Journal of Insect Behavior

, Volume 31, Issue 2, pp 222–239 | Cite as

The impact of ant attendance on protecting Aphis gossypii against two aphidophagous predators and it’s role on the Intraguild Predation between them

  • Tahereh Karami-jamour
  • Alinaghi Mirmoayedi
  • Abbasali Zamani
  • Yadolah Khajehzadeh


In this study the changes in Aphis gossypii Glover populations tended by the homopteran- tending ant, Tapinoma simrothi Krausse when exposed to the natural enemies Chrysoperla carnea Stephens and Coccinellia septempunctata Mulsant was studied. We also studied the effect of ant’s attendance on the consequence of intraguild predation (IGP) between these two predators. The presence of ants T. simrothi had deterrent impact on natural enemies of A. gossypii compared to control aphid populations in absence of ants. Equally we observed that IGP between two aphid predators decreased when T. simrothi was present. The lowest IGP level was observed when both aphids and ants were present in the microcosm arena. In the microcosm arena the presence of ants had an indirect effect on the occurrence of IGP. Our results suggest that although the mutualistic ants have an indirect impact on the IGP by aphidophages predators, but their roles should not be ignored.


Hemipteran aphidophages intraguild predation mutualism Aphis gossypii Tapinoma simrothi 



This study was a part of PhD dissertation of the first author, approved and supported by the Razi University of Kermanshah, Iran, which we thank cordially. Equally we appreciate and thank the head of Plant Protection Research Institute, Agricultural Research Center of Ahvaz, Khuzestan, Iran for technical support.


  1. Addicott JF (1979) A multispecies aphid-ant association: density dependence and species-specific effects. Can J Zool 56:2093–2096CrossRefGoogle Scholar
  2. Bach CE (1991) Direct and indirect interactions between ants (Pheidole megacephala), scales (Coccus viridis) and plants (Pluchea indica). Oecologia 87:233–239CrossRefPubMedGoogle Scholar
  3. Barbani LE (2003) Foraging activity and food preferences of the odorous house ant (Tapinoma sessile Say) (Hymenoptera: Formicidae). Virginia Polytechnic Institute and State University, BlacksburgGoogle Scholar
  4. Beattie AJ (1985) The evolutionary ecology of ant–plant mutualisms. Cambridge University Press, Cambridge University Press, CambridgeCrossRefGoogle Scholar
  5. Bishop DB, Bristow CM (2003) Effects of the presence of the Allegheny mound ant (Hymenoptera: Formicidae) in providing enemy-free space to myrmecophilous aphid and soft scale populations. Ann Entomol Soc Am 96:202–210CrossRefGoogle Scholar
  6. Bristow CM (1984) Differential benefits from ant attendance to two species of Homoptera on New York ironweed. J Anim Ecol 53:715–726CrossRefGoogle Scholar
  7. Buczkowski G, Bennet G (2008) Seasonal polydomy in a polygynous supercolony of the odorous house ant, Tapinoma sessile. Ecol Entomol 33(6):780–788Google Scholar
  8. Bugg RL, Dutcher JD (1989) Warm-season cover crops for pecan orchards: horticultural and entomological implications. Biol Agric Hortic 6:123–148CrossRefGoogle Scholar
  9. Carletto J, Lombaert E, Chavigny P, Brevault T, Lapchin L, Vanlerberghe-Masutti F (2009) Ecological specialization of the aphid Aphis gossypii Glover on cultivated host plants. Mol Ecol 18:2198–2212CrossRefPubMedGoogle Scholar
