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Do the interactions among natural enemies compromise the biological control of the whitefly Bemisia tabaci?

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Abstract

The whitefly Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) is a worldwide pest which has become one of the main pests in tomato crops. The predators Macrolophus pygmaeus (Rambur) and Nesidiocoris tenuis Reuter (Hemiptera: Miridae) and the parasitoid Eretmocerus mundus (Mercet) (Hymenoptera: Aphelinidae) have shown their efficacy at controlling B. tabaci populations when used as biological control agents. Intraguild predation (IGP) between natural enemies can affect their effectiveness at controlling pests. In the present study, the interaction of these three natural enemies and their effect on B. tabaci was studied on tomato plants by combining morphological observations and molecular analysis of trophic interactions. Under the conditions used in the present study, no IGP was detected between M. pygmaeus and N. tenuis by either counting dead predators or by PCR using prey-specific cytochrome c oxidase I primers. However, predation on B. tabaci decreased when they coexisted on the same plant, which could compromise the biological control of this pest. Although PCR analyses using E. mundus-specific primers showed predation on B. tabaci-parasitized nymphs in 27 % of M. pygmaeus and 17 % of N. tenuis, B. tabaci control was improved when both predators coexisted on the same plant with the parasitoid. The combined use of E. mundus and M. pygmaeus/N. tenuis is therefore recommended in order to improve B. tabaci control in conservation biological control strategies.

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References

  • Abrams PA (1993) Why predation rate should not be proportional to predator density. Ecology 74(3):726–733

    Article  Google Scholar 

  • Agustí N, Gabarra R (2009a) Puesta a punto de una cría masiva del depredador polífago Dicyphus tamaninii Wagner (Heteroptera: Miridae). Bol Sanid Veg, Plagas 35:205–218

    Google Scholar 

  • Agustí N, Gabarra R (2009b) Effect of adult age and insect density of Dicyphus tamaninii Wagner (Heteroptera: Miridae) on progeny. J Pest Sci 82(3):241–246

    Article  Google Scholar 

  • Agustí N, Shayler SP, Harwood JD, Vaughan IP, Sunderland KD, Symondson WOC (2003) Collembola as alternative prey sustaining spiders in arable ecosystems: prey detection within predators using molecular markers. Mol Ecol 12:3467–3475

    Article  PubMed  Google Scholar 

  • Agustí N, Bourguet D, Spataro T, Delos M, Eychenne N, Folcher L, Arditi R (2005) Detection, identification and geographical distribution of European corn borer larval parasitoids using molecular markers. Mol Ecol 14:3267–3274

    Article  PubMed  Google Scholar 

  • Alomar O, Riudavets J, Castañé C (2006) Macrolophus caliginosus in the biological control of Bemisia tabaci on greenhouse melons. Biol Control 36(2):154–162

    Article  Google Scholar 

  • Arim M, Marquet PA (2004) Intraguild predation: a widespread interaction related to species biology. Ecol Lett 7:557–564

    Article  Google Scholar 

  • Arnó J, Matas M, Martí M, Arino J, Roig J, Gabarra R (2005) Coexistence between Trialeurodes vaporariorum and Bemisia tabaci and impact of natural enemies in tomato crops under Mediterranean conditions. IOBC/WPRS Bull 28:1–4

    Google Scholar 

  • Arnó J, Castañé C, Riudavets J, Roig J, Gabarra R (2006) Characterization of damage to tomato plants produced by the zoophytophagous predator Nesidiocoris tenuis. IOBC/WPRS Bull 29:249–254

    Google Scholar 

  • Ashfaq M, Shah GS, Noor AR, Ansari SP, Mansoor S (2010) Report of a parasitic wasp (Hymenoptera: Encyrtidae) parasitizing cotton mealybug (Hemiptera: Pseudococcidae) in Pakistan and use of PCR for estimating parasitism levels. Biocontrol Sci Technol 20(6):625–630

    Article  Google Scholar 

  • Avilla J, Albajes R, Alomar O, Castañé C, Gabarra R (2004) Biological control of whiteflies in protected vegetable crops. In: Parrella MP, Heinz KM (eds) Biological control of arthropods pests in protected culture. Ball Publishing, Batavia, pp 171–184

