, Volume 185, Issue 1, pp 95–106 | Cite as

Native predators living in invaded areas: responses of terrestrial amphibian species to an Argentine ant invasion

  • Paloma Alvarez-Blanco
  • Stephane Caut
  • Xim Cerdá
  • Elena Angulo
Behavioral ecology – original research


Predator–prey interactions play a key role in the success and impacts of invasive species. However, the effects of invasive preys on native predators have been poorly studied. Here, we first reviewed hypotheses describing potential relationships between native predators and invasive preys. Second, we examined how an invasive prey, the Argentine ant (Linepithema humile), affected a native terrestrial amphibian community. In the field, we looked at the structure of the amphibian community in invaded versus uninvaded areas and characterized amphibian trophic ecology. The amphibian community sampled seemed to show a species-dependent response in abundance to invasion: adults of the natterjack toad (Bufo calamita), the species demonstrating the highest degree of ant specialization, were less abundant in invaded areas. Although available ant biomass was significantly greater in invaded than in uninvaded areas (only Argentine ants occurred in the former), amphibians consumed relatively fewer ants in invaded areas. In the lab, we quantified amphibian consumption of Argentine ants versus native ants and assessed whether consumption patterns could have been influenced by prior exposure to the invader. The lab experiments corroborated the field results: amphibians preferred native ants over Argentine ants, and prior exposure did not influence consumption. Differences in preference explained why amphibians consumed fewer Argentine ants in spite of their greater relative availability; they might also explain why the most ant-specialized amphibians seemed to avoid invaded areas. Our results suggest the importance to account for predator feeding capacities and dietary ranges to understand the effects of invasive species at higher trophic levels.


Biotic resistance Enemy release Exotic prey naïveté Invasive prey Linepithema humile 



We thanks R. Arribas, O. Blight, E. Guirlet, N. Guirlet, and P. Serpe for their help with sampling and C. Díaz-Paniagua, I. Gómez-Mestre and R. Boulay for their scientific input.

Author contribution statement

EA, XC and SC conceived the ideas. SC and EA collected the data in the field and SC prepared the samples for isotopic analyses. PA-B and EA conducted the laboratory experiments and analyzed the data. PA-B led the writing of the manuscript and all the authors revised it.

Compliance with ethical standards


This study was funded by the Consolider MONTES project (CSD 2008-00040); the Spanish Ministry of Economy and Competitiveness and FEDER (CGL2012-36181, CGL2013-43660-P); and fellowships to P.A.-B. (FPI program, CGL2012-36181), to S.C. (the Juan de la Cierva) and E.A. (Ramón y Cajal).

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable institutional and national guidelines for the care and use of animals were followed.

Supplementary material

442_2017_3929_MOESM1_ESM.doc (270 kb)
Supplementary material 1 (DOC 270 kb)


