Naturwissenschaften

, 96:1421 | Cite as

Fire ant venom alkaloids act as key attractants for the parasitic phorid fly, Pseudacteon tricuspis (Diptera: Phoridae)

ORIGINAL PAPER

Abstract

The phorid fly, Pseudacteon tricuspis Borgmeier, is an introduced parasitoid of imported fire ants, Solenopsis spp., in the USA. Although the assumption that phorid flies use fire ant alarm pheromones for host location is probably true, we demonstrated in a previous study the possible involvement of other ant semiochemicals in the response of P. tricuspis to fire ants. This study was conducted to determine the glandular sources and identity of the semiochemicals mediating this interaction. First, we tested the electroantennogram response of P. tricuspis to extracts of key body parts and glands of workers of the red imported fire ant, S. invicta Buren. The results confirm that the poison (venom) gland/sac is the key source of compounds which elicited strong antennal activity in P. tricuspis. Follow-up studies were conducted by using a combination of bioassay-guided fractionation and behavioral bioassays to test the hypothesis that attraction of this parasitoid to fire ants is mediated by venom alkaloids. The results confirm the response of P. tricuspis to physiologically relevant amounts of the two venom alkaloid fractions (cis and trans alkaloid fractions) of S. invicta. Further analysis by coupled gas chromatography–electroantennogram detection revealed nine venom alkaloid components including two novel 2,6-dialkylpiperideines that elicited significant antennal activity in P. tricuspis. This is the first demonstration of the role of venom alkaloids of ants as attractants for their natural enemies. We propose a semiochemical-mediated host location mechanism for P. tricuspis involving both alarm pheromones and venom alkaloids. The ecological significance of these findings, including the attraction of male P. tricuspis to fire ant venom alkaloids, possibly for mate location, is discussed.

