1887

Abstract

The Argentine ant (, Mayr) is a highly invasive species. Recently, several RNA viruses have been identified in samples from invasive Argentine ant colonies. Using quantitative PCR, we investigated variation in the levels of these viruses in the main European supercolony over the course of a year. We discovered that virus prevalence and amounts of viral RNA were affected by season and caste: ants had more virus types during warm versus cold months, and queens had more virus types and higher virus prevalence than did workers or males. This seasonal variation was largely due to the appearance of positive-strand RNA viruses in the summer and their subsequent disappearance in the winter. The prevalences of positive-strand RNA viruses were positively correlated with worker foraging activity. We hypothesise that during warmer months, ants are more active and more numerous and, as a result, they have more conspecific and heterospecific interactions that promote virus transmission.

Funding
This study was supported by the:
  • Koneen Säätiö (Award 001)
    • Principle Award Recipient: Jaana Jurvansuu
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2020-01-27
2024-04-20
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References

  1. Schmid-Hempel P. Parasites in Social Insects Princeton, New Jersey: Princeton University Press; 1998
    [Google Scholar]
  2. Boomsma JJ, Schmid-Hempel P, Hughes WOH. Life histories and parasite pressure across the major groups of social insects. In Fellowes M, Holloway J, Rolff J. (editors) Insect Evolutionary Ecology: Proceedings of the Royal Entomological Society’s 22nd Symposium Reading, UK: CABI publishing; 2005 pp 139–175
    [Google Scholar]
  3. Valles SM, Oi DH, Yu F, Tan X-X, Buss EA. Metatranscriptomics and pyrosequencing facilitate discovery of potential viral natural enemies of the invasive Caribbean crazy ant, Nylanderia pubens. PLoS One 7:0031828 [View Article]
    [Google Scholar]
  4. Sébastien A, Lester PJ, Hall RJ, Wang J, Moore NE et al. Invasive ants carry novel viruses in their new range and form reservoirs for a honeybee pathogen. Biol Lett 2015; 11:20150610 [View Article]
    [Google Scholar]
  5. Tragust S, Feldhaar H, Espadaler X, Pedersen JS. Rapid increase of the parasitic fungus Laboulbenia formicarum in supercolonies of the invasive garden ant Lasius neglectus. Biol Invasions 2015; 17:2795–2801 [View Article]
    [Google Scholar]
  6. Plowes RM, Becnel JJ, LeBrun EG, Oi DH, Valles SM et al. Myrmecomorba nylanderiae gen. et sp. nov., a microsporidian parasite of the tawny crazy ant Nylanderia fulva. J Invertebr Pathol 2015; 129:45–56 [View Article]
    [Google Scholar]
  7. Gruber MAM, Cooling M, Baty JW, Buckley K, Friedlander A et al. Single-Stranded RNA viruses infecting the invasive Argentine ant, Linepithema humile. Sci Rep 2017; 7:3304 [View Article]
    [Google Scholar]
  8. Viljakainen L, Holmberg I, Abril S, Jurvansuu J. Viruses of invasive Argentine ants from the European main supercolony: characterization, interactions and evolution. J Gen Virol 2018; 99:1129–1140 [View Article]
    [Google Scholar]
  9. Holway DA, Lach L, Suarez AV, Tsutsui ND, Case TJ. The causes and consequences of ant invasions. Annu Rev Ecol Syst 2002; 33:181–233 [View Article]
    [Google Scholar]
  10. Passera L. Characteristics of tramp species. In Williams D. editor Exotic Ants: Biology, Impact, and Control of Introduced Species Boulder, CO: Westview Press; 1994 pp 23–43
    [Google Scholar]
  11. Bertelsmeier C, Ollier S, Liebhold A, Keller L. Recent human history governs global ant invasion dynamics. Nat Ecol Evol 2017; 1:0184 [View Article]
    [Google Scholar]
