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Experimental and Applied Acarology

, Volume 79, Issue 1, pp 87–97 | Cite as

Red imported fire ant (Solenopsis invicta) aggression influences the behavior of three hard tick species

  • MacKenzie K. KjeldgaardEmail author
  • Oona M. Takano
  • Alison A. Bockoven
  • Pete D. Teel
  • Jessica E. Light
  • Sarah A. Hamer
  • Gabriel L. Hamer
  • Micky D. Eubanks
Article
  • 66 Downloads

Abstract

Few studies have documented the indirect effects of predators on tick behavior. We conducted behavioral assays in the laboratory to quantify the effects of a highly abundant predator, the red imported fire ant (Solenopsis invicta), on three species of ticks endemic to the southern USA: the lone star tick (Amblyomma americanum), the Gulf Coast tick (A. maculatum), and the Cayenne tick (A. mixtum). We documented ant aggression toward ticks (biting, carrying, and stinging) and determined the effects of ants on tick activity. Ticks were significantly less active in the presence of fire ants, and tick activity was negatively associated with ant aggression, but in many cases the effects of fire ants on ticks varied by tick species, stage, and engorgement status. For example, fire ants took half as long (~ 62 s) to become aggressive toward unfed A. americanum adults compared with unfed A. maculatum, and only ~ 8 s to become aggressive toward engorged A. maculatum nymphs. Correspondingly, the activity of unfed A. americanum adults and engorged A. maculatum nymphs was reduced by 67 and 93%, respectively, in the presence of fire ants. This reduction in tick activity translated to less questing by unfed ticks and less time spent walking by engorged nymphs. Our results suggest that fire ants may have important non-consumptive effects on ticks and demonstrate the importance of measuring the indirect effects of predators on tick behavior.

Keywords

Predation Indirect effects Questing Ixodidae Ticks 

Notes

Acknowledgements

We thank Otto F. Strey, Tick Research Laboratory, who reared all of the ticks used in this experiment. We also thank Eric Bockoven for helping maintain fire ant colonies and collect data. This work was funded by a grant from the Management of Invasive Ants in Texas Program through Texas A&M AgriLife Research. This is publication 1611 of the Biodiversity Research and Teaching Collections at Texas A&M University.

Supplementary material

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Electronic supplementary material 1 (DOCX 253 kb)