  10. Carroll CR, Janzen DH (1973) Ecology of foraging by ants. Annu Rev Ecol Syst 4:231–257CrossRefGoogle Scholar
  11. Charaabi K, Carletto J, Chavigny P, Marrakchi M, Makni M, Vanlerberghe-Masutti F (2008) Clonal diversity of the melon aphid Aphis gossypii (Glover) in Tunisia is structured by host plants. Bull Entomol Res 98:333–341CrossRefPubMedGoogle Scholar
  12. Cushman JH, Whitham TG (1989) Conditional mutualism in a membracid–ant association: temporal, age-specific and density-dependent effects. Ecol 70:1040–1047CrossRefGoogle Scholar
  13. Daane KM, Sime KR, Fallon J, Cooper ML (2007) Impacts of Argentine ants on mealybugs and their natural enemies in California’s coastal vineyards. Ecol Entomol 32:583–596CrossRefGoogle Scholar
  14. Debaraj Y, Singh TK (1990) Biology of an aphidophagous Coccinella predator, Coccinella tranversalis. J Biol Control 4:93–95Google Scholar
  15. Dutcher JD (1998) Conservation of aphidophaga in pecan orchards. In: Barbosa P (ed) Conservation biological control. Academic Press, New York, pp 291–305CrossRefGoogle Scholar
  16. Ebert TA, Cartwright B (1997) Biology and ecology of Aphis gossypii (Homoptera: Aphididae). Southwest Entomol 22:116–153Google Scholar
  17. Feng DD, Michaud JP, Li P, Zhou ZS, Xu ZF (2015) The native ant, Tapinoma melanocephalum, improves the survival of an invasive mealybug, Phenacoccus solenopsis, by defending it from parasitoids. Sci Rep 5:1569Google Scholar
  18. Finlayson CJ, Alyokhin AV, Porter EW (2009) Interactions of native and non-native lady beetle species (Coleoptera : Coccinellidae) with aphid-tending ants in laboratory arenas. Environ Entomol 38(3):846–855CrossRefPubMedGoogle Scholar
  19. Fischer MK, Hoffmann KH, Völkl W (2001) Competition for mutualisms in an ant-homopteran interaction mediated by hierarchies of ant attendance. Oikos 92:531–541CrossRefGoogle Scholar
  20. Fox L (1975) Cannibalism in natural populations. Annu Rev Ecol Systemat 6:87–106CrossRefGoogle Scholar
  21. Frazer BD, van den Bosch R (1973) Biological control of the walnut aphid in California: the interrelationship of the aphid and its parasite. Environ Entomol 2:561–568CrossRefGoogle Scholar
  22. Hagen Ks (1986) Nutritional ecology of terrestrial insect predators. In: Slansky F Jr, Rodriguez JG (eds) Nutritional Ecology of Insects, Mites, Spiders and Related Invertebrates. Wiley, New York, pp 533–577Google Scholar
  23. Harmon JP, Andow DA (2007) Behavioral mechanisms underlying ants’ density-dependent deterrence of aphid-eating predators. Oikos 116:1030–1036CrossRefGoogle Scholar
  24. Hindayana D, Meyhofer R, Scholz D, Poehling HM (2001) Intraguild predation among the hoverfly Episyrphus balteatus de Geer (Diptera: Syrphidae) and other aphidophagous predators. Biol Control 20:236–246CrossRefGoogle Scholar
  25. Hölldobler B, Wilson EO (1990) The ants. Belknap Press, Belknap Press, CambridgeCrossRefGoogle Scholar
  26. Hu GY, Frank JH (1996) Effect of the red imported fire ant (Hymenoptera: Formicidae) on dung-inhabiting arthropods in Florida. Environ Entomol 25:1290–1296CrossRefGoogle Scholar
  27. James DG, Stevens MM, O’Malley KJ, Faulder RJ (1999) Ant foraging reduces the abundance of beneficial and incidental arthropods in citrus canopies. Biol Control 14:121–126CrossRefGoogle Scholar
  28. Kaneko S (2002) Aphid-attending ants increase the number of emerging adults of the aphid’s primary parasitoid and hyperparasitoids by repelling intraguild predators. Entomol Sci 5:131–146Google Scholar