  1. Angulo E, Boulay R, Rodrigo A, Retana J, Cerda X (2007) Efecto de una especie invasora, Linepithema humile, la hormiga argentina, sobre la biodiversidad del Parque Nacional de Doñana (Huelva): descripción de las interacciones con las hormigas nativas. In: Ramírez L, Asensio B (eds) Investigación en Parques Nacionales: 2003–2006. Ministerio de Medio Ambiente, Madrid, pp 161–179Google Scholar
  2. Angulo E, Caut S, Cerdá X (2011) Scavenging in Mediterranean ecosystems: effect of the invasive Argentine ant. Biol Invasions 13:1183–1194CrossRefGoogle Scholar
  3. Arnan X, Cerdá X, Retana J (2014) Ant functional responses along environmental gradients. J Anim Ecol 83:1398–1408CrossRefPubMedGoogle Scholar
  4. Banks PB, Dickman CR (2007) Alien predation and the effects of multiple levels of prey naiveté. Trends Ecol Evolut 22(5):229–230CrossRefGoogle Scholar
  5. Bytheway JP, Price CJ, Banks PB (2016) Deadly intentions: naïve introduced foxes show rapid attraction to odour cues of an unfamiliar native prey. Sci Rep 6:30078CrossRefPubMedPubMedCentralGoogle Scholar
  6. Cabrera-Guzmán E, Crossland MR, Shine R (2012) Predation on the eggs and larvae of invasive cane toads (Rhinella marina) by native aquatic invertebrates in tropical Australia. Biol Conserv 153:1–9CrossRefGoogle Scholar
  7. Callaway RM, Ridenour WM (2004) Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Environ 2(8):436–443CrossRefGoogle Scholar
  8. Carlsson NO, Sarnelle O, Strayer DL (2009) Native predators and exotic prey—an acquired taste? Front Ecol Environ 7:525–532CrossRefGoogle Scholar
  9. Carpintero S, Reyes-López J, Arias de Reyna L (2005) Impact of Argentine ants (Linepithema humile) on an arboreal ant community in Doñana National Park, Spain. Biodivers Conserv 14:151–163CrossRefGoogle Scholar
  10. Carpintero S, Retana J, Cerdá X, Reyes-López J, Arias de Reyna L (2007) Exploitative strategies of the invasive Argentine ant (Linepithema humile) and native ant species in a southern Spanish pine forest. Environ Entomol 36:1100–1111CrossRefPubMedGoogle Scholar
  11. Carthey AJ, Banks PB (2014) Naïveté in novel ecological interactions: lessons from theory and experimental evidence. Biol Rev 89(4):932–949CrossRefPubMedGoogle Scholar
  12. Catford JA, Jansson R, Nilsson C (2009) Reducing redundancy in invasion ecology by integrating hypotheses into a single theoretical framework. Divers Distrib 15(1):22–40CrossRefGoogle Scholar
  13. Caut S, Angulo E, Courchamp F (2008) Dietary shift of an invasive predator: rats, seabirds and sea turtles. J Appl Ecol 45:428–437CrossRefPubMedPubMedCentralGoogle Scholar
  14. Caut S, Angulo E, Courchamp F (2009) Variation in discrimination factors (∆15N and ∆13C): the effect of diet isotopic values and applications for diet reconstruction. J Appl Ecol 46(2):443–453CrossRefGoogle Scholar
  15. Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7:721–733CrossRefGoogle Scholar
  16. Díaz-Paniagua C, Gómez-Rogríguez C, Portheault, de Vries, W (2005) Los anfibios de Doñana. Organismo Autónomo De Parques Nacionales, Ministerio de Medio Ambiente, Estación Biológica de Doñana, SpainGoogle Scholar
  17. Díaz-Paniagua C, Fernández-Zamudio R, Florencio M, García-Murillo P, Gómez-Rodríguez C, Portheault A, Serrano L, Siljeström P (2010) Temporay ponds from Doñana National Park: a system of natural habitats for the preservation of aquatic flora and fauna. Limnetica 29(1):41–58Google Scholar
  18. Estany-Tigerström D, Bas JM, Pons P (2010) Does Argentine ant invasion affect prey availability for foliage-gleaning birds? Biol Invasions 12:827–839CrossRefGoogle Scholar
  19. Estany-Tigerström D, Bas JM, Clavero M, Pons P (2013) Is the blue tit falling into an ecological trap in Argentine ant invaded forests? Biol Invasions 15:2013–2027CrossRefGoogle Scholar
  20. Fisher RN, Suarez AV, Case TJ (2002) Spatial patterns in the abundance of the coastal horned lizard. Conserv Biol 16:205–215CrossRefGoogle Scholar
  21. Glenn S, Holway D (2008) Consumption of introduced prey by native predators: Argentine ants and pit-building ant lions. Biol Invasions 10:273–280CrossRefGoogle Scholar
