Skip to main content
Log in

Defense Response of Native and Alien Mealybugs (Hemiptera: Pseudococcidae) Against the Solitary Parasitoid Anagyrus sp. nr. pseudococci (Girault) (Hymenoptera: Encyrtidae)

  • Published:
Journal of Insect Behavior Aims and scope Submit manuscript

Abstract

The host behavioral and immune (encapsulation) defenses against the parasitoid Anagyrus sp. nr. pseudococci were compared for five mealybug species with different phylogenetic relationships and geographical origins: i) a Mediterranean native mealybug species, Planococcus ficus, with a long co-evolutionary history with the parasitoid; ii) three alien mealybugs species, Planococcus citri, Pseudococcus calceolariae and Pseudococcus viburni, with a more recent co-evolutionary history; and iii) a fourth alien mealybug species, Phenacoccus peruvianus, with no previous common history with the parasitoid. Three host defense behaviors were registered: abdominal flipping, reflex bleeding and walking away. The native host Pl. ficus and its congener Pl. citri exhibited the lowest probability of defense behavior (0.11 ± 0.01 and 0.09 ± 0.01 respectively), whereas the highest value was observed in P. viburni (0.31 ± 0.02). Intermediate levels of defense behavior were registered for Ps. calceolariae, and Ph. peruvianus. The probability of parasitoid encapsulation was lowest and highest for two alien host species, Ph. peruvianus (0.20 ± 0.07) and Ps. viburni (0.86 ± 0.05), respectively. The native host Pl. ficus, its congener Pl. citri and Ps. calceolariae showed intermediate values (0.43 ± 0.07, 0.52 ± 0.06, and 0.45 ± 0.09, respectively). The results are relevant with respect to biological control and to understand possible evolutionary processes involved in host range of A. sp. nr. pseudococci.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Beltrà A, Soto A, Germain J-F, Matile-Ferrero D, Mazzeo G, Pellizzari G, Russo A, Franco JC, William DJ (2010) The Bougainvillea mealybug Phenacoccus peruvianus, a rapid invader from South America to Europe. Entomol Hellenica 19:137–143

    Google Scholar 

  • Ben-Dov Y (1994). A systematic catalogue of the mealybugs of the world (Insecta: Homoptera: Coccoidea: Pseudoccocidae and Putoidae) with data on their geographical distribution, host plants, biology and economic importance. Intercept, Andover

  • Blumberg D (1997) Parasitoid encapsulation as a defense mechanism in the Coccoidea (Homoptera) and its importance in biological control. Biol Control 8:225–236

    Article  Google Scholar 

  • Blumberg D, Van Driesche RG (2001) Encapsulation rates of three encyrtid parasitoids by three mealybug species (Homoptera: Pseudococcidae) found commonly as pests in commercial greenhouses. Biol Control 22:191–199

    Article  Google Scholar 

  • Blumberg D, Klein M, Mendel Z (1995) Response by encapsulation of four mealybug species (Homoptera: Pseudococcidae) to parasitization by Anagyrus pseudococci. Phytoparasitica 23:157–163

    Article  Google Scholar 

  • Blumberg D, Franco JC, Suma P, Russo A, Mendel Z (2001) Parasitoid encapsulation in mealybugs (Hemiptera: Pseudococcidae) as affected by the host-parasitoid association and superparasitism. Boll Zool Agrar Bachicoltura 33:385–395

    Google Scholar 

  • Bugila AAA, Branco M, Silva EB, Franco JC (2014) Host selection behavior and specificity of the solitary parasitoid of mealybugs Anagyrus sp. nr. pseudococci (Girault) (Hymenoptera, Encyrtidae). Biocontrol Sci Techn 24:22–38. doi:10.1080/09583157.2013.840771