  29. Kaneko S (2003) Different impacts of two species of aphid-tending ants with different aggressiveness on the number of emerging adults of the aphid's primary parasitoid and hyperparasitoids. Ecol Res 18:199–212CrossRefGoogle Scholar
  30. Kaneko S (2007) Predator and parasitoid attacking ant-attended aphids: effects of predator presence and attending ant species on emerging parasitoid numbers. Ecol Res 22:451–458CrossRefGoogle Scholar
  31. Kaplan I, Eubanks MD (2002) Disruption of the cotton aphid (Homoptera: Aphididae) natural enemy dynamics by red imported fire ants (Hymenoptera: Formicidae). Environ Entomol 31:1175–1183CrossRefGoogle Scholar
  32. Katayama N, Suzuki N (2002) Cost and benefit of ant attendance for Aphis craccivora (Hemiptera: Aphididae) with reference to aphid colony size. Can Entomol 134:241–249CrossRefGoogle Scholar
  33. Katayama N, Suzuki N (2003) Bodyguard effects for aphids of Aphis craccivora Koch (Homoptera: Aphididae) as related to the activity of two ant species, Tetramorium caespitum Linnaeus (Hymenoptera: Formicidae) and Lasius niger L: (Hymenoptera: Formicidae). Appl Entomol Zool 38:427–433CrossRefGoogle Scholar
  34. Liere H, Perfecto L (2008) Cheating on a mutualism: indirect benefits of ant attendance to a coccidophagous coccinellid. Environ Entomol 37:143–149CrossRefPubMedGoogle Scholar
  35. Lucas E (2005) Intraguild predation among aphidophagous predators. Eur J Entomol 102:351–364CrossRefGoogle Scholar
  36. Lucas E, Coderre D, Brodeur J (1998) Intraguild predation among aphid predators: characterization and influence of extraguild prey density. Ecol 79:1084–1092CrossRefGoogle Scholar
  37. Majerus MEN (1989) Coccinella magnifica (Redtenbacher) a myrmecophilous ladybird. Br J Entomol Nat Hist 2:97–106Google Scholar
  38. Majerus, M. (1994). Ladybirds. Harper Collins, London, 367 pGoogle Scholar
  39. Mansour R, Suma P, Mazzeo G, Pergola AL, Pappalardo V, Lebdi KG, Russo A (2012) Interactions between the ant Tapinoma nigerrimum (Hymenoptera: Formicidae) and the main natural enemies of the vine and citrus mealybugs (Hemiptera: Pseudococcidae). Biocontrol Sci Techn 22:527–537CrossRefGoogle Scholar
  40. Mgocheki N, Addison P (2009) Interference of ants (Hymenoptera: Formicidae) with biological control of the vine mealybug Planococcus ficus (Signoret) (Hemiptera: Pseudococcidae). Biol Control 49:180–185CrossRefGoogle Scholar
  41. Mirmoayedi, A. (2001). Release of eggs and larvae of Chrysoperla carnea for control of eggs and nymphs of cotton’s spiny bollworm (Earias insulana). In: Proceedings of the 2nd Irano-Russia Agricultural and natural Resources Conference 2001; 1–2 February 2001; Moscow, Timiryazev: Agricultural Academy, RussiaGoogle Scholar
  42. Morales MA (2000) Survivorship of an ant-tended membracid as a function of ant recruitment. Oikos 90:469–476CrossRefGoogle Scholar
  43. Muller CB, Godfray HCJ (1999) Predators and mutualists influence the exclusion of aphid species from natural communities. Oecologia 119:120–125CrossRefPubMedGoogle Scholar
  44. Nakamuta K, Saito T (1985) Recognition of aphid prey by the lady beetle, Coccinella septempunctata (Coleoptera; Coccinellidae). Appl Entomol Zool 20:479–483CrossRefGoogle Scholar
  45. Nedved O, Fois X, Ungerova D, Kalushkov P (2013) Alien vs. Predator – the native lacewing Chrysoperla carnea is the superior intraguild predator in trials against the invasive ladybird Harmonia axyridis. Bull Insectology 66:73–78Google Scholar