References

  1. Arsnoe I, Tsao JI, Hickling GJ (2019) Nymphal Ixodes scapularis questing behavior explains geographic variation in Lyme borreliosis risk in the eastern United States. Ticks Tick Borne Dis 10:553–563CrossRefGoogle Scholar
  2. Banks WA et al (1981) Techniques for collecting, rearing, and handling imported fire ants. USDA SEA AATS-S-21Google Scholar
  3. Barré N, Mauleon H, Garris GI, Kermarrec A (1991) Predators of the tick Amblyomma variegatum (Acari: Ixodidae) in Guadeloupe, French West indies. Exp Appl Acarol 12:163–170CrossRefGoogle Scholar
  4. Beati L et al (2013) Amblyomma cajennense (Fabricius, 1787)(Acari: Ixodidae), the Cayenne tick: phylogeography and evidence for allopatric speciation. BMC Evol Biol 13:267CrossRefGoogle Scholar
  5. Bock R, Jackson L, De Vos A, Jorgensen W (2004) Babesiosis of cattle. Parasitology 129:S247–S269CrossRefGoogle Scholar
  6. Bockoven A, Wilder S, Eubanks M, Pratt S (2015) Intraspecific variation among social insect colonies: persistent regional and colony-level differences in fire ant foraging behavior. PLoS One 10:e0133868–e0133868CrossRefGoogle Scholar
  7. Burns EC, Melancon DG (1977) Effect of imported fire ant (Hymenoptera: Formicidae) invasion on lone star tick (Acarina: Ixodidae) populations. J Med Entomol 14:247–249CrossRefGoogle Scholar
  8. Burtis J, Pflueger C (2017) Interactions between soil-dwelling arthropod predators and Ixodes scapularis under laboratory and field conditions. Ecosphere 8:e01914CrossRefGoogle Scholar
  9. Cassill DL, Tschinkel WR (1999) Regulation of diet in the fire ant, Solenopsis invicta. J Insect Behav 12:307–328CrossRefGoogle Scholar
  10. Castellanos AA et al (2016) Decreased small mammal and on-host tick abundance in association with invasive red imported fire ants (Solenopsis invicta). Biol Lett 12:20160463CrossRefGoogle Scholar
  11. Crowl TA, Crist TO, Parmenter RR, Belovsky G, Lugo AE (2008) The spread of invasive species and infectious disease as drivers of ecosystem change. Front Ecol Environ 6:238–246CrossRefGoogle Scholar
  12. Dawes-Gromadzki TZ, Bull CM (1997) Ant predation on different life stages of two Australian ticks. Exp Appl Acarol 21:109–115CrossRefGoogle Scholar
  13. Eisen R, Eisen L (2018) The blacklegged tick, Ixodes scapularis: an increasing public health concern. Trends Parasitol 34:295–309CrossRefGoogle Scholar
  14. Finke DL (2012) Contrasting the consumptive and non-consumptive cascading effects of natural enemies on vector-borne pathogens. Entomol Exp Appl 144:45–55CrossRefGoogle Scholar
  15. Fischhoff IR, Burtis JC, Keesing F, Ostfeld RS (2018) Tritrophic interactions between a fungal pathogen, a spider predator, and the blacklegged tick. Ecol Evol 8:7824–7834CrossRefGoogle Scholar
  16. Fleetwood S, Teel P, Thompson G (1984) Impact of imported fire ant on lone star tick mortality in open and canopied pasture habitats of east central Texas. Southwest Entomol 9:158–162Google Scholar
  17. Fox J, Weisberg S (2018) An R companion to applied regression. Sage, Thousand OaksGoogle Scholar
  18. Gage KL, Burkot TR, Eisen RJ, Hayes EB (2008) Climate and vectorborne diseases. Am J Prev Med 35:436–450CrossRefGoogle Scholar
  19. Hawlena D, Pérez Mellado V (2009) Change your diet or die: predator-induced shifts in insectivorous lizard feeding ecology. Oecologia 161:411–419CrossRefGoogle Scholar
  20. Jeger M, Chen Z, Powell G, Hodge S, Van den Bosch F (2011) Interactions in a host plant-virus–vector–parasitoid system: modelling the consequences for virus transmission and disease dynamics. Virus Res 159:183–193CrossRefGoogle Scholar
  21. Keesing F et al (2009) Hosts as ecological traps for the vector of Lyme disease. Proc R Soc B 276:3911–3919CrossRefGoogle Scholar
  22. Krause P et al (2013) Human Borrelia miyamotoi infection in the United States. N Engl J Med 368:291–293CrossRefGoogle Scholar
  23. Lenth R (2018) emmeans: estimated marginal means, aka least-squares means. R package version 1.4. https://CRAN.R-project.org/package=emmeans
  24. Levi T, Keesing F, Holt RD, Barfield M, Ostfeld RS (2016) Quantifying dilution and amplification in a community of hosts for tick-borne pathogens. Ecol Appl 26:484–498CrossRefGoogle Scholar
  25. Long EY, Finke DL (2015) Predators indirectly reduce the prevalence of an insect-vectored plant pathogen independent of predator diversity. Oecologia 177:1067–1074CrossRefGoogle Scholar
  26. Mac S, da Silva SR, Sander B (2019) The economic burden of Lyme disease and the cost-effectiveness of Lyme disease interventions: a scoping review. PLoS One 14:e0210280CrossRefGoogle Scholar
