.

    Google Scholar 

  4. Booth, R. G., Cross, A. E., Fowler, S. V. &Shaw, R. H. — 1995. The biology and taxonomy ofHyperaspis pantherina (Coleoptera: Coccinellidae) and the classical biological control of its prey.Orthezia insignis (Homoptera: Ortheziidae). —Bull. Entomol. Res., 85, 307–314.

    Google Scholar 

  5. Caltagirone, L. E. &Doutt, R. L. — 1989. The history of the vedalia beetle importation to California and its impact on the development of biological control. —Annu. Rev. Entomol., 34, 1–16.

    Article  Google Scholar 

  6. Campbell, C. D. &Hutchinson, W. D. — 1995. Rearing methods and demographic statistics for a subterranean morph of the sugarbeet root aphid (Homoptera: Aphididae). —Can. Entomol., 127, 65–77.

    Article  Google Scholar 

  7. Carroll, D. P. &Hoyt, S. C. — 1986. Developmental rate, weight and ovarian parameters of apple aphids,Aphis pomi (Homoptera: Aphididae), reared at one or two constant temperatures, with evidence of residual effects. —Environ. Entomol., 15, 607–613.

    Google Scholar 

  8. Chazeau, J. — 1981. Données sur la biologie deColeophora quadrivittata [Col.: Coccinellidae], prédateur deCoccus viridis [Hom.: Coccidae] en Nouvelle-Calédonie. —Entomophaga, 26, 301–312.

    Article  Google Scholar 

  9. Clausen, C. P. — 1940. Entomophagous Insects. —McGraw, New York, 688 pp.

    Google Scholar 

  10. Cressman, A. W. — 1935. Biology of the camphor scale and a method for predicting the time of appearance of stages in the field. —J. Agric. Res., 50, 267–283.

    Google Scholar 

  11. Dixon, A. F. G. — 1959. An experimental study of the searching behaviour of the predatory coccinellid beetleAdalia decempunctata (L.). —J. Anim. Ecol., 28, 259–281.

    Article  Google Scholar 

  12. Dixon, A. F. H., Hemptinne, J.-L. &Kindlmann, P. — 1995. The ladybird fantasy - prospects and limits to their use in the biocontrol of aphids.Züchtungsforschung (Proceedings International Symposium 75 years of Phytopathological and Resistance Research at Aschersleben) 1(2), 395–397.

    Google Scholar 

  13. El Din, N. S. — 1976. Effects of temperature on the aphidMyzus persicae (Sulz.), with special reference to critically low and high temperature. —Z. angew. Entomol., 80, 7–14.

    Google Scholar 

  14. El-Minshawy, A. M. &Moursi, K. — 1976. Biological studies on some soft scale-insects (Hom., Coccidae) attacking guava trees in Egypt. —Z. angew. Entomol., 81, 363–371.

    Google Scholar 

  15. El-Minshawy, A. M., Karam, H. H. &El-Sawaf, S. K. — 1974. Biological studies on the long tailed mealy bug,Pseudococcus longispinus (Targ. and Tozzeti). —Bull. Soc. Entomol. Egypte, 58, 385–391.

    Google Scholar 

  16. Fabres, G. &Kiyindou, A. — 1985. Comparaison du potentiel biotique de deux coccinelles (Exochomus flaviventris etHyperaspis senegalensis hottentotta, Col. Coccinellidae) prédatrices dePhenacoccus manihoti (Hom., Pseudococcidae) au Congo. —Acta Oecol./Oecol. appl., 6, 339–348.

    Google Scholar 

  17. Graf, B., Baumgärtner, J. &Delucchi, V. — 1985. Life table statistics of three apple aphids,Dysaphis plantaginea, Rhopalosiphum insertum, andAphis pomi (Homoptera, Aphididiae), at constant temperatures. —Z. angew. Entomol., 99, 285–294.

    Google Scholar 

  18. Groeters, F. R. — 1992. Geographic conservation of developmental rate in the milkweed-oleander aphid,Aphis nerii. —Acta oecol., 13, 649–661.