  46. Ness JH, Bronstein JL (2004) The effects of invasive ants on prospective ant mutualists. Biol Invasions 6:445–461CrossRefGoogle Scholar
  47. Noppe, C., Michaud, J.P., and De Clercq, P. (2012). Intraguild predation between lady beetles and lacewings: outcomes and consequences vary with focal prey and arena of Interaction. Ann Entomol Soc Am 105: 562–571Google Scholar
  48. Novgorodova TA (2015) Organization of honeydew collection by foragers of different species of ants (Hymenoptera: Formicidae): Effect of colony size and species specificity. Eur J Entomol 112(4):688–697Google Scholar
  49. Novgorodova TA, Gavrilyuk AV (2012) The degree of protection different ants (Hymenoptera: Formicidae) provide aphids (Hemiptera: Aphididae) against aphidophages. Eur J Entomol 109(2):187–196CrossRefGoogle Scholar
  50. Nunez-Perez E, Tizado-Morales EJ, Nieto Nafria JM (1992) Coccinellid (Coleoptera: Coccinellidae) predators of aphids on cultivated plants in Leon. Bol San veg Plagas 18:765–775Google Scholar
  51. Obrycki JJ, Hamid MN, Sajap SA (1989) Suitability of corn insect pests for development and survival of Chrysoperla carnea and Chrysopa oculata (Neuroptera: Chrysopidae). Environ Entomol 18:1126–1130CrossRefGoogle Scholar
  52. Okuyama T (2009) Intraguild predation in biological control: consideration of multiple resource species. BioControl 54:3–7CrossRefGoogle Scholar
  53. Phoofolo MW, Obrycki JJ (1998) Potential for intraguild predation and competition among predatory Coccinellidae and Chrysopidae. Entomol Exp Appl 89:47–55CrossRefGoogle Scholar
  54. Powell BE, Silverman J (2010) Impact of Linepithema humile and Tapinoma sessile (Hymenoptera: Formicidae) on three natural enemies of Aphis gossypii (Hemiptera: Aphididae). Biol Control 54:285–291CrossRefGoogle Scholar
  55. Ridgway RL, Murphy WL (1984) Biological control in the field. In: Semeria Y, New TR (eds) Canard M. Dr. W. Junk Publishers, The Hague, pp 220–228Google Scholar
  56. Ridgway RL, Morrison RK, Badgley M (1970) Mass rearing of green lacewing. J Econ Entomol 62:834–836CrossRefGoogle Scholar
  57. Rondoni G, Ielo F, Ricci C, Conti E (2014) Intraguild predation responses in two aphidophagous coccinellids identify differences among juvenile stages and aphid densities. Insects 5:974–983CrossRefPubMedPubMedCentralGoogle Scholar
  58. Satar S, Kersting U, Uygun N (1999) Development and fecundity of Aphis gossypii Glover (Homoptera: Aphididae) on three Malvaceae hosts. Turk J Agric For 23:637–643Google Scholar
  59. Sengonca C, Frings B (1985) Interference and competitive behavior of the aphid predators, Chrysoperla carnea and Coccinella septempunctata in the laboratory. Entomophaga 30:245–251CrossRefGoogle Scholar
  60. Simon T, Hefetz A (1999) Trail-following responses of Tapinoma simrothi (Formicidae: Dolichoderinae) to pygidial gland extracts. Insect Soc 38(1):17–25CrossRefGoogle Scholar
  61. Singh NN, Manoj K (2000) Potentiality of Chrysoperla carnea in suppression of mustard aphid population. Indian J Entomol 62:323–326Google Scholar
  62. SPSS Inc (2007) SPSS for Windows, version 16.0. SPSS Inc, ChicagoGoogle Scholar
  63. Stadler B, Dixon AFG (2005) Ecology and evolution of aphid–ant interactions. Annu Rev Ecol Evol S 36:345–372CrossRefGoogle Scholar