  12. Fournier A, Penone C, Pennino MG, Courchamp F. Predicting future invaders and future invasions. Proc Natl Acad Sci U S A 2019; 116:7905–7910 [View Article]
    [Google Scholar]
  13. Ugelvig LV, Cremer S. Effects of social immunity and unicoloniality on host-parasite interactions in invasive insect societies. Funct Ecol 2012; 26:1300–1312 [View Article]
    [Google Scholar]
  14. Lester PJ, Gruber MAM, Booms GMAM. Booms, busts and population collapses in invasive ants. Biol Invasions 2016; 18:3091–3101 [View Article]
    [Google Scholar]
  15. Hsu H-W, Chiu M-C, Lee C-C, Lee C-Y, Yang C-CS. The association between virus prevalence and Intercolonial aggression levels in the yellow crazy ant, Anoplolepis Gracilipes (Jerdon). Insects 2019; 10:436 [View Article]
    [Google Scholar]
  16. Lowe S, Browne M, Boudjelas S, De Poorter M. 100 of the world’s worst invasive alien species. A selection from the Global Invasive Species Database. Invasive Species Spec Gr a Spec Gr Species Surviv Comm World Conserv Union 2000; 12:
    [Google Scholar]
  17. Suarez A V, Tsutsui ND. The evolutionary consequences of biological invasions. Mol Ecol 2008; 17:351–360 [View Article]
    [Google Scholar]
  18. Wetterer JK, Wild AL, Suarez A V, Roura-Pascual N, Espadaler X. Worldwide spread of the Argentine ant, Linepithema humile (Hymenoptera: Formicidae). Myrmecological News 2009; 12:187–194
    [Google Scholar]
  19. Cammell ME, Way MJ, Paiva MR. Diversity and structure of ant communities associated with oak, pine, Eucalyptus and arable habitats in Portugal. Insectes Soc 1996; 43:37–46 [View Article]
    [Google Scholar]
  20. Human KG, Gordon DM. Effects of Argentine ants on invertebrate biodiversity in northern California. Conservation Biology 1997; 11:1242–1248 [View Article]
    [Google Scholar]
  21. Holway DA. Effect of Argentine ant invasions on ground-dwelling arthropods in northern California riparian woodlands. Oecologia 1998; 116:252–258 [View Article]
    [Google Scholar]
  22. Gómez C, Oliveras J. Can the Argentine ant (Linepithema humile Mayr) replace native ants in myrmecochory?. Acta Oecologica 2003; 24:47–53 [View Article]
    [Google Scholar]
  23. Gómez C, Pons P, Bas JM. Effects of the Argentine ant Linepithema humile on seed dispersal and seedling emergence of Rhamnus alaternus . Ecography 2003; 26:532–538 [View Article]
    [Google Scholar]
  24. Oliveras J, Bas JM, Casellas D, Gómez C. Numerical dominance of the Argentine ant vs native ants and consequences on soil resource searching in Mediterranean cork-oak forests (Hymenoptera: Formicidae). Sociobiology 2006; 45:1–16
    [Google Scholar]
  25. Lach L. Invasive ants: unwanted partners in Ant-Plant interactions?. Annals of the Missouri Botanical Garden 2003; 90:91–108 [View Article]
    [Google Scholar]
  26. Blancafort X, Gómez C. Consequences of the Argentine ant, Linepithema humile (Mayr), invasion on pollination of Euphorbia characias (L.) (Euphorbiaceae). Acta Oecologica 2005; 28:49–55 [View Article]
    [Google Scholar]
  27. Blancafort X, Gómez C. Downfall of pollen carriage by ants after Argentine ant invasion in two Mediterranean Euphorbia species. Vie Milieu 2006; 56:243–246
    [Google Scholar]
  28. Cole FR, Medeiros AC, Loope LL, Zuehlke WW. Effects of the Argentine ant on arthropod fauna of Hawaiian high-elevation Shrubland. Ecology 1992; 73:1313–1322 [View Article]
    [Google Scholar]
  29. Human KG, Gordon DM. Exploitation and interference competition between the invasive Argentine ant, Linepithema humile, and native ant species. Oecologia 1996; 105:405–412 [View Article]
    [Google Scholar]
