Skip to main content
SpringerLink
Log in

Hyperpredation of local adults ladybirds on the eggs of Cryptolaemus montrouzieri a potential predator of carmine cactus cochineal Dactylopius opuntiae in Morocco

  • Original Research Article
  • Published:
International Journal of Tropical Insect Science Aims and scope Submit manuscript

Abstract

The mealybug destroyer Cryptolaemus montrouzieri has been introduced in many countries for biological control of mealybug species, recently the ladybeetle was tested on the biocontrol efficiency of Dactylopius opuntiae in many countries such as Brazil, Israel, and Morocco. Also, a total of thirteen species belonging to three orders and three families of local natural enemies associated to D. opuntiae were collected from Zemamra locality, and Gharbia locality in the Sidi Bennour region (120 km north-west of Marrakech), Morocco, and identified. A laboratory examination of C. montrouzieri eggs predation by eleven Morocco local generalist predators adults Hyperaspis campestris, Scymnus interruptus. Scymnus loewii, Nephus redtenbacheri, Scymnus latemaculatus, Scymnus guttulatus, Exochomus nigripennis, Coccinella septempunctata, Hippodamia convergens, Chilocorus bipustulatus, and Chilocorus politus showed that C. septempunctata had the highest predation on C. montrouzieri eggs (51 to 99% after 24 h) when provided with, or without, an alternative food supply (D. opuntiae first and second instars nymphs and Aphis fabae larvae). The addition of an alternative food source reduced egg predation by local polyphagous ladybeetles adults tested. These findings should be considered during biocontrol program on D. opuntiae and mass-rearing production.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Aldama-Aguilera C, Llanderal-Cázares C (2003) Cochineal: comparison of production methods in cut cladodes. Agrociencia 37:11–19

    Google Scholar 

  • Agarwala BK, Yasuda H (2001) Overlapping oviposition and chemical defense of eggs in two co-occurring species of ladybird predators of aphids. J Ethol 19:47–53

    Article  Google Scholar 

  • Barbosa PRR, Oliveira MD, Giorgi JA, Oliveira JEM, Torres JB (2014) Suitability of two prey species for development, reproduction, and survival of Tenuisvalvae notata (Coleoptera: Coccinellidae). Ann Entomol Soc Am 107:1102–1109

    Article  Google Scholar 

  • Bouharroud R, Sbaghi M, Boujghagh M, El Bouhssini M (2018) Biological control of the prickly pear cochineal Dactylopius opuntiae Cockerell (Hemiptera: Dactylopiidae). EPPO Bulletin 48:300–306

    Article  Google Scholar 

  • Bouharroud R, El Aalaoui M, Boujghagh M, Hilali L, El Bouhssini M, Sbaghi M (2019) New record and predatory activity of Hyperaspis campestris (Herbst 1783) (Coleoptera: Coccinellidae) on Dactylopius opuntiae (Hemiptera: Dactylopiidae) in Morocco. Entomol News 128(2):156–161

    Article  Google Scholar 

  • Canepari C, Fursch H, Kreissl E (1985) Die Hyperaspis-Arten von Mittel-,West-und Südeuropa. Systematik und Verbreitung. G Ital Entomol 2:223–252

    Google Scholar 

  • Carver RH, Nash JG (2011). Doing data analysis with SPSS: version 18.0. Cengage learning

  • Chacón JM, Landis DA, Heimpel GE (2008) Potential for biotic interference of a classical biological control agent of the soybean aphid. Biol Control 46:216–225

    Article  Google Scholar 

  • Chong JH, Oetting RD (2006) Functional response and progeny production of the Madeira mealybug parasitoid, Anagyrus sp. nov. nr. Sinope: the effects of host and parasitoid densities. Biol Control 39:320–328

    Article  Google Scholar 

  • Clausen CP (1978). Introduced parasites and predators of arthropod and weeds: a world review. (Ed. Clausen, C. P.), agriculture handbook no. 480, USDA Agricultural Research Service, Washington, D. C., 545 pp

  • Cottrell TE, Yeargan KV (1998) Influence of a native weed, Acalypha ostryaefolia (Euphorbiaceae), on Coleomegilla maculate (Coleoptera: Coccinellidae) population density, predation, and cannibalism in sweet corn. Environ Entomol 27:1375–1385

    Article  Google Scholar 

  • Cottrell TE (2005) Predation and cannibalism of lady beetle eggs by adult lady beetles. Biol Control 34(2):159–164