    Google Scholar 

  • Calvo J, Bolckmans K, Stansly PA, Urbaneja A (2009) Predation by Nesidiocoris tenuis on Bemisia tabaci and injury to tomato. Biocontrol 54:237–246

    Article  Google Scholar 

  • Castañé C, Alomar O, Goula M, Gabarra R (2004) Colonization of tomato greenhouses by the predatory mirid bugs Macrolophus caliginosus and Dicyphus tamaninii. Biol Control 30:591–597

    Article  Google Scholar 

  • Castañé C, Agustí N, Arnó J, Gabarra R, Riudavets J, Comas J, Alomar O (2013) Taxonomic identification of Macrolophus pygmaeus and Macrolophus melanotoma based on morphometry and molecular markers. Bull Entomol Res 103:204–215

    Article  PubMed  Google Scholar 

  • 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 

  • Colfer RG, Rosenheim JA (2001) Predation on immature parasitoids and its impact on aphid suppression. Oecologia 126:292–304

    Article  Google Scholar 

  • Davey JS, Vaughan IP, King RA, Bell JR, Bohan DA, Bruford MW, Holland JM, Symondson WOC (2013) Intraguild predation in winter wheat: prey choice by a common epigeal carabid consuming spiders. J Appl Ecol 50:271–279

    Article  Google Scholar 

  • Finke DL, Denno RF (2003) Intra-guild predation relaxes natural enemy impacts on herbivore populations. Ecol Entomol 28:67–73

    Article  Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for the amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3(5):294–299

    CAS  PubMed  Google Scholar 

  • Foltan F, Sheppard S, Konvicka M, Symondson WOC (2005) The significance of facultative scavenging in generalist predator nutrition. Detecting decayed prey in the guts of predators using PCR. Mol Ecol 14:4147–4158

    Article  CAS  PubMed  Google Scholar 

  • Fréchette B, Rojo S, Alomar O, Lucas E (2007) Intraguild predation between syrphids and mirids: Who is the prey? Who is the predator? Biocontrol 52:175–191

    Article  Google Scholar 

  • Gabarra R, Zapata R, Castañé C, Riudavets J, Arnó J (2006) Releases of Eretmocerus mundus and Macrolophus caliginosus for controling Bemisia tabaci on spring and autumn greenhouse tomato crops. IOBC/WPRS Bull 29:71–76

    Google Scholar 

  • Gariepy TD, Kuhlmann U, Gillott C, Erlandson M (2007) Parasitoids, predators and PCR: the use of diagnostic molecular markers in biological control of Arthropods. J Appl Entomol 131:225–240

    Article  CAS  Google Scholar 

  • Gerling D (1990) Natural enemies of whiteflies: predators and parasitoids. In: Gerling D (ed) Whiteflies: their bionomics, pest status and management. Intercept Ltd, Wimborne, pp 147–186

    Google Scholar 

  • Gerling D, Fried R (2000) Biological studies with Eretmocerus mundus Mercet (Hymenoptera: Aphelinidae) in Israel. IOBC/WPRS Bull 23(1):117–123

    Google Scholar 

  • Harwood JD, Obrycki JJ (2005) Web-construction behavior of linyphiid spiders (Araneae, Linyphiidae): competition and co-existence within a generalist predator guild. J Insect Behav 18(5):593–607

    Article  Google Scholar 

  • Herrick NJ, Reitz SR, Carpenter JE, O’Brien CW (2008) Predation by Podisus maculiventris (Hemiptera: Pentatomidae) on Plutella xylostella (Lepidoptera: Plutellidae) larvae parasitized by Cotesia plutellae (Hymenoptera: Braconidae) and its impact on cabbage. Biol Control 45:386–395

    Article  Google Scholar 

  • Hindayana D, Meyhöfer R, Scholz D, Poehling HM (2001) Intraguild predation among the Hoverfly Episyrphus balteatus de Geer (Diptera: Syrphidae) and other aphidophagous predators. Biol Control 20:236–246