    Google Scholar 

  19. Hafez, M. &Salama, H. S. — 1969. Biological studies on the sugarcane mealy bug,Saccharicoccus sacchari CKII., in Egypt [Hemiptera-Homoptera: Coccoidea]. —Bull. Soc. Entomol. Egypte, 53, 499–516.

    Google Scholar 

  20. Hafez, M. &Salama, H. S. — 1969. Biology of the citrus purple scaleLepidosaphes beckii Newm., in Egypt [Hemiptera-Homoptera: Coccoidea]. —Bull. Soc. Entomol. Egypte, 53, 518–532.

    Google Scholar 

  21. Hayakawa, D. L., Grafius, E. &Stehr, F. W. — 1990. Effects of temperature on longevity, reproduction, and development of the asparagus aphid (Homoptera: Aphididae) and the parasitoid,Diaeretiella rapae (Hymenoptera: Braconidae). —Environ. Entomol., 19, 890–897.

    Google Scholar 

  22. Heidari, M. — 1989. Biological control of glasshouse mealy bugs using coccinellid predators. — PhD Thesis, Wye College, University of London.

  23. Herrera, C. J., van Driesche, R. G. &Bellotti, A. C. — 1989. Temperature-dependent growth rates for the cassava mealy bug,Phenacoccus herreni, and two of its encyrtid parasitoids,Epidinocarsis diversicornis andAcerophagus coccois in Columbia. —Entomol. exp. appl., 50, 21–27.

    Article  Google Scholar 

  24. Hodek, I. — 1973. Biology of Coccinellidae.Academia, Prague, 260 p.

    Google Scholar 

  25. Ibrahim, M. M. — Studies ofCoccinella undecimpunctata aegyptiaca Rche II. Biology and Life-history [Coleoptera: Coccinellidae]. —Bull. Soc. Entomol. Egypte, 39, 395–423.

  26. Iheagwam, E. U. &Eluwa, M. C. — 1983. The effects of temperature on the development of the immature stages of the Cassava mealy bug,Phenacoccus manihoti Mat-Ferr. (Homoptera, Pseudococcidae). —Deutsche Entomologische Zeitschrift, 30, 17–22.

    Article  Google Scholar 

  27. Ito, K. — 1938. Studies on the life history of the pineapple mealy bug,Pseudococcus brevipes (Ckll.). —J. Econ. Entomol., 31, 291–298.

    Google Scholar 

  28. Izhevsky, S. S. &Orlinsky, A. D. — 1988. Life history of the importedScymnus (Nephus) reunioni [Col.: Coccinellidae] predator of mealy bugs. —Entomophaga, 33, 101–114.

    Article  Google Scholar 

  29. Kaakeh, W. &Dutcher, J. D. — 1992. Estimation of life parameters ofMonelliopsis pecanis, Monellia caryella andMelanocallis caryaefoliae (Homoptera: Aphididae) on single pecan leaflets. —Environ. Entomol., 21, 632–639.

    Google Scholar 

  30. Kanika-Kiamfu, J., Kiyindou, A., Brun, J. &Iperti, G. — 1992. Comparaison des potentialités biologiques de trois coccinelles prédatrices de la cochenille farineuse du maniocPhenaccocus manihoti (Hom. Pseudococcidae). —Entomophaga, 37, 277–282.

    Article  Google Scholar 

  31. Kapur, A. P. — 1942. Bionomics of some Coccinellidae, predaceous on aphids and coccids in North India. —Indian J. Entomol., 4, 49–66.

    Google Scholar 

  32. Kawauchi, S. — 1983. The threshold temperature and thermal constant for development from the egg to the adult form ofCoccinella septempunctata brucki, Propylea japonica andScymnus (Pullus) hoffmanni (Coleoptera, Coccinellidae). —Kurume University Journal, 32, 45–51.