  30. Suarez AV, Bolger DT, Case TJ. Effects of fragmentation and invasion on native ant communities in coastal southern California. Ecology 1998; 79:2041–2056 [View Article]
    [Google Scholar]
  31. Bolger DT, Suarez AV, Crooks KR, Morrison SA, Case TJ. Arthropods in urban habitat fragments in southern California: area, age, and edge effects. Ecol Appl 2000; 10:1230–1248 [View Article]
    [Google Scholar]
  32. Suarez AV, Holway DA, Case TJ. Patterns of spread in biological invasions dominated by long-distance jump dispersal: insights from argentine ants. Proc Natl Acad Sci U S A 2001; 98:1095–1100 [View Article]
    [Google Scholar]
  33. Walters AC, MacKay DA. Importance of large colony size for successful invasion by Argentine ants (Hymenoptera: Formicidae): evidence for biotic resistance by native ants. Austral Ecol 2005; 30:395–406 [View Article]
    [Google Scholar]
  34. Daane KM, Sime KR, Fallon J, Cooper ML. Impacts of Argentine ants on mealybugs and their natural enemies in California’s coastal vineyards. Ecol Entomol 2007; 32:583–596 [View Article]
    [Google Scholar]
  35. Estany-Tigerström D, Bas JM, Pons P. Does Argentine ant invasion affect prey availability for foliage-gleaning birds?. Biol Invasions 2010; 12:827–839 [View Article]
    [Google Scholar]
  36. Alvarez-Blanco P, Caut S, Cerdá X, Angulo E. Native predators living in invaded areas: responses of terrestrial amphibian species to an Argentine ant invasion. Oecologia 2017; 185:95–106 [View Article]
    [Google Scholar]
  37. Fisher RN, Suarez AV, Case TJ. Spatial patterns in the abundance of the coastal horned lizard. Conservation Biology 2002; 16:205–215 [View Article]
    [Google Scholar]
  38. Suarez AV, Case TJ. Bottom-Up effects on persistence of a specialist predator: ant invasions and horned lizards. Ecological Applications 2002; 12:291–298 [View Article]
    [Google Scholar]
  39. Laakkonen J, Fisher RN, Case TJ. Effect of land cover, habitat fragmentation and ant colonies on the distribution and abundance of shrews in southern California. J Anim Ecol 2001; 70:776–788 [View Article]
    [Google Scholar]
  40. Stanley MC, Ward DF. Impacts of Argentine ants on invertebrate communities with below-ground consequences. Biodivers Conserv 2012; 21:2653–2669 [View Article]
    [Google Scholar]
  41. Davis P, van Schagen J. Effective control of pest ants. West Aust J Agric 1993; 34:92–95
    [Google Scholar]
  42. Maria S, Obispo SL, Argentine T. To control mealybugs, stop honeydew-seeking ants. Calif Agric 1989; 45:26–28
    [Google Scholar]
  43. Vega SJ, Rust MK. The Argentine ant - A significant invasive species in agricultural, urban and natural environments. Sociobiology 2000; 37:3–25
    [Google Scholar]
  44. Hölldobler B, Wilson EO. The ants; 1990
  45. Chapman RE, Bourke AFG. The influence of sociality on the conservation biology of social insects. Ecol Lett 2001; 4:650–662 [View Article]
    [Google Scholar]
  46. Giraud T, Pedersen JS, Keller L. Evolution of supercolonies: the Argentine ants of southern Europe. Proc Natl Acad Sci U S A 2002; 99:6075–6079 [View Article]
    [Google Scholar]
  47. Heller NE, Sanders NJ, Gordon DM. Linking temporal and spatial scales in the study of an Argentine ant invasion. Biol Invasions 2006; 8:501–507 [View Article]
    [Google Scholar]
  48. Diaz M, Abril S, Enríquez ML, Gómez C. Assessment of the Argentine ant invasion management by means of manual removal of winter nests in mixed cork oak and pine forests. Biol Invasions 2014; 16:315–327 [View Article]
    [Google Scholar]
  49. Heller NE, Gordon DM. Seasonal spatial dynamics and causes of nest movement in colonies of the invasive Argentine ant (Linepithema humile). Ecol Entomol 2006; 31:499–510 [View Article]
    [Google Scholar]