    Article  Google Scholar 

  • Hrcek J, Miller SE, Quicke DLJ, Smith MA (2011) Molecular detection of trophic links in a complex insect host–parasitoid food web. Mol Ecol Resour 11(5):786–794

    Article  PubMed  Google Scholar 

  • Jakobsen L, Enkegaard A, Brødsgaard HF (2004) Interactions between two polyphagous predators, Orius majusculus (Hemiptera: Anthocoridae) and Macrolophus caliginosus (Heteroptera: Miridae). Biocontrol Sci Technol 14:17–24

    Article  Google Scholar 

  • Jarman SN (2004) Amplicon: software for designing PCR primers on aligned DNA sequences. Bioinformatics 20:1644–1645

    Article  CAS  PubMed  Google Scholar 

  • Juen A, Traugott M (2005) Detecting predation and scavenging by DNA gut-content analysis a case study using a soil insect predator–prey system. Oecologia 142:344–352

    Article  PubMed  Google Scholar 

  • Kuusk A-K, Cassel-Lundhagen A, Kvarnheden A, Ekbom B (2008) Tracking aphid predation by lycosid spiders in spring-sown cereals using PCR-based gut-content analysis. Basic Appl Ecol 9:718–725

    Article  CAS  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, Fréchette B, Alomar O (2009) Resource quality, resource availability, and intraguild predation among omnivorous mirids. Biocontrol Sci Technol 19(6):555–572

    Article  Google Scholar 

  • Magalhães S, Tudorache C, Montserrat M, van Maanen R, Sabelis MW, Janssen A (2004) Diet of intraguild predators affects anti predator behavior in intraguild prey. Behav Ecol 16:364–370

    Article  Google Scholar 

  • Malo S, Arnó J, Gabarra R (2012) Intraguild interactions between the predator Macrolophus pygmaeus and the parasitoid Eretmocerus mundus, natural enemies of Bemisia tabaci. Biocontrol Sci Technol 22(9):1059–1073

    Article  Google Scholar 

  • Martinou AF, Milonas PG, Wright DJ (2009) Patch residence decisions made by Aphidius colemani in the presence of a facultative predator. Biol Control 49(3):234–238

    Article  Google Scholar 

  • Moreno-Ripoll R, Gabarra R, Symondson WOC, King RA, Agustí N (2012a) Trophic relationships between predators, whiteflies and their parasitoids in tomato greenhouses: a molecular approach. Bull Entomol Res 102:415–423

    Article  CAS  Google Scholar 

  • Moreno-Ripoll R, Agustí N, Berruezo R, Gabarra R (2012b) Conspecific and heterospecific interactions between two omnivorous predators on tomato. Biol Control 62:189–196

    Article  Google Scholar 

  • Naranjo SE, Cañas L, Ellsworth PC (2004) Mortalidad de Bemisia tabaci en un sistema de cultivos múltiples. Hortic Int 43:14–21

    Google Scholar 

  • Noppe C, Michaud JP, de Clercq P (2012) Intraguild predation between lady beetles and lacewings: outcomes and consequences vary with focal prey and arena of interaction. Ecol Popul Biol 105:562–571

    Google Scholar 

  • Okuyama T (2002) The role of antipredator behavior in an experimental community of jumping spiders with intraguild predation. Popul Ecol 44:121–125

    Article  Google Scholar 

  • Perdikis D, Lucas E, Garantonakis N, Giatropoulos A, Kitsis P, Maselou D, Panagakis S, Paraskevopoulos A, Lykouressis D, Fantinou A (2009) Intraguild predation between Macrolophus pygmaeus and Nesidiocoris tenuis. IOBC/WPRS Bull 49:301–305

    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 

  • Preisser EL, Bolnick DI, Benard MF (2005) Scared to death? The effects of intimidation and consumption in predator-prey interactions. Ecology 86:501–509

    Article  Google Scholar 

  • Rosenheim JA, Kaya HK, Ehler LE, Marois JJ, Jaffee BA (1995) Intraguild predation among biological control agents: theory and evidence. Biol Control 5:303–335