  64. Stechmann DH, Völkl W, Starý P (1996) Ant-attendance as a critical factor in the biological control of the banana aphid Pentalonia nigronervosa Coq. (Hom. Aphididae) in Oceania. J Appl Ent 120:119–123CrossRefGoogle Scholar
  65. Styrsky JD, Eubauks MD (2010) A facultative mutualism between cotton aphids and an invasive ant indirectly benefits plant reproduction. Ecol Entomol 35:190–100CrossRefGoogle Scholar
  66. Takizawa T, Yasuda H (2005) Relative strength of direct and indirect interactions of mutualistic ants and a large sized ladybird on the fate of two small sized ladybirds. In: Hirose Y et al (eds) Proceedings of the international symposium on biological control of aphids and coccids. Faculty of Agriculture. Yamagata University, Yamagata, pp 134–136Google Scholar
  67. Tedders WL, Reilly CC, Morrison BW, Lofgren CS (1990) Behavior of Solenopsis invicta (Hymenoptera: Formicidae) in pecan orchards. Environ Entomol 19:44–53CrossRefGoogle Scholar
  68. Uddin J, Holliday NJ, Mackay PA (2005) Rearing lacewings, Chrysoperla carnea and Chrysopa oculata (Neuroptera: Chrysopidae), on prepupae of alfalfa leaf cutting bee, Megachile rotundata (Hymenoptera: Megachilidae). Proc Ent Soc Mb 61:11–19Google Scholar
  69. Van den Bosch R, Hom R, Matteson P, Frazer BD, Messenger PS, Davis CS (1979) Biological control of the walnut aphid in California: impact of the parasite, Trioxys pallidus. Hilgardia 47:1–13CrossRefGoogle Scholar
  70. Venkatesan M, Singh SP, Jalali SK (2000a) Rearing of Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae) on semi-synthetic diet and its predatory efficacy against cotton pests. Entomon 25(2):81–89Google Scholar
  71. Venkatesan T, Singh SP, Jalali SK, Joshi S (2000b) Evaluation of predatory efficiency of Chrysoperla carnea (Stephens) reared on artificial diet against tobacco aphid, Myzus persicae (Sulzer) in comparison with other predators. J Entomol Res 26:193–196Google Scholar
  72. Völkl W (1992) Aphids or their parasitoids: who actually benefits from ant-attendance? J Anim Ecol 61:273–281CrossRefGoogle Scholar
  73. Volkl W (1995) Behavioral and morphological adaptations of the coccinellid Platynaspis luteorubra for exploiting ant-attended resources (Coleoptera: Coccinellidae). J Insect Behav 8:653–670CrossRefGoogle Scholar
  74. Way MJ (1963) Mutualism between ants and honeydew-producing Homoptera. Annu Rev Entomol 8:307–344CrossRefGoogle Scholar
  75. Wilbur HM (1998) Interactions between growing predators and growing prey. In: Ebenman B, Persson L (eds) Size-structured populations. Springer Publishers, Berlin, pp 157–172Google Scholar
  76. Yao I, Shibao H, Akimoto S (2000) Costs and benefits of ant attendance to the drepanosiphid aphid Tuberculatus quercicola. Oikos 89:3–10CrossRefGoogle Scholar
  77. Zaki FN, Gesraha MA (2001) Production of the green lacewing, Chrysoperla carnea (Steph.) (Neuroptera: Chrysopidae) reared on semi-artificial diet based on algae, Chlorella vulgaris. J Appl Entomol 125:97–98CrossRefGoogle Scholar
  78. Zarpas KD, Margaritopoulos JT, Tsitsipis JA (2007) Life histories of generalist predatory species, control agents of the cotton aphid Aphis gossypii (Hemiptera: Aphididae). Entomol Gener 30(1):85–101CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Plant Protection, Faculty of AgricultureRazi University of KermanshahKermanshahIran
  2. 2.Plant Protection Research InstituteAgricultural Research CenterAhwazIran

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