  50. Abril S, Oliveras J, Gómez C. Effect of seasonal dynamics on Queen densities of the Argentine ant (Linepithema humile) (Hymenoptera: Formicidae) in an invaded natural area of the Ne Iberian Peninsula. Sociobiology 2008; 51:1–10
    [Google Scholar]
  51. Keller L, Passera LUC, Suzzoni J-P. Queen execution in the Argentine ant, Iridomyrmex humilis. Physiol Entomol 1989; 14:157–163 [View Article]
    [Google Scholar]
  52. Markin GP. The seasonal life cycle of the Argentine ant, Iridomyrmex humilis (Hymenoptera: Formicidae), in southern California. Ann Entomol Soc Am 1970; 63:1238–1242 [View Article]
    [Google Scholar]
  53. Reuter M, Balloux F, Lehmann L, Keller L. Kin structure and Queen execution in the Argentine ant Linepithema humile. J Evol Biol 2001; 14:954–958 [View Article]
    [Google Scholar]
  54. Abril S, Oliveras J, Gómez C. Foraging activity and dietary spectrum of the Argentine ant (Hymenoptera: Formicidae) in invaded natural areas of the Northeast Iberian Peninsula. Environ Entomol 2007; 36:1166–1173 [View Article]
    [Google Scholar]
  55. Runckel C, Flenniken ML, Engel JC, Ruby JG, Ganem D et al. Temporal analysis of the honey bee microbiome reveals four novel viruses and seasonal prevalence of known viruses, Nosema, and Crithidia. PLoS One 2011; 6:e20656 [View Article]
    [Google Scholar]
  56. D'Alvise P, Seeburger V, Gihring K, Kieboom M, Hasselmann M. Seasonal dynamics and co‐occurrence patterns of honey bee pathogens revealed by high‐throughput RT‐qPCR analysis. Ecol Evol 2019; 9:10241–10252 [View Article]
    [Google Scholar]
  57. Dalmon A, Peruzzi M, Le Conte Y, Alaux C, Pioz M. Temperature-Driven changes in viral loads in the honey bee Apis mellifera. J Invertebr Pathol 2019; 160:87–94 [View Article]
    [Google Scholar]
  58. Valles SM, Strong CA, Dang PM, Hunter WB, Pereira RM et al. A picorna-like virus from the red imported fire ant, Solenopsis invicta: initial discovery, genome sequence, and characterization. Virology 2004; 328:151–157 [View Article]
    [Google Scholar]
  59. Valles SM, Strong CA, Oi DH, Porter SD, Pereira RM et al. Phenology, distribution, and host specificity of Solenopsis invicta virus-1. J Invertebr Pathol 2007; 96:18–27 [View Article]
    [Google Scholar]
  60. Valles SM, Oi DH, Porter SD. Seasonal variation and the co-occurrence of four pathogens and a group of parasites among monogyne and polygyne fire ant colonies. Biological Control 2010; 54:342–348 [View Article]
    [Google Scholar]
  61. Valles SM, Porter SD. Influence of temperature on the pathogenicity of Solenopsis invicta virus 3. J Invertebr Pathol 2019; 166:107217 [View Article]
    [Google Scholar]
  62. Amiri E, Meixner M, Nielsen SL, Kryger P. Four categories of viral infection describe the health status of honey bee colonies. PLoS One 2015; 10:e0140272 [View Article]
    [Google Scholar]
  63. Francis RM, Nielsen SL, Kryger P. Patterns of viral infection in honey bee queens. J Gen Virol 2013; 94:668–676 [View Article]
    [Google Scholar]
  64. Retschnig G, Williams GR, Mehmann MM, Yañez O, de Miranda JR et al. Sex-Specific differences in pathogen susceptibility in honey bees (Apis mellifera). PLoS One 2014; 9:e85261 [View Article]
    [Google Scholar]
  65. Viljakainen L, Jurvansuu J, Holmberg I, Pamminger T, Erler S et al. Social environment affects the transcriptomic response to bacteria in ant queens. Ecol Evol 2018; 8:11031–11070 [View Article]
    [Google Scholar]
  66. Lester PJ, Buick KH, Baty JW, Felden A, Haywood J. Different bacterial and viral pathogens trigger distinct immune responses in a globally invasive ant. Sci Rep 2019; 9:5780 [View Article]
    [Google Scholar]