    Article  Google Scholar 

  • Rudgers JA, Hodgen JG, White JW (2003) Behavioral mechanisms underlie an ant–plant mutualism. Oecologia 135:51–59

    PubMed  Google Scholar 

  • Schmitz OJ (2007) Predator diversity and trophic interactions. Ecology 88(10):2415–2426

    Article  PubMed  Google Scholar 

  • Schmitz OJ, Beckerman AP, O’Brien KM (1997) Behaviourally mediated trophic cascades: effects of predation risk on food web interactions. Ecology 78:1388–1399

    Article  Google Scholar 

  • Snyder WE, Ives AR (2001) Generalist predators disrupt biological control by a specialist parasitoid. Ecology 82:705–716

    Article  Google Scholar 

  • Snyder WE, Ives AR (2003) Interactions between specialist and generalist natural enemies: parasitoids, predators, and pea aphid biocontrol. Ecology 84:91–107

    Article  Google Scholar 

  • Stansly PA, Calvo J, Urbaneja A (2005) Release rates for control of Bemisia tabaci (Homoptera: Aleyrodidae) biotype “Q” with Eretmocerus mundus (Hymenoptera: Aphelinidae) in greenhouse tomato and pepper. Biol Control 35:124–133

    Article  Google Scholar 

  • Symondson WOC, Sunderland KD, Greenstone MH (2002) Can generalist predators be effective biocontrol agents? Ann Rev Entomol 47:561–594

    Article  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) CLUSTAL X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Torreno HS, Magallona ED (1994) Biological relationship of the bug, Cyrtopeltis tenuis Reuter (Hemiptera: Miridae) with tobacco. Philipp Entomol 9(4):406–425

    Google Scholar 

  • Traugott M, Symondson WOC (2008) Molecular analysis of predation on parasitized hosts. Bull Entomol Res 98:223–231

    CAS  PubMed  Google Scholar 

  • Traugott M, Bell JR, Raso L, Sint D, Symondson WOC (2012) Generalist predators disrupt parasitoid aphid control by direct and coincidental intraguild predation. Bull Entomol Res 102:239–247

    Article  CAS  PubMed  Google Scholar 

  • van der Hammen T, de Roos AM, Sabelis MW, Janssen A (2010) Order of invasion affects the spatial distribution of a reciprocal intraguild predator. Oecologia 163:79–89

    Article  PubMed Central  PubMed  Google Scholar 

  • Zhang GF, Lü ZC, Wan FH (2007) Detection of Bemisia tabaci remains in predator guts using a sequence-characterized amplified region marker. Entomol Exp Appl 123:81–90

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Thaïs Aznar, Ramon Berruezo, and Yi-Bo Zhang for their technical support. This work has been funded by the Spanish Ministry of Science and Innovation (MICINN) (Projects AGL2008-00546 and AGL2010-18811). R. Moreno-Ripoll was supported by a FPI grant.

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  1. R. A. King

    Present address: College of Life and Environmental Sciences, University of Exeter, Geoffrey Pope Building, Stocker Road, Exeter, EX4 4QD, UK

Authors and Affiliations

  1. IRTA, Entomology, Ctra. de Cabrils, Km. 2, 08348, Cabrils, Barcelona, Spain

    R. Moreno-Ripoll, R. Gabarra & N. Agustí

  2. Cardiff School of Biosciences, Cardiff University, Biomedical Sciences Building, Museum Avenue, Cardiff, CF10 3AX, UK

    W. O. C. Symondson & R. A. King

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  1. R. Moreno-Ripoll
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  2. R. Gabarra
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  3. W. O. C. Symondson
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  5. N. Agustí
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Correspondence to R. Moreno-Ripoll.

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Communicated by M. Traugott.

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Moreno-Ripoll, R., Gabarra, R., Symondson, W.O.C. et al. Do the interactions among natural enemies compromise the biological control of the whitefly Bemisia tabaci?. J Pest Sci 87, 133–141 (2014). https://doi.org/10.1007/s10340-013-0522-x

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