    Article  Google Scholar 

  • El Aalaoui M, Bouharroud R, Sbaghi M, El Bouhssini M, Hilali L (2019a) Predatory potential of eleven native Moroccan adult ladybird species on different stages of Dactylopius opuntiae (Cockerell) (Hemiptera: Dactylopiidae). EPPO Bulletin 49(2):374–379

    Article  Google Scholar 

  • El Aalaoui M, Bouharroud R, Sbaghi M, El Bouhssini M, Hilali L, Dari K (2019b) First study of the biology of Cryptolaemus montrouzieri and its potential to feed on the mealybug Dactylopius opuntiae (Hemiptera: Dactylopiidae) under laboratory conditions in Morocco. Arch Phytopathol Plant Protect 52:1112–1124

    Article  Google Scholar 

  • El Aalaoui M, Bouharroud R, Sbaghi M, El Bouhssini M, Hilali L, Dari K (2019c) Comparative toxicity of different chemical and biological insecticides against the scale insect Dactylopius opuntiae and their side effects on the predator Cryptolaemus montrouzieri. Arch Phytopathol Plant Protect 52:155–169

    Article  Google Scholar 

  • Felix SANDRA, Soares AO (2004) Intraguild predation between the aphidophagous ladybird beetles Harmonia axyridis and Coccinella undecimpunctata (Coleoptera: Coccinellidae): the role of body weight. Eur J Entomol 101:237–242

    Article  Google Scholar 

  • Fox TB, Landis DA, Cardoso FF, Difonzo CD (2004) Predators suppress Aphis glycines Matsumura population growth in soybean. Environ Entomol 33:608–618

    Article  Google Scholar 

  • Gillespie DR, Quiring DJM (1992) Competition between Orius tristicolor (white) (Hemiptera: Anthocoridae) and Amblyseius cucumeris (Oudemans) (Acari: Phytoseiidae) feeding on Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). Can Entomol 124:1123–1128

    Article  Google Scholar 

  • Kratina P, Vos M, Bateman A, Anholt BR (2007) Species diversity modulates predation. Ecology 88:1917–1923

    Article  Google Scholar 

  • Kratina P, Vos M, Bateman A, Anholt BR (2009) Functional responses modified by predator density. Oecologia 159:425–433

    Article  Google Scholar 

  • Koch RL, Hutchinson WD, Venette RC, Heimpel GE (2003) Susceptibility of immature monarch butterfly, Danaus plexippus (Lepidoptera: Nymphalidae) to predation by Harmonia axyridis (Coleoptera: Coccinellidae). Biol Control 28:265–270

    Article  Google Scholar 

  • Labbé RM, Cloutier C, Brodeur J (2006) Prey selection by Dicyphus hesperus of infected or parasitized greenhouse whitefly. Biocontrol Sci Tech 16:485–494

    Article  Google Scholar 

  • Lucas E, Coderre D, Brodeur J (1998) Intraguild predation among aphid predators: characterization and influence of extraguild prey density. Ecology 79:1084–1092

    Article  Google Scholar 

  • Lucas E (2005) Intraguild predation among aphidophagous predators. Eur J Entomol 102:351–364

    Article  Google Scholar 

  • Martinou AF, Raymond B, Milonas PG, Wright DJ (2010) Impact of intraguild predation on parasitoid foraging behaviour. Ecol Entomol 35:183–189

    Article  Google Scholar 

  • Martinou AF, Stavrinides MC (2015) Effects of sublethal concentrations of insecticides on the functional response of two Mirid generalist predators. PLoS One 10(12):e0144413

    Article  Google Scholar 

  • Musser FR, Shelton AM (2003) Factors affecting the temporal and within plant distribution of coccinellids in corn and their impact on potential intra-guild predation. Environ Entomol 32:575–583

    Article  Google Scholar 

  • Noia M, Borges I, Soares AO (2008) Intraguild predation between the aphidophagous ladybird beetles Harmonia axyridis and Coccinella undecimpunctata (Coleoptera: Coccinellidae): the role of intra and extraguild prey densities. Biol Control 46(2):140–146

    Article  Google Scholar 

  • Polis GA, Myers CA, Holt RD (1989) The ecology and evolution of intraguild predation: potential competitors that eat each other. Annu Rev Ecol Syst 20:297–330

    Article  Google Scholar 

  • Polis GA, Holt RD (1992) Intraguild predation: the dynamics of complex trophic interactions. Trends Ecol E vol 7:151–154