    Article  Google Scholar 

  • Bugila AAA, Franco, JC, Silva EB, Branco M (in preparation). Parasitism success, development time, sex ratio and progeny body size of Anagyrus sp. nr. pseudococci (Hymenoptera: Encyrtidae) on five mealybug host species. Unpublished manuscript

  • Calatayud PA, Polanía MA, Seligmann CD, Bellotti AC (2002) Influence of water-stressed cassava on Phenacoccus herreni and three associated parasitoids. Entomol Exp Appl 102:163–175. doi:10.1046/j.1570-7458.2002.00936.x

    Google Scholar 

  • Carton Y, Poirié M, Nappi AJ (2008) Insect immune resistance to parasitoids. Insect Sci 15:67–87

    Article  CAS  Google Scholar 

  • Cerdá X, Palacios J, Retana J (2009) Ant community structure in citrus orchards in the Mediterranean basin: impoverishment as a consequence of habitat homogeneity. Environ Entomol 38:317–324

    Article  PubMed  Google Scholar 

  • Chong J–H, Oetting RD (2007) Specificity of Anagyrus sp. nov. nr. sinope and Leptomastix dactylopii for six mealybug species. BioControl 52:289–308. doi:10.1007/s10526-006-9025-5

    Article  Google Scholar 

  • Dill LM, Fraser AHG, Roitberg RD (1990) The economics of escape behaviour in the pea aphid, Acyrthosiphon pisum. Oecologia 83:473–478

    Article  Google Scholar 

  • Ennis DE, Dillon AB, Griffin CT (2010) Pine weevils modulate defensive behaviour in response to parasites of differing virulence. Anim Behav 80:283–288

    Article  Google Scholar 

  • Firlej A, Lucas E, Coderre D, Boivin G (2010) Impact of host behavioral defenses on parasitization efficacy of a larval and adult parasitoid. BioControl 55:339–348

    Article  Google Scholar 

  • Franco JC, Silva EB, Carvalho JP (2000) Mealybugs (Hemiptera, Pseudococcidae) associated with citrus in Portugal. ISA Press, Lisbon (in Portuguese)

    Google Scholar 

  • Franco JC, Silva EB, Cortegano E, Campos L, Branco M, Zada A, Mendel Z (2008) Kairomonal response of the parasitoid Anagyrus spec. nov. near pseudococci to the sex pheromone of the vine mealybug. Entomol Exp Appl 126:122–130

    Article  CAS  Google Scholar 

  • Franco JC, Zada A, Mendel Z (2009) In: Ishaaya I, Horowitz AR (eds) Novel approaches for the management of mealybug pests, Biorational control: application and resistance managements. Springer, Netherland, pp 233–278

    Chapter  Google Scholar 

  • Franco JC, Silva EB, Fortuna T, Cortegano E, Branco M, Suma P, La Torre I, Russo A, Elyahu M, Protasov A, Levi-Zada A, Mendel Z (2011) Vine mealybug sex pheromone increases citrus mealybug parasitism by Anagyrus sp. near pseudococci (Girault). Biol Control 58:230–238. doi:10.1016/j.biocontrol.2011.06.008

    Article  CAS  Google Scholar 

  • Gentry GL, Dyer LA (2002) On the conditional nature of Neotropical caterpillar defenses against their natural enemies. Ecology 83:3108–3119

    Article  Google Scholar 

  • Gillani WA, Copland MJW (1999) Defense behavior of the longtailed mealybug Pseudococcus longispinus (Targioni Tozzetti) (Hemiptera: Pseudococcidae) against the brown lacewing Sympherobius fallax Navas (Neuroptera: Hemerobiidae). Entomologica 33:279–285

    Google Scholar 

  • Giordanengo P, Nénon JP (1990) Melanization and encapsulation of eggs and larvae of Epidinocarsis lopezi by its host Phenacoccus manihoti: effects of superparasitism and egg laying patterns. Entomol Exp App 56:155–163. doi:10.1111/j.1570-7458.1990.tb01393.x