    Google Scholar 

  33. Kehat, M. — 1968. The feeding behaviour ofPharoscymnus numidicus (Coccinellidae), predator of the date palm scaleParlatoria blanchardi. —Entomol. Exp. Appl., 11, 30–42.

    Article  Google Scholar 

  34. Kieckhefer, R. W. &Elliot, N. C. — 1989. Effect of fluctuating temperature on development of immature Russian wheat aphid (Homoptera, Aphididae) and demographic statistics. —J. Econ. Entomol., 82, 119–122.

    Google Scholar 

  35. Kindlmann, P. &Dixon, A. F. G. — 1989. Developmental constraints in the evolution of reproductive strategies; telescoping of generations in parthenogenetic aphids. —Funct. Ecol., 3, 531–537.

    Article  Google Scholar 

  36. Kindlmann, P. &Dixon, A. F. G. — 1993. Optimal foraging in ladybird beetles (Coleoptera Coccinellidae) and its consequences for their use in biological control. —Eur. J. Entomol., 90, 443–450.

    Google Scholar 

  37. Kindlmann, P. & Dixon, A. F. G. — 1996. Strategies of aphidophagous predators: lessons for modelling insect predator-prey dynamics. —Entomophaga.

  38. Kirkland, R. L., Peries, I. D. &Hamilton, G. C. — 1981. Differentiation and development rate of nymphal instars of greenbug reared on sorghum. —J. Kans. Entomol. Soc., 54, 743–747.

    Google Scholar 

  39. Kiyindou, A. &Fabres, G. — 1987. Étude de la capacité d’accroissement chezHyperaspis raynevali [Col.: Coccinellidae] prédateur introduit au Congo pour la régulation des populations dePhenacoccus manihoti [Hom.: Pseudococcidae]. —Entomophaga, 32, 181–189.

    Article  Google Scholar 

  40. Kiyindou, A. — 1989. Seuil thermique de développement de trois Coccinelles prédatrices de la Cochenille du Manioc au Congo. —Entomophaga, 34, 409–415.

    Article  Google Scholar 

  41. Kiyindou, A., Iperti, F., Ferran, A. &Brun, J. — 1992. Influence de la température et de la biomasse alimentaire sur le développement d’une coccinelle,Diomus hennesseyi (Coleoptera: Coccinellidae), prédatrice dePhenacoccus manihoti (Homoptera: Pseudococcidae) en Afrique intertropicale. —J. Afr. Zool., 106, 479–488.

    Google Scholar 

  42. Kocourek, F. &Beránková, J. — 1989. Temperature requirements for development and population growth of the green peach aphidMyzus persicae on sugar beet. —Acta Entomol. Bohemoslov., 86, 349–355.

    Google Scholar 

  43. Komazaki, S. — 1982. Effects of constant temperatures on population growth of three aphid species,Toxoptera citricidus (Kirkaldy),Aphis citricola van der Goot andAphis gossypii Glover (Homoptera: Aphididae) on Citrus. —Appl. Entomol. Zool., 17, 75–81.

    Google Scholar 

  44. Lamana, M. L. &Miller, J. C. — 1995. Temperature-dependent development in a polymorphic lady beetle,Calvia quatuordecimguttata (Coleoptera: Coccinellidae). —Ann. Entomol. Soc. Am., 88, 785–790.

    Google Scholar 

  45. Lamb, R. J. — 1992. Developmental rate ofAcyrthosiphon pisum (Homoptera: Aphididae) at low temperatures: implications for estimating rate parameters for insects. —Environ. Entomol., 21, 10–19.

    Google Scholar 

  46. Lema, K. M. &Herren, H. R. — 1985. The influence of constant temperature on population growth rates of the cassava mealy bugPhenacoccus manihoti. —Entomol. exp. appl., 38, 165–169.

    Article  Google Scholar 

  47. Leather, S. R. — 1980. Aspects of the ecology of the bird cherry-oat aphid,Rhopalosiphum padi L. PhD. thesis, University of East Anglia.