  22. Gordon DM, Heller NE (2014) The invasive Argentine ant Linepithema humile (Hymenoptera: Formicidae) in Northern California reserves: from foraging behavior to local spread. Mirmecol News 19:103–110Google Scholar
  23. Gove AD, Majer JD, Rico-Gray V (2009) Ant assemblages in isolated trees are more sensitive to species loss and replacement than their woodland counterparts. Basic Appl Ecol 10(2):187–195CrossRefGoogle Scholar
  24. Heller NE, Ingram KK, Gordon DM (2008) Nest connectivity and colony structure in unicolonial Argentine ants. Insect Soc 55(4):397–403. doi: 10.1007/s00040-008-1019-0 CrossRefGoogle Scholar
  25. Hoffmann M, Hilton-Taylor C, Angulo A, Böhm M, Brooks TM, Butchart SH et al (2010) The impact of conservation on the status of the world’s vertebrates. Science 330:1503–1509CrossRefPubMedGoogle Scholar
  26. Holway DA, Suarez AV (2006) Homogenization of ant communities in mediterranean California: the effects of urbanization and invasion. Biol Conserv 127(3):319–326CrossRefGoogle Scholar
  27. Holway DA, Lach L, Suarez AV, Ysutsui ND, Case TJ (2002) The causes and consequences of ant invasions. Annu Rev Ecol Syst 33:181–233CrossRefGoogle Scholar
  28. Hooper-Bui LM, Rust MK, Reierson DA (2004) Predation of the endangered California Least Tern, Sterna antillarum browni by the Southern Fire Ant, Solenopsis xyloni (Hymenoptera, Formicidae). Sociobiology 43:401–418Google Scholar
  29. Isacch JP, Barg M (2002) Are bufonid toads specialized ant-feeders? A case test from the Argentinian flooding pampa. J Nat Hist 36:2005–2012CrossRefGoogle Scholar
  30. Ito F, Okaue M, Ichikawa T (2009) A note on prey composition of the Japanese treefrog, Hyla japonica, in an area invaded by Argentine ants, Linepithema humile, in Hiroshima Prefecture, western Japan (Hymenoptera: Formicidae). Myrmecol News 12:35–39Google Scholar
  31. Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170CrossRefGoogle Scholar
  32. Kurz-Benson K, Otieno D, Lobo do Vale R, Siegwolf R, Schmidt M, Herd A et al (2006) Hydraulic lift in cork oak trees in a savannah-type Mediterranean ecosystem and its contribution to the local water balance. Plant Soil 282:361–378CrossRefGoogle Scholar
  33. Lach L, Parr C, Abbott K (2010) Ant ecology. Oxford University Press, OxfordGoogle Scholar
  34. Li Y, Ke Z, Wang S, Smith GR, Liu X (2011) An exotic species is the favorite prey of a native enemy. PLoS One 6(9):e24299CrossRefPubMedPubMedCentralGoogle Scholar
  35. Lorrain A, Graham BS, Popp BN, Allain V, Olson RJ, Hunt BPV, Potier M, Fry B, Galván-Magaña F, Menkes CER, Kaehler S, Ménard F (2014) Nitrogen isotopic baselines and implications for estimating foraging habitat and trophic position of yellowfin tuna in the Indian and Pacific Oceans. Deep-Sea Res Pt II 113:188–198CrossRefGoogle Scholar
  36. Lowe S, Browne M, Boudjelas S, De Poorter M (2000) 100 of the world’s worst invasive alien species: a selection from the global invasive species database. Invasive Species Specialist Group Auckland, New ZealandGoogle Scholar
  37. Luque GM, Bellard C, Bertelsmeier C, Bonnaud E, Genovesi P, Simberloff D, Courchamp F (2013) The 100th among some of the worst. Biol Invasions 16:981–985CrossRefGoogle Scholar
  38. Maerz JC, Karuzas JM, Madison DM, Blossey B (2005) Introduced invertebrates are important prey for a generalist predator. Divers Distrib 11:83–90CrossRefGoogle Scholar
  39. Miaud C, Sanuy D, Avrillier JN (2000) Terrestrial movements of the natterjack toad Bufo calamita (Amphibia, Anura) in a semi-arid, agricultural landscape. Amphibia Reptilia 21:357–370CrossRefGoogle Scholar
  40. Monzo C, Juan-Blasco M, Pekar S, Molla O, Castanera P, Urbaneja A (2013) Pre-adaptive shift of a native predator (Araneae, Zodariidae) to an abundant invasive ant species (Hymenoptera, Formicidae). Biol Invasions 15:89–100CrossRefGoogle Scholar
  41. Oliver JA (1955) The natural history of North American amphibians and reptiles. Princeton, New JerseyGoogle Scholar
