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

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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.

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References

  • 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 27:33–43

    Article  CAS  PubMed  Google Scholar 

  • 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 28

  • Baer H, Liu T-Y, Anderson MC, Blum M, Schmid WH, James FJ (1979) Protein components of fire ant venom (Solenopsis invicta). Toxicon 17:397–405

    Article  CAS  PubMed  Google Scholar 

  • 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 85–95

    Google Scholar 

  • Blum MS, Walder JR, Callahan PS (1958) Chemical, insecticidal, and antibiotic properties of fire ant venom. Science 128:307–308

    Article  Google Scholar 

  • 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 1:57–63

    CAS  Google Scholar 

  • Brand JM, Blum MS, Fales HM, MacConnell JG (1972) Fire ant venoms: comparative analyses of alkaloidal components. Toxicon 10:259–271

    Article  CAS  PubMed  Google Scholar 

  • Brand JM, Blum MS, Ross HH (1973) Biochemical evolution in fire ant venoms. Insect Biochem 3:45–51

    Article  CAS  Google Scholar 

  • 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 57:3128–3133

    Article  CAS  PubMed  Google Scholar 

  • 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 20:267–287

    Article  Google Scholar 

  • Chen L, Fadamiro HY (2009a) Re-investigation of venom chemistry in Solenopsis fire ants. I. Identification of novel alkaloids in S. richteri. Toxicon 53:463–478

    Google Scholar 

  • Chen L, Fadamiro HY (2009b) Re-investigation of venom chemistry in Solenopsis fire ants. II. Identification of novel alkaloids in S. invicta. Toxicon 53:479–486

    Article  CAS  PubMed  Google Scholar 

  • 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 34:246–255

    Article  CAS  Google Scholar 

  • 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 29:115–130

    Article  CAS  PubMed  Google Scholar 

  • Deslippe RJ, Guo Y (2000) Venom alkaloids of fire ants in relation to worker size and age. Toxicon 38:223–232

    Article  CAS  PubMed  Google Scholar 

  • Gilbert LE, Morrison LW (1997) Patterns of host specificity in Pseudacteon parasitoid flies (Diptera: Phoridae) that attack Solenopsis fire ants (Hymenoptera: Formicidae). Environ Entomol 26:1149–1154

    Google Scholar 

  • 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 33:15–29

    Article  Google Scholar 

  • 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 58:9–18

    Google Scholar 

  • Javors MA, Zhou W, Maas JW, Han S, Keenan RW (1993) Effects of fire ant venom alkaloids on platelet and neutrophil function. Life Sci 53:1105–1112

    Article  CAS  PubMed  Google Scholar 

  • Köpf A, Rank NE, Roininen H, Tahvanainen J (1997) Defensive larval secretions of leaf beetles attract a specialist predator Parasyrphus nigritarsis. Ecol Entomol 22:176–183

    Article  Google Scholar 

  • 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 

  • 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 35:8–19

    Article  CAS  PubMed  Google Scholar 

  • MacConnell JG, Blum MS, Fales HM (1971) Chemistry of fire ant venom. Tetrahedron 27:1129–1139

    Article  CAS  Google Scholar 

  • MacConnell JG, Blum MS, Buren WF, Williams RN, Fales HM (1976) Fire ant venoms: chemotaxonomic correlations with alkaloidal compositions. Toxicon 14:69–78

    Article  CAS  PubMed  Google Scholar 

  • 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 83:642–647

    Google Scholar 

  • 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 3:1–13

    Google Scholar 

  • Morrison LW, King JR (2004) Host location behavior in a parasitoid of imported fire ants. J Insect Behav 17:367–383

    Article  Google Scholar 

  • Morrison LW, Porter SD (2006) Post-release host-specificity testing of Pseudacteon tricuspis, a phorid parasitoid of Solenopsis invicta fire ants. Biocontrol 51:195–205

    Article  Google Scholar 

  • Obin MS, Vander Meer RK (1985) Gaster flagging by fire ants (Solenopsis spp.): functional significance of venom dispersal behavior. J Chem Ecol 11:1757–1768

    Article  CAS  Google Scholar 

  • Orr MR, Seike SH, Gilbert LE (1997) Foraging ecology and patterns of diversification in dipteran parasitoids of fire ants in south Brazil. Ecol Entomol 22:305–314

    Article  Google Scholar 

  • 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 89:536–538

    Article  Google Scholar 

  • 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 79:455–457

    Article  Google Scholar 

  • Porter SD (1998a) Host-specific attraction of Pseudacteon flies (Diptera: Phoridae) to fire ant colonies in Brazil. Fla Entomol 81:423–429

    Article  Google Scholar 

  • Porter SD (1998b) Biology and behavior of Pseudacteon decapitating flies (Diptera: Phoridae) that parasitize Solenopsis fire ants (Hymenoptera: Formicidae). Fla Entomol 81:292–309

    Article  Google Scholar 

  • 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 152–176

    Google Scholar 

  • Porter SD, Fowler HG, MacKay WP (1992) Fire ant mound densities in the United States and Brazil (Hymenoptera: Formicidae). J Econ Entomol 85:1154–1161

    Google Scholar 

  • 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 78:70–75

    Article  Google Scholar 

  • 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 90:135–138

    Google Scholar 

  • SAS Institute (2007) JMP® 7.0.1. Cary, NC, USA

  • Thead LG, Vogt JT, Streett DA (2005) Dispersal of the fire ant decapitating fly, Pseudacteon curvatus (Diptera: Phoridae) in Northeast Mississippi. Fla Entomol 88:214–216

    Article  Google Scholar 

  • Vander Meer RK, Alonso LE (1996) Fire ant alarm pheromones. Proceedings of the 1996 Imported Fire Ant Conference. Louisiana, New Orleans, pp 9–11

    Google Scholar 

  • 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 159–192

  • Vander Meer RK, Lofgren CS (1988) Use of chemical characters in defining populations of fire ants, Solenopsis saevissima complex, (Hymenoptera: Formicidae). Fla Entomol 71:323–332

    Article  CAS  Google Scholar 

  • 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 77–80

  • 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 12:123–127

    Article  CAS  Google Scholar 

  • Williams DF, Oi DH, Porter SD, Pereira RM, Briano JA (2003) Biological control of imported fire ants (Hymenoptera: Formicidae). Am Entomol 49:150–163

    Google Scholar 

  • Wilson EO (1958) Origin of the variation in the imported fire ant. Evolution 7:262–263

    Article  Google Scholar 

  • 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 10:135–164

    Google Scholar 

  • Zvereva EL, Rank NE (2004) Fly parasitoid Megaselia opacicornis uses defensive secretions of the leaf beetle Chrysomela lapponica to locate its host. Oecologia 140:516–522

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Debbie Roberts and Amy Croft (USDA-APHIS-PPQ-CPHST Laboratory/Florida DPI, Gainesville, FL, USA) for the supply of adult P. tricuspis for this study, and Dr. Art Appel (Auburn University) for helping to review an earlier version of this article. This research was funded in part by grants (to H.Y.F.) from the Alabama Fire Ant Management Program and Auburn University Biogrants Program.

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Correspondence to Henry Y. Fadamiro.

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Chen, L., Sharma, K.R. & Fadamiro, H.Y. Fire ant venom alkaloids act as key attractants for the parasitic phorid fly, Pseudacteon tricuspis (Diptera: Phoridae). Naturwissenschaften 96, 1421–1429 (2009). https://doi.org/10.1007/s00114-009-0598-6

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