    Article  CAS  Google Scholar 

  • Protasov A, Mendel Z, Spodek M, Carvalho CJ (2017) Management of the Opuntia cochineal scale insect, Dactylopius opuntiae (Cockerell) in Israel. Alon Hanotea 71:48–51

    Google Scholar 

  • Rosenheim JA (1998) Higher-order predators and the regulation of insect herbivore populations. Annu Rev Entomol 43:421–447

    Article  CAS  Google Scholar 

  • Sanches NF, Carvalho RS (2010). Procedimentos para manejo da criação e multiplicação do predador exótico Cryptolaemus montrouzieri. Cruz das Almas: Embrapa Mandioca e Fruticultura 5 p

  • Sato S, Dixon AF, Yasuda H (2003) Effect of emigration on cannibalism and intraguild predation in aphidophagous ladybirds. Ecol Entomol 28(5):628–633

    Article  Google Scholar 

  • Sato S, Jimbo R, Yasuda H, Dixon AF (2008) Cost of being an intraguild predator in predatory ladybirds. Appl Entomol Zool 43(1):143–147

    Article  Google Scholar 

  • Sengonca C, Frings B (1985) Interference and competitive behaviour of the aphid predators, Chrysoperla carnea and Coccinella septempunctata in the laboratory. Entomophaga 30:245–251

    Article  Google Scholar 

  • Solangi GS, Lohar MK, Abro GH, Buriro AS (2012) Biology and release of exotic predator Cryptolaemus montrouzieri Mulsant on mealybug Phenacoccus solenopsis Tinsley at Tandojam. Sarhad J Agric 28:429–435

    Google Scholar 

  • Stubbs AE, Falk JS (1996). British hover flies: an illustrated identification guide. British Entomological and Natural History Society. 253 pp

  • Symondson WOC (2002) Molecular identification of prey in predator diets. Mol Ecol 11:627–641

    Article  CAS  Google Scholar 

  • Vanegas-Rico JM, Lomeli-Flores JR, Rodríguez-Leyva E, Mora-Aguilera G, Valdez JM (2010) Natural enemies of Dactylopius opuntiae (Cockerell) on Opuntia ficus-indica (L.) miller in Central Mexico. Acta Zool Mex (ns) 26:415–433

    Google Scholar 

  • Van Lenteren JC, Bale J, Bigler F, Hokkanen HMT, Loomans AJM (2006) Assession risks of releasing exotic biological control agents of arthropod pests. Annu Rev Entomol 51:609–643

    Article  Google Scholar 

  • Yasuda H, Shinya K (1997) Cannibalism and interspecific predation in two predatory ladybirds in relation to prey abundance in the field. Entomophaga 42:153–163

    Article  Google Scholar 

  • Yasuda H, Kikuchi T, Kindlmann P, Sato S (2001) Relationships between attack and escape rates, cannibalism, and intraguild predation in larvae of two predatory ladybirds. J Insect Behav 14:373–384

    Article  Google Scholar 

  • Yasuda H, Evans EW, Kajita Y, Urakawa K, Takizawa T (2004) Asymmetric larval interactions between introduced and indigenous ladybirds in North America. Oecologia 141:722–731

    Article  Google Scholar 

Download references

Funding

The research of this study was carried out as part of the collaborative program between the National Institute of Agronomic Research (INRA) and the International Center for Agricultural Research in the Dry Areas (ICARDA) in Morocco.

Author information

Authors and Affiliations

  1. National Institute of Agronomic Research, Rabat, Morocco

    Mohamed El Aalaoui, Mohamed Sbaghi & Rachid Bouharroud

  2. Faculty of Science and Technology of Settat, University Hassan I Settat, Settat, Morocco

    Mohamed El Aalaoui & Lahoucine Hilali

  3. International Center for Agricultural Research in the Dry Areas (ICARDA), Rabat, Morocco

    Mustapha El Bouhssini

Authors
  1. Mohamed El Aalaoui
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mohamed Sbaghi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rachid Bouharroud
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mustapha El Bouhssini
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lahoucine Hilali
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mohamed El Aalaoui.

Ethics declarations

Conflict of interest

Author A declares that he has no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

El Aalaoui, M., Sbaghi, M., Bouharroud, R. et al. Hyperpredation of local adults ladybirds on the eggs of Cryptolaemus montrouzieri a potential predator of carmine cactus cochineal Dactylopius opuntiae in Morocco. Int J Trop Insect Sci 41, 1011–1016 (2021). https://doi.org/10.1007/s42690-020-00282-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42690-020-00282-w

Keywords

Search

Navigation