Keywords

Pseudacteon tricuspis Solenopsis invicta Host location GC-EAD Venom Alkaloid 

References

  1. Al-Abassi S, Birkett MA, Pettersson J, Pickett JA, Wadhams LJ, Woodcock CM (2001) Response of the ladybird parasitoid Dinocampus coccinellae to toxic alkaloids from the seven-spot ladybird, Coccinella septempunctata. J Chem Ecol 27:33–43CrossRefPubMedGoogle Scholar
  2. APHIS (2007) Imported fire ant 2007: quarantine treatments for nursery stock and other regulated articles. United States Department of Agriculture, Animal and Plant Health Inspection Service (APHIS). Program Aid No. 1904. pp 28Google Scholar
  3. Baer H, Liu T-Y, Anderson MC, Blum M, Schmid WH, James FJ (1979) Protein components of fire ant venom (Solenopsis invicta). Toxicon 17:397–405CrossRefPubMedGoogle Scholar
  4. Billen J (1990) A survey of the glandular system of fire ants. In: Vander Meer RK, Jaffe K, Cedeno A (eds) Applied mymecology: a world perspective. Westview Press, Boulder, CO, pp 85–95Google Scholar
  5. Blum MS, Walder JR, Callahan PS (1958) Chemical, insecticidal, and antibiotic properties of fire ant venom. Science 128:307–308CrossRefGoogle Scholar
  6. Blum MS, Fales HM, Leadbetter G, Leonhardt BA, Duffield RM (1992) A new dialkylpiperidine in the venom of the fire ant Solenopsis invicta. J Nat Toxins 1:57–63Google Scholar
  7. Brand JM, Blum MS, Fales HM, MacConnell JG (1972) Fire ant venoms: comparative analyses of alkaloidal components. Toxicon 10:259–271CrossRefPubMedGoogle Scholar
  8. Brand JM, Blum MS, Ross HH (1973) Biochemical evolution in fire ant venoms. Insect Biochem 3:45–51CrossRefGoogle Scholar
  9. Chen J, Cantrell CL, Shang HW, Rojas MG (2009) Piperideine alkaloids from the poison gland of the red imported fire ant (Hymenoptera: Formicidae). J Agric Food Chem 57:3128–3133CrossRefPubMedGoogle Scholar
  10. Chen L, Fadamiro HY (2007) Behavioral and electroantennogram responses of phorid fly Pseudacteon tricuspis (Diptera: Phoridae) to red imported fire ant Solenopsis invicta odor and trail pheromone. J Insect Behav 20:267–287CrossRefGoogle Scholar
  11. Chen L, Fadamiro HY (2009a) Re-investigation of venom chemistry in Solenopsis fire ants. I. Identification of novel alkaloids in S. richteri. Toxicon 53:463–478Google Scholar
  12. Chen L, Fadamiro HY (2009b) Re-investigation of venom chemistry in Solenopsis fire ants. II. Identification of novel alkaloids in S. invicta. Toxicon 53:479–486CrossRefPubMedGoogle Scholar
  13. Chen L, Onagbola EO, Fadamiro HY (2005) Effects of temperature, sugar availability, gender, mating, and size on the longevity of phorid fly Pseudacteon tricuspis (Diptera: Phoridae). Environ Entomol 34:246–255CrossRefGoogle Scholar
  14. Conti E, Salerno G, Bin F, Williams HJ, Vinson SB (2003) Chemical cues from Murgantia histrionica eliciting host location and recognition in the egg parasitoid Trissolcus brochymenae. J Chem Ecol 29:115–130CrossRefPubMedGoogle Scholar
  15. Deslippe RJ, Guo Y (2000) Venom alkaloids of fire ants in relation to worker size and age. Toxicon 38:223–232CrossRefPubMedGoogle Scholar
  16. Gilbert LE, Morrison LW (1997) Patterns of host specificity in Pseudacteon parasitoid flies (Diptera: Phoridae) that attack Solenopsis fire ants (Hymenoptera: Formicidae). Environ Entomol 26:1149–1154Google Scholar
  17. Gilbert LE, Barr CL, Calixto AA, Cook JL, Drees BM, Lebrun EG, Patrock RJ, Plowes RM, Porter SD, Puckett RT (2008) Introducing phorid fly parasitoids of red imported fire ant workers from South America to Texas: outcomes vary by region and by Pseudacteon species released. Southwest Entomol 33:15–29CrossRefGoogle Scholar
  18. Greenberg L, Fletcher DJC, Vinson SB (1985) Differences in worker size and mound distribution in monogynous and polygynous colonies of the fire ant Solenopsis invicta Buren. J Kans Entomol Soc 58:9–18Google Scholar
  19. Javors MA, Zhou W, Maas JW, Han S, Keenan RW (1993) Effects of fire ant venom alkaloids on platelet and neutrophil function. Life Sci 53:1105–1112CrossRefPubMedGoogle Scholar
  20. Köpf A, Rank NE, Roininen H, Tahvanainen J (1997) Defensive larval secretions of leaf beetles attract a specialist predator Parasyrphus nigritarsis. Ecol Entomol 22:176–183CrossRefGoogle Scholar
  21. Lard CF, Schmidt J, Morris B, Estes L, Ryan C, Bergquist D (2006) An economic impact of imported fire ants in the United States of America. Texas A&M University, College Station (http://fireantecon.tamu.edu)Google Scholar
  22. Laumann R, Aquino M, Moraes M, Pareja M, Borges M (2009) Response of the egg parasitoids Trissolcus basalis and Telenomus podisi to compounds from defensive secretions of stink bugs. J Chem Ecol 35:8–19CrossRefPubMedGoogle Scholar
  23. MacConnell JG, Blum MS, Fales HM (1971) Chemistry of fire ant venom. Tetrahedron 27:1129–1139CrossRefGoogle Scholar
  24. MacConnell JG, Blum MS, Buren WF, Williams RN, Fales HM (1976) Fire ant venoms: chemotaxonomic correlations with alkaloidal compositions. Toxicon 14:69–78CrossRefPubMedGoogle Scholar
  25. Morel L, Vander Meer RK, Lofgren CS (1990) Comparison of nestmate recognition between monogyne and polygyne populations of Solenopsis invicta (Hymenoptera: Formicidae). Ann Entomol Soc Am 83:642–647Google Scholar
