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.
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References
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 10:553–563
Banks WA et al (1981) Techniques for collecting, rearing, and handling imported fire ants. USDA SEA AATS-S-21
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 12:163–170
Beati L et al (2013) Amblyomma cajennense (Fabricius, 1787)(Acari: Ixodidae), the Cayenne tick: phylogeography and evidence for allopatric speciation. BMC Evol Biol 13:267
Bock R, Jackson L, De Vos A, Jorgensen W (2004) Babesiosis of cattle. Parasitology 129:S247–S269
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–e0133868
Burns EC, Melancon DG (1977) Effect of imported fire ant (Hymenoptera: Formicidae) invasion on lone star tick (Acarina: Ixodidae) populations. J Med Entomol 14:247–249
Burtis J, Pflueger C (2017) Interactions between soil-dwelling arthropod predators and Ixodes scapularis under laboratory and field conditions. Ecosphere 8:e01914
Cassill DL, Tschinkel WR (1999) Regulation of diet in the fire ant, Solenopsis invicta. J Insect Behav 12:307–328
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 12:20160463
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 6:238–246
Dawes-Gromadzki TZ, Bull CM (1997) Ant predation on different life stages of two Australian ticks. Exp Appl Acarol 21:109–115
Eisen R, Eisen L (2018) The blacklegged tick, Ixodes scapularis: an increasing public health concern. Trends Parasitol 34:295–309
Finke DL (2012) Contrasting the consumptive and non-consumptive cascading effects of natural enemies on vector-borne pathogens. Entomol Exp Appl 144:45–55
Fischhoff IR, Burtis JC, Keesing F, Ostfeld RS (2018) Tritrophic interactions between a fungal pathogen, a spider predator, and the blacklegged tick. Ecol Evol 8:7824–7834
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 9:158–162
Fox J, Weisberg S (2018) An R companion to applied regression. Sage, Thousand Oaks
Gage KL, Burkot TR, Eisen RJ, Hayes EB (2008) Climate and vectorborne diseases. Am J Prev Med 35:436–450
Hawlena D, Pérez Mellado V (2009) Change your diet or die: predator-induced shifts in insectivorous lizard feeding ecology. Oecologia 161:411–419
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 159:183–193
Keesing F et al (2009) Hosts as ecological traps for the vector of Lyme disease. Proc R Soc B 276:3911–3919
Krause P et al (2013) Human Borrelia miyamotoi infection in the United States. N Engl J Med 368:291–293
Lenth R (2018) emmeans: estimated marginal means, aka least-squares means. R package version 1.4. https://CRAN.R-project.org/package=emmeans
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 26:484–498
Long EY, Finke DL (2015) Predators indirectly reduce the prevalence of an insect-vectored plant pathogen independent of predator diversity. Oecologia 177:1067–1074
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:e0210280
McMullan L et al (2012) A new phlebovirus associated with severe febrile illness in Missouri. N Engl J Med 367:834–841
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 22:312
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 11:199–204
Mwangi EN, Dipeolu OO, Newson RM, Kaaya GP, Hassan SM (1991) Predators, parasitoids and pathogens of ticks: a review. Biocontrol Sci Tech 1:147–156
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:e0199644
Paddock CD, Childs JE (2003) Ehrlichia chaffeensis: a prototypical emerging pathogen. Clin Microbiol Rev 16:37–64
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 26:373–384
Pritt B et al (2011) Emergence of a new pathogenic Ehrlichia species, Wisconsin and Minnesota, 2009. N Engl J Med 365:422–429
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Randolph S (2004) Tick ecology: processes and patterns behind the epidemiological risk posed by ixodid ticks as vectors. Parasitology 129:S37–S65
Rashid T, Chen J, Vogt JT, McLeod PJ (2013) Arthropod prey of imported fire ants (Hymenoptera: Formicidae) in Mississippi sweetpotato fields. Insect Science 20:467–471
Samish M, Alekseev E (2001) Arthropods as predators of ticks (Ixodoidea). J Med Entomol 38:1–11
Samish M, Rehacek J (1999) Pathogens and predators of ticks and their potential in biological control. Annu Rev Entomol 44:159–182
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 53:949–956
Schmitz OJ, Beckerman AP, O’Brien KM (1997) Behaviorally mediated trophic cascades: effects of predation risk on food web interactions. Ecology 78:1388–1399
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 47:707–722
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 35:483–488
Trussell G, Ewanchuk P, Bertness M (2002) Field evidence of trait-mediated indirect interactions in a rocky intertidal food web. Ecol Lett 5:241–245
Vinson SB (1997) Invasion of the red imported fire ant (Hymenoptera: Formicidae): spread, biology, and impact. Am Entomol 43:23–39
Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer, Dordrecht
Wilder S, Eubanks M (2010) Extrafloral nectar content alters foraging preferences of a predatory ant. Biol Lett 6:177–179
Zeileis A, Kleiber C, Jackman S (2008) Regression models for count data in. R J Stat Softw 27:1–25
Zhang X, Meltzer MI, Peña CA, Hopkins AB, Wroth L, Fix AD (2006) Economic impact of Lyme disease. Emerg Infect Dis 12:653
Zingg S, Dolle P, Voordouw MJ, Kern M (2018) The negative effect of wood ant presence on tick abundance. Parasites Vectors 11:164
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.
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Kjeldgaard, M.K., Takano, O.M., Bockoven, A.A. et al. Red imported fire ant (Solenopsis invicta) aggression influences the behavior of three hard tick species. Exp Appl Acarol 79, 87–97 (2019). https://doi.org/10.1007/s10493-019-00419-8
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DOI: https://doi.org/10.1007/s10493-019-00419-8