  48. Le Rü, B. &Fabres, G. — 1987. Influence de la température et de l’hygrométrie relative sur la capacité d’accroissement et le profil d’abondance des populations de la cochenille du maniocPhenacoccus manihoti (Hom., Pseudococcidae), au Congo. —Acta Oecol. Oecol. Appl., 8, 165–174.

    Google Scholar 

  49. McMullen, R. D. — 1967. The effects of photoperiod, temperature, and food supply on rate of development and diapause inCoccinella novemnotata. —Can. Entomol., 99, 578–586.

    Article  Google Scholar 

  50. Michels, G. J. &Behle, R. W. — 1991. Effects of two prey species on the development ofHippodamia sinnuata (Coleoptera: Coccinellidae) larvae at constant temperatures. —J. Econ. Entomol., 84, 1480–1484.

    Google Scholar 

  51. Michels, G. J. &Flanders, R. V. — 1992. Larval development, aphid consumption and oviposition for five imported coccinellids at constant temperature on Russian wheat aphids and greenbugs. —Southwest. Entomol., 17, 233–243.

    Google Scholar 

  52. Mills, N. J. — 1982. Satiation and the functional response: a test of a new model. —Ecol. Entomol., 7, 305–315.

    Google Scholar 

  53. Moutia, L. A. — 1944. The sugar-cane scale,Aulacaspis tegalensis, Zehnt. —Bull. Entomol. Res., 35, 69–77.

    Article  Google Scholar 

  54. Muma, M. H. — 1955. Some ecological studies on the twice-stabbed lady beetleChilocorus stigma (Say). —Ann. Entomol. Soc. Am., 48, 493–498.

    Google Scholar 

  55. Myers, L. E. — 1932. Two economic greenhouse mealy bugs of Mississippi. The citrus mealy bug and the Mexican mealy bug. —J. Econ. Entomol., 24, 891–896.

    Google Scholar 

  56. Naranjo, S. E., Gibson, R. L. &Walgenbach, D. D. — 1990. Development, survival and reproduction ofScymnus frontalis (Coleoptera: Coccinellidae), an imported predator of Russian wheat aphid, at four fluctuating temperatures. —Ann. Entomol. Soc. Am., 83, 527–531.

    Google Scholar 

  57. Nsiama She, H. D., Odebiyi, J. A. &Herren, H. R. — 1984. The biology ofHyperaspis jucunda [Col.: Coccinellidae] an exotic predator of the cassava mealy bugPhenacoccus manihoti [Hom.: Pseudococcidae] in Southern Nigeria. —Entomophaga, 29, 87–93.

    Article  Google Scholar 

  58. Obrycki, J. J. &Tauber, M. J. — 1982. Thermal requirements for development ofHippodamia convergens (Coleoptera: Coccinellidae). —Ann. Entomol. Soc. Am., 75, 678–683.

    Google Scholar 

  59. Okrouhlá, M., Chakrabarti, S. &Hodek, I. — 1983. Developmental rate and feeding capacity inCheilomenes sulphurea (Coleoptera: Coccinellidae). —Vestnik ceskoslovlenske spolecnosti zoologicke, 47, 105–117.

    Google Scholar 

  60. Pdoler, H. &Henen, J. — 1983. A comparative study of the effects of constant temperatures on development time and survival of two coccinellid beetles of the genusChilocorus. —Phytoparasitica, 11, 167–176.

    Google Scholar 

  61. Ponsonby, D. J. — 1994. Biological control of glasshouse scale insects using the Coccinellid predatorChilocorus nigritus. PhD Thesis, Wye College, University of London.

  62. Rodriguez-Saonia, C. &Miller, J. C. — 1995. Life history traits inHippodamia convergens (Coleoptera: Coccinellidae) after selection for fast development. —Biol. Contr., 5, 389–396.

    Article  Google Scholar 

  63. Rohitha, B. H. &Penman, D. R. — 1983. Effect of temperature of the biology of blue green lucerne aphid,Acyrthosiphon kondoi. —N. Z. J. Zool., 10, 299–308.