  26. Morrison LW (2000) Biology of Pseudacteon (Diptera: Phoridae) ant parasitoids and their potential to control imported Solenopsis fire ants (Hymenoptera: Formicidae). Recent Res Dev Entomol 3:1–13Google Scholar
  27. Morrison LW, King JR (2004) Host location behavior in a parasitoid of imported fire ants. J Insect Behav 17:367–383CrossRefGoogle Scholar
  28. Morrison LW, Porter SD (2006) Post-release host-specificity testing of Pseudacteon tricuspis, a phorid parasitoid of Solenopsis invicta fire ants. Biocontrol 51:195–205CrossRefGoogle Scholar
  29. Obin MS, Vander Meer RK (1985) Gaster flagging by fire ants (Solenopsis spp.): functional significance of venom dispersal behavior. J Chem Ecol 11:1757–1768CrossRefGoogle Scholar
  30. Orr MR, Seike SH, Gilbert LE (1997) Foraging ecology and patterns of diversification in dipteran parasitoids of fire ants in south Brazil. Ecol Entomol 22:305–314CrossRefGoogle Scholar
  31. Pereira RM, Porter SD (2006) Range expansion of the fire ant decapitating fly, Pseudacteon tricuspis, eight to nine years after releases in North Florida. Fla Entomol 89:536–538CrossRefGoogle Scholar
  32. Pesquero MA, Campiolo S, Fowler HG, Porter SD (1996) Diurnal patterns of ovipositional activity in two Pseudacteon fly parasitoids (Diptera: Phoridae) of Solenopsis fire ants (Hymenoptera: Formicidae). Fla Entomol 79:455–457CrossRefGoogle Scholar
  33. Porter SD (1998a) Host-specific attraction of Pseudacteon flies (Diptera: Phoridae) to fire ant colonies in Brazil. Fla Entomol 81:423–429CrossRefGoogle Scholar
  34. Porter SD (1998b) Biology and behavior of Pseudacteon decapitating flies (Diptera: Phoridae) that parasitize Solenopsis fire ants (Hymenoptera: Formicidae). Fla Entomol 81:292–309CrossRefGoogle Scholar
  35. Porter SD, Gilbert LE (2004) Assessing host specificity and field release potential of fire ant decapitating flies (Phoridae: Pseudacteon). In: van Driesche RG, Reardon R (eds) Assessing host ranges for parasitoids and predators used for classical biological control: a guide to best practice. Forest health technology enterprise team- 2004-03. USDA Forest Service, Morgantown, pp 152–176Google Scholar
  36. Porter SD, Fowler HG, MacKay WP (1992) Fire ant mound densities in the United States and Brazil (Hymenoptera: Formicidae). J Econ Entomol 85:1154–1161Google Scholar
  37. Porter SD, Fowler HG, Campiolo S, Pesquero MA (1995) Host specificity of several Pseudacteon (Diptera: Phoridae) parasites of fire ants (Hymenoptera: Formicidae) in South America. Fla Entomol 78:70–75CrossRefGoogle Scholar
  38. Porter SD, Williams DF, Patterson RS (1997) Rearing the decapitating fly Pseudacteon tricuspis (Diptera: Phoridae) in imported fire ants (Hymenoptera: Formicidae) from the United States. J Econ Entomol 90:135–138Google Scholar
  39. SAS Institute (2007) JMP® 7.0.1. Cary, NC, USAGoogle Scholar
  40. Thead LG, Vogt JT, Streett DA (2005) Dispersal of the fire ant decapitating fly, Pseudacteon curvatus (Diptera: Phoridae) in Northeast Mississippi. Fla Entomol 88:214–216CrossRefGoogle Scholar
  41. Vander Meer RK, Alonso LE (1996) Fire ant alarm pheromones. Proceedings of the 1996 Imported Fire Ant Conference. Louisiana, New Orleans, pp 9–11Google Scholar
  42. Vander Meer RK, Alonso LE (1998) Pheromone directed behavior in ant. In: Vander Meer RK, Breed MD, Espelie KE, Winston ML (eds) Pheromone communication in social insects. Westview Press, Boulder, CO, pp 159–192Google Scholar
  43. Vander Meer RK, Lofgren CS (1988) Use of chemical characters in defining populations of fire ants, Solenopsis saevissima complex, (Hymenoptera: Formicidae). Fla Entomol 71:323–332CrossRefGoogle Scholar
  44. Vander Meer RK, Porter SD (2002) Fire ant, Solenopsis invicta, worker alarm pheromones attract Pseudacteon phorid flies. Proceedings of the 2002 Imported Fire Ant Conference. Athens, Georgia. pp 77–80Google Scholar
  45. Vander Meer RK, Glancey BM, Lofgren CS (1982) Biochemical changes in the crop, oesophagus and postpharyngeal gland of colony-founding red imported fire ant queens (Solenopsis invicta). Insect Biochem 12:123–127CrossRefGoogle Scholar
  46. Williams DF, Oi DH, Porter SD, Pereira RM, Briano JA (2003) Biological control of imported fire ants (Hymenoptera: Formicidae). Am Entomol 49:150–163Google Scholar
  47. Wilson EO (1958) Origin of the variation in the imported fire ant. Evolution 7:262–263CrossRefGoogle Scholar
  48. Wilson EO (1962) Chemical communication among workers of the fire ant Solenopsis saevissima (F. Smith) 1. The organization of mass-foraging. 2. An information analysis of the odour trail. 3. The experimental induction of social responses. Anim Behav 10:135–164Google Scholar
  49. Zvereva EL, Rank NE (2004) Fly parasitoid Megaselia opacicornis uses defensive secretions of the leaf beetle Chrysomela lapponica to locate its host. Oecologia 140:516–522CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Li Chen
    • 1
    • 2
  • Kavita R. Sharma
    • 1
  • Henry Y. Fadamiro
    • 1
  1. 1.Department of Entomology and Plant PathologyAuburn UniversityAuburnUSA
  2. 2.Key Laboratory of Silviculture and Forest Conservation, Chinese Ministry of EducationBeijing Forestry UniversityBeijingPeople’s Republic of China

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