    Article  Google Scholar 

  • Gross P (1993) Insect behavioral and morphological defenses against parasitoids. Ann Rev Entomol 38:251–273

    Article  Google Scholar 

  • Güleç G, Kilinçer A, Kaydan MB, Ülgentürk S (2007) Some biological interactions between the parasitoid Anagyrus pseudococci (Girault) (Hymenoptera: Encyrtidae) and its host Planococcus ficus (Signoret) (Hemiptera: Coccoidea: Pseudococcidae). J Pest Sci 80:43–49

    Article  Google Scholar 

  • Gullan P, Kosztarab M (1997) Adaptations in scale insects. Ann Rev Entomol 42:23–50

    Article  CAS  Google Scholar 

  • Hamilton WD (1964) The genetical evolution of social behaviour I and II. J Theor Biol 7(1–16):17–52

    Article  CAS  PubMed  Google Scholar 

  • Hardy NB, Gullan PJ, Hodgson CJ (2008) A subfamily-level classification of mealybugs (Hemiptera: Pseudococcidae) based on integrated molecular and morphological data. Syst Entomol 33:51–71

    Article  Google Scholar 

  • Hartbauer M (2010) Collective defense of Aphis nerii and Uroleucon hypochoeridis (Homoptera, Aphididae) against natural enemies. PLoS ONE 5(4):e10417. doi:10.1371/journal.pone.0010417

    Article  PubMed Central  PubMed  Google Scholar 

  • Heidari M, Jahan M (2000) A study of ovipositional behaviour of Anagyrus pseudococci a parasitoid of mealybugs. J Agric Sci Technol 1:49–53

    Google Scholar 

  • Kraaijeveld AR, van Alphen JJM, Godfray HCJ (1998) The coevolution of host resistance and parasitoid virulence. Parasitology 116:S29–S45

    Article  PubMed  Google Scholar 

  • Mgocheki N, Addison P (2009) Incorporating sampling precision into an action threshold for monitoring ant (Hymenoptera: Formicidae) population levels in vineyards. Crop Prot 28:257–263

    Article  Google Scholar 

  • Nestel D, Cohen H, Saphir N, Klein M, Mendel Z (1995) Spatial distribution of scale insects comparative study using Taylor’s power-law. Environ Entomol 24:506–512

    Google Scholar 

  • Noyes J, Hayat M (1994) Oriental mealybug parasitoids of the Anagyrini (Hymenoptera: Encyrtidae). CAB International, Wallingford

    Google Scholar 

  • Pekas A, Tena A, Agular A, Garcia-Marí F (2011) Spacio-temporal patterns and interactions with honeydew-producing Hemiptera of ants in a Mediterranean citrus orchard. Agric Forest Entomol 13:89–97

    Article  Google Scholar 

  • Sagarra LA, Peterkin DD, Vincent C, Stewart RK (2000) Immune response of the hibiscus mealybug, Maconellicoccus hirsutus Green (Homoptera: Pseudococcidae), to oviposition of the parasitoid Anagyrus kamali Moursi (Hymenoptera: Encyrtidae). J Insect Physiol 46:647–653

    Article  CAS  PubMed  Google Scholar 

  • Sagarra LA, Vincent C, Stewart RK (2001) Suitability of nine Mealybug species (Homoptera: Pseudococcidae) as hosts for the parasitoid Anagyrus kamali (Hymenoptera: Encyrtidae). Florida Entomol 84:112–116

    Article  Google Scholar 

  • Sasaki A, Godfray HCJ (1999) A model for the coevolution of resistance and virulence in coupled host-parasitoid interactions. Proc R Soc Lond B 266:455–463

    Article  Google Scholar 

  • Schmid-Hempel P (2005) Evolutionary ecology of insect immune defenses. Ann Rev Entomol 50:529–551