  67. Heller NE, Ingram KK, Gordon DM. Nest connectivity and colony structure in unicolonial Argentine ants. Insectes Soc 2008; 55:397–403 [View Article]
    [Google Scholar]
  68. Markin GP. Foraging behavior of the Argentine ant in a California citrus Grove1. J Econ Entomol 1970; 63:740–744 [View Article]
    [Google Scholar]
  69. Chen Y, Evans J, Feldlaufer M. Horizontal and vertical transmission of viruses in the honey bee, Apis mellifera. J Invertebr Pathol 2006; 92:152–159 [View Article]
    [Google Scholar]
  70. Lequime S, Paul RE, Lambrechts L. Determinants of arbovirus vertical transmission in mosquitoes. PLoS Pathog 2016; 12:e1005548 [View Article]
    [Google Scholar]
  71. Markin GP. Food distribution within laboratory colonies of the argentine ant,Tridomyrmex humilis (Mayr). Insectes Soc 1970; 17:127–157 [View Article]
    [Google Scholar]
  72. Reber A, Chapuisat M. No evidence for immune priming in ants exposed to a fungal pathogen. PLoS One 2012; 7:e35372 [View Article]
    [Google Scholar]
  73. Gálvez D, Chapuisat M. Immune priming and pathogen resistance in ant queens. Ecol Evol 2014; 4:1761–1767 [View Article]
    [Google Scholar]
  74. Wang M-R, Cui Z-H, Li J-W, Hao X-Y, Zhao L et al. In vitro thermotherapy-based methods for plant virus eradication. Plant Methods 2018; 14:87 [View Article]
    [Google Scholar]
  75. Michael H. Mycoviruses: viruses that infect fungi. Adv Virus Res 1978; 22:2–46
    [Google Scholar]
  76. Park AW, Cleveland CA, Dallas TADA, Corn JL. Vector species richness increases haemorrhagic disease prevalence through functional diversity modulating the duration of seasonal transmission. Parasitology 2016; 143:874–879 [View Article]
    [Google Scholar]
  77. Geoghegan JL, Walker PJ, Duchemin J-B, Jeanne I, Holmes EC. Seasonal drivers of the epidemiology of arthropod-borne viruses in Australia. PLoS Negl Trop Dis 2014; 8:e3325 [View Article]
    [Google Scholar]
  78. Bailey L, Ball B V, Perry JN. The prevalence of viruses of honey bees in Britain. Ann Applied Biology 1981; 97:109–118 [View Article]
    [Google Scholar]
  79. Francis RM, Nielsen SL, Kryger P. Varroa-Virus interaction in collapsing honey bee colonies. PLoS One 2013; 8:e57540 [View Article]
    [Google Scholar]
  80. Tentcheva D, Gauthier L, Zappulla N, Dainat B, Cousserans F et al. Prevalence and seasonal variations of six bee viruses in Apis mellifera L. and Varroa destructor mite populations in France. Appl Environ Microbiol 2004; 70:7185–7191 [View Article]
    [Google Scholar]
  81. Porrini C, Mutinelli F, Bortolotti L, Granato A, Laurenson L et al. The status of honey bee health in Italy: results from the nationwide bee monitoring network. PLoS One 2016; 11:e0155411 [View Article]
    [Google Scholar]
  82. Shen M, Yang X, Cox-Foster D, Cui L. The role of varroa mites in infections of Kashmir bee virus (KBV) and deformed wing virus (DWV) in honey bees. Virology 2005; 342:141–149 [View Article]
    [Google Scholar]
  83. Tantillo G, Bottaro M, Di Pinto A, Martella V, Di Pinto P et al. Virus infections of honeybees Apis mellifera. Ital J Food Safety 2015; 4:5364 [View Article]
    [Google Scholar]
  84. Benois A, Lafont JP, Marro JP. Incidence des facteurs écologiques sur le cycle annuel et l'activité saisonnière de la fourmi d'Argentine,Iridomyrmex humilis Mayr (Hymenoptera, Formicidae), dans la région d'Antibes. Insectes Soc 1973; 20:267–295 [View Article]
    [Google Scholar]
  85. Antúnez K, Anido M, Branchiccela B, Harriet J, Campa J et al. Seasonal variation of honeybee pathogens and its association with pollen diversity in Uruguay. Microb Ecol 2015; 70:522–533 [View Article]
    [Google Scholar]
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