    Google Scholar 

  64. Schneider, B., Podoler, H. &Rosen, D. — 1987. Population dynamics of the Florida wax scale,Ceroplastes floridensis (Homoptera: Coccidea) on citrus in Israel 3. Developmental rate and progression of mean age. —Acta Oecol. Oecol. Appl., 8, 95–103.

    Google Scholar 

  65. Sengonça, C., Hoffman, A. &Kleinhenz, B. — 1994. Laboruntersuchungen zur Entwicklung, Lebendsdauer und Fruchtbarkeit der GetreideblattlausartenSitobion avenae (F.) undRhopalosiphum padi (L.) (Hom., Aphididae) bei verschiedenen tieferen Temperaturen. —J. Appl. Entomol., 117, 224–233.

    Article  Google Scholar 

  66. Shu-sheng, L. &Hughes, R. D. — 1987. The influence of temperature and photoperiod on the developmental, survival and reproduction of the sowthistle aphid,Hyperomyzus lactucae. —Entomol. Exp. Appl., 43, 31–38.

    Article  Google Scholar 

  67. Simpson, R. G. &Burkhardt, C. C. — 1966. Biology and evaluation of certain predators ofTherioaphis maculata (Buckton). —J. Econ. Entomol., 53, 89–94.

    Google Scholar 

  68. Tawfik, M. F. S., Nasr, S. A. &Saad, B. M. — 1973. The biology ofScymnus interruptus [Coleoptera: Coccinellidae]. —Bull. Soc. Entomol. Egypte, 57, 9–26.

    Google Scholar 

  69. Taylor, T. H. C. — 1935. The campaign againstAspidiotus destructor, Sign., in Fiji. —Bull. Entomol. Res., 26, 1–102.

    Article  Google Scholar 

  70. Uichanco, L. B. &Villanueva, F. E. — 1932. Biology of the pink mealy bug of sugar caneTrionymus sacchari (Cockerell), in the Philippines. —The Philippine Agriculturist, 21, 205–276.

    Google Scholar 

  71. Umeh, E. D. N. N. — 1982. Biological studies onHyperaspis marmottani Fairm. (Col.: Coccinellidae), a predator of the cassava mealy bugPhenacoccus manihoti Mat-Ferr. (Hom., Pseudococcidae). —Z. angew. Entomol., 94, 530–532.

    Google Scholar 

  72. Washburn, J. O. & Frankie, G. W. — 1985. Biological studies of iceplant scales,Pulvinariella mesembryanthemi andPulvinaria delottoi (Homoptera: Coccidae), in California. —Hilgardia, 53, 27 pp.

  73. Wellings, P. W. — 1981. The effect of temperature on the growth and reproduction of two closely related aphid species on sycamore. —Ecol. Entomol., 6, 209–214.

    Google Scholar 

  74. Wright, E. J. &Laing, J. E. — 1978. The effects of temperature on development, adult longevity and fecundity ofColeomegilla maculata lengi and its parasitePerilitus coccinellae. —Proc. Entomol. Soc. Ontario, 109, 33–47.

    Google Scholar 

  75. Yu, D. S. &Luck, R. F. — 1988. Temperature-dependent size and development of California Red Scale (Homoptera: Diaspididae) and its effect on host availability for the ectoparasitoidAphytis melinus De Bach (Hymenoptera: Aphelinidae). —Environ. Entomol., 17, 154–161.

    Google Scholar 

  76. Zar, J. H. — 1984. Biostatistical Analysis. —Prentice Hall International, London.

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to A. F. G. Dixon.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Dixon, A.F.G., Hemptinne, J.-. & Kindlmann, P. Effectiveness of ladybirds as biological control agents: Patterns and processes. Entomophaga 42, 71–83 (1997). https://doi.org/10.1007/BF02769882

Download citation

Key-words

  • aphids
  • biological control
  • coccids
  • ladybirds