    Article  CAS  Google Scholar 

  • Strand MR (2008) The insect cellular immune response. Insect Sci 15:1–14

    Article  CAS  Google Scholar 

  • Strand MR, Obrycki JJ (1996) Host specificity of insect parasitoids and predators. Bioscience 46:422–429

    Article  Google Scholar 

  • Strand MR, Pech LL (1995) Immunological basis for compatibility in parasitoid-host relationships. Ann Rev Entomol 40:31–56

    Article  CAS  Google Scholar 

  • Suma P, Mansour R, Russo A, La Torre I, Bugila AA, Franco JC (2012) Encapsulation rates of the parasitoid Anagyrus sp. nr. pseudococci, by three mealybug species (Hemiptera: Pseudococcidae). Phytoparasitica 40:11–16

    Article  Google Scholar 

  • Thompson JN (2001) The geographic dynamics of coevolution. In: Fox CW, Roff DA, Fairbairn DJ (eds) Evolutionary ecology: concepts and case studies. Oxford University Press, Oxford, pp 331–343

    Google Scholar 

  • Triapitsyn SV, González D, Vickerman DB, Noyes J, White EB (2007) Morphological, biological, and molecular comparisons among the different geographical populations of Anagyrus pseudococci (Hymenoptera: Encyrtidae), parasitoids of Planococcus spp. (Hemiptera: Pseudococcidae), with notes on Anagyrus dactylopii. Biol Control 41:14–24

    Article  Google Scholar 

  • Vinson SB (1998) The general host selection behavior of parasitoid Hymenoptera and a comparison of initial strategies utilized by larvaphagous and oophagous species. Biol Control 11:79–96

    Article  Google Scholar 

  • Völkl W, Woodring J, Fischer M, Lorenz MW, Hoffmann KH (1999) Ant-aphid mutualisms: the impact of honeydew production and honeydew sugar composition on ant preferences. Oecologia 118:483–491

    Article  Google Scholar 

  • Way MJ (1963) Mutualism between ants and honeydew-producing Homoptera. Ann Rev Entomol 8:307–344

    Article  Google Scholar 

  • Way MJ, Khoo KC (1992) Role of ants in pest management. Ann Rev Entomol 37:479–503

    Article  Google Scholar 

  • Williams DJ (1978) The anomalous antattended mealybugs (Homoptera, Coccoidea, Pseudococcidae) of south-east Asia. Bull British Mus Nat Hist Entomol 37:1–72

    Google Scholar 

  • Zhou A, Lu Y, Zeng L, Xu Y, Liang G (2012) Fire ant—hemipteran mutualism: comparison of ant preference for honeydew excreted by an invasive mealybug and a native aphid. Sociobiology 59:795–804

    Google Scholar 

  • Zina, V., Soares, C., Laranjo, H., Franco, J. C. (2011). Ant species associated to tree canopy in citrus orchards in the southern region of Portugal. In Garcia Mari, F. (ed.), Proceedings of the meeting of the Working Group “Integrated Control in Citrus Fruit Crops”, Agadir (Morocco), 1–3 Mar 2010. IOBC/wprs Bull. 62: 351. (abstract)

Download references

Acknowledgments

We are most grateful to Manuel Cariano and Vera Zina, for helping in the mealybug and parasitoid rearing in the laboratory; this research was supported by the Fundação para a Ciência e Tecnologia (project PTDC/AGR-AAM/099560/455/2008). The first author benefited from a PhD grant from the Libyan Government.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Abdalbaset A. A. Bugila.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bugila, A.A.A., Franco, J.C., da Silva, E.B. et al. Defense Response of Native and Alien Mealybugs (Hemiptera: Pseudococcidae) Against the Solitary Parasitoid Anagyrus sp. nr. pseudococci (Girault) (Hymenoptera: Encyrtidae). J Insect Behav 27, 439–453 (2014). https://doi.org/10.1007/s10905-014-9440-x

Download citation

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10905-014-9440-x

Keywords

Navigation