  42. Pekár S, Mayntz D (2014) Comparative analysis of the macronutrient content of Central European ants (Formicidae): implications for ant-eating predators. J Insect Physiol 62:32–38CrossRefPubMedGoogle Scholar
  43. Pintor LM, Byers JE (2015) Do native predators benefit from non-native prey? Ecol Lett 18:1174–1180CrossRefGoogle Scholar
  44. Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83(3):703–718CrossRefGoogle Scholar
  45. Pysek P, Richardson DM, Pergl J, Jarosik V, Sixtová Z, Weber E (2008) Geographical and taxonomic biases in invasion ecology. Trends Ecol Evol 23(5):237–244CrossRefPubMedGoogle Scholar
  46. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Accessed 16 Aug 2017
  47. Ricciardi A, Hoopes MF, Marchetti MP, Lockwood JL (2013) Progress toward understanding the ecological impacts of nonnative species. Ecol Monogr 83:263–282CrossRefGoogle Scholar
  48. Robbins TR, Freidenfelds NA, Langkilde T (2013) Native predator eats invasive toxic prey: evidence for increased incidence of consumption rather than aversion-learning. Biol Invasions 15:407–415CrossRefGoogle Scholar
  49. SAS Institute Inc® (2008) 9.2 User Guide. SAS Inst, Cary, NC, USAGoogle Scholar
  50. Sax DF, Stachowicz JJ, Brown JH, Bruno JF, Dawson MN, Gaines SD, Grosberg RK, Hastings A, Holt RD, Mayfield MM, O’Connor MI, Rice WR (2007) Ecological and evolutionary insights from species invasions. Trends Ecol Evol 22(9):465–471CrossRefPubMedGoogle Scholar
  51. Sih A, Bolnick DI, Luttbeg B, Orrock JL, Peacor SD, Pintor LM, Preisser E, Rehage JS, Vonesh JR (2010) Predator–prey naïveté, antipredator behavior, and the ecology of predator invasions. Oikos 119:610–621CrossRefGoogle Scholar
  52. Sockman KW (1997) Variation in life-history traits and nest-site selection affects risk of nest predation in the California gnatcatcher. Auk 114:324–332CrossRefGoogle Scholar
  53. Suarez AV, Case TJ (2002) Bottom-up effects on persistence of a specialist predator: ant invasions and horned lizards. Ecol Appl 12:291–298CrossRefGoogle Scholar
  54. Suarez AV, Bolger DT, Case TJ (1998) Effects of fragmentation and invasion on native ant communities in coastal southern California. Ecology 79(6):2041–2056CrossRefGoogle Scholar
  55. Suarez AV, Richmond JQ, Case TJ (2000) Prey selection in horned lizards following the invasion of Argentine ants in southern California. Ecol Appl 10:711–725CrossRefGoogle Scholar
  56. Suarez AV, Holway DA, Case TJ (2001) Patterns of spread in biological invasions dominated by long-distance jump dispersal: insights from Argentine ants. P Natl Acad Sci USA 98:1095–1100CrossRefGoogle Scholar
  57. Suarez A, Yeh P, Case TJ (2005) Impacts of Argentine ants on avian nesting success. Insect Soc 52:378–382CrossRefGoogle Scholar
  58. Therneau TM (2015) coxme: Mixed Effects Cox Models. R package version 2.2-5. Accessed 16 Aug 2017
  59. Touyama Y, Ihara Y, Ito F (2008) Argentine ant infestation affects the abundance of the native myrmecophagic jumping spider Siler cupreus Simon in Japan. Insect Soc 55:144–146CrossRefGoogle Scholar
  60. Twardochleb LA, Novak M, Moore JW (2012) Using the functional response of a consumer to predict biotic resistance to invasive prey. Ecol Appl 22(4):1162–1171CrossRefPubMedGoogle Scholar
  61. Vanderklift MA, Ponsard S (2003) Sources of variation in consumer-diet δN-15 enrichment: a meta-analysis. Oecologia 136(2):169–182CrossRefPubMedGoogle Scholar
  62. Vogel V, Pedersen JS, Giraud T, Krieger MJ, Keller L (2010) The worldwide expansion of the Argentine ant. Divers Distrib 16(1):170–186CrossRefGoogle Scholar
  63. Wanger TC, Wielgoss AC, Motzke I, Clough Y, Brook BW, Sodhi NS, Tscharntke T (2011) Endemic predators, invasive prey and native diversity. P Roy Soc B-Biol Sci 278:690–694CrossRefGoogle Scholar
  64. Wetterer JK, Wild AL, Suarez AV, Roura-Pascual N, Espadaler X (2009) Worldwide spread of the Argentine ant, Linepithema humile (Hymenoptera: Formicidae). Mirmecol News 12:187–194Google Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Paloma Alvarez-Blanco
    • 1
  • Stephane Caut
    • 1
  • Xim Cerdá
    • 1
  • Elena Angulo
    • 1
  1. 1.Estación Biológica de Doñana, CSICSevilleSpain

Personalised recommendations