  27. McMullan L et al (2012) A new phlebovirus associated with severe febrile illness in Missouri. N Engl J Med 367:834–841CrossRefGoogle Scholar
  28. Mitchell EA, Williamson PC, Billingsley PM, Seals JP, Ferguson EE, Allen MS (2016) Frequency and distribution of Rickettsiae, Borreliae, and Ehrlichiae detected in human-parasitizing ticks, Texas, USA. Emerg Infect Dis 22:312CrossRefGoogle Scholar
  29. Morrison LW, Korzukhin MD, Porter SD (2005) Predicted range expansion of the invasive fire ant, Solenopsis invicta, in the eastern United States based on the VEMAP global warming scenario. Divers Distrib 11:199–204CrossRefGoogle Scholar
  30. Mwangi EN, Dipeolu OO, Newson RM, Kaaya GP, Hassan SM (1991) Predators, parasitoids and pathogens of ticks: a review. Biocontrol Sci Tech 1:147–156CrossRefGoogle Scholar
  31. Nieto NC, Porter WT, Wachara JC, Lowrey TJ, Martin L, Motyka PJ, Salkeld DJ (2018) Using citizen science to describe the prevalence and distribution of tick bite and exposure to tick-borne diseases in the United States. PLoS One 13:e0199644CrossRefGoogle Scholar
  32. Paddock CD, Childs JE (2003) Ehrlichia chaffeensis: a prototypical emerging pathogen. Clin Microbiol Rev 16:37–64CrossRefGoogle Scholar
  33. Porter SD, Williams DF, Patterson RS, Fowler HG (1997) Intercontinental differences in the abundance of Solenopsis fire ants (Hymenoptera: Formicidae): escape from natural enemies? Environ Entomol 26:373–384CrossRefGoogle Scholar
  34. Pritt B et al (2011) Emergence of a new pathogenic Ehrlichia species, Wisconsin and Minnesota, 2009. N Engl J Med 365:422–429CrossRefGoogle Scholar
  35. R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  36. Randolph S (2004) Tick ecology: processes and patterns behind the epidemiological risk posed by ixodid ticks as vectors. Parasitology 129:S37–S65CrossRefGoogle Scholar
  37. Rashid T, Chen J, Vogt JT, McLeod PJ (2013) Arthropod prey of imported fire ants (Hymenoptera: Formicidae) in Mississippi sweetpotato fields. Insect Science 20:467–471CrossRefGoogle Scholar
  38. Samish M, Alekseev E (2001) Arthropods as predators of ticks (Ixodoidea). J Med Entomol 38:1–11CrossRefGoogle Scholar
  39. Samish M, Rehacek J (1999) Pathogens and predators of ticks and their potential in biological control. Annu Rev Entomol 44:159–182CrossRefGoogle Scholar
  40. Sayler K et al (2016) Prevalence of tick-borne pathogens in host-seeking Amblyomma americanum (Acari: Ixodidae) and Odocoileus virginianus (Artiodactyla: Cervidae) in Florida. J Med Entomol 53:949–956CrossRefGoogle Scholar
  41. Schmitz OJ, Beckerman AP, O’Brien KM (1997) Behaviorally mediated trophic cascades: effects of predation risk on food web interactions. Ecology 78:1388–1399CrossRefGoogle Scholar
  42. Teel P, Ketchum H, Mock D, Wright R, Strey O (2010) The Gulf Coast tick: a review of the life history, ecology, distribution, and emergence as an arthropod of medical and veterinary importance. J Med Entomol 47:707–722CrossRefGoogle Scholar
  43. Teel PD, Hopkins SW, Donahue WA, Strey OF (1998) Population dynamics of immature Amblyomma maculatum (Acari: Ixodidae) and other ectoparasites on meadowlarks and northern bobwhite quail resident to the coastal prairie of Texas. J Med Entomol 35:483–488CrossRefGoogle Scholar
  44. Trussell G, Ewanchuk P, Bertness M (2002) Field evidence of trait-mediated indirect interactions in a rocky intertidal food web. Ecol Lett 5:241–245CrossRefGoogle Scholar
  45. Vinson SB (1997) Invasion of the red imported fire ant (Hymenoptera: Formicidae): spread, biology, and impact. Am Entomol 43:23–39CrossRefGoogle Scholar
  46. Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer, ‎DordrechtCrossRefGoogle Scholar
  47. Wilder S, Eubanks M (2010) Extrafloral nectar content alters foraging preferences of a predatory ant. Biol Lett 6:177–179CrossRefGoogle Scholar
  48. Zeileis A, Kleiber C, Jackman S (2008) Regression models for count data in. R J Stat Softw 27:1–25Google Scholar
  49. Zhang X, Meltzer MI, Peña CA, Hopkins AB, Wroth L, Fix AD (2006) Economic impact of Lyme disease. Emerg Infect Dis 12:653CrossRefGoogle Scholar
  50. Zingg S, Dolle P, Voordouw MJ, Kern M (2018) The negative effect of wood ant presence on tick abundance. Parasites Vectors 11:164CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of EntomologyTexas A&M UniversityCollege StationUSA
  2. 2.Department of Wildlife and Fisheries SciencesTexas A&M UniversityCollege StationUSA
  3. 3.Department of Veterinary Integrative BiosciencesTexas A&M UniversityCollege StationUSA
  4. 4.Department of Biology and Museum of Southwestern BiologyUniversity of New MexicoAlbuquerqueUSA

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