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.
This is a preview of subscription content, log in to check access.
Buy single article
Instant access to the full article PDF.
Price includes VAT for USA
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
This is the net price. Taxes to be calculated in checkout.
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 161–179
Angulo E, Caut S, Cerdá X (2011) Scavenging in Mediterranean ecosystems: effect of the invasive Argentine ant. Biol Invasions 13:1183–1194
Arnan X, Cerdá X, Retana J (2014) Ant functional responses along environmental gradients. J Anim Ecol 83:1398–1408
Banks PB, Dickman CR (2007) Alien predation and the effects of multiple levels of prey naiveté. Trends Ecol Evolut 22(5):229–230
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 6:30078
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 153:1–9
Callaway RM, Ridenour WM (2004) Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Environ 2(8):436–443
Carlsson NO, Sarnelle O, Strayer DL (2009) Native predators and exotic prey—an acquired taste? Front Ecol Environ 7:525–532
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 14:151–163
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 36:1100–1111
Carthey AJ, Banks PB (2014) Naïveté in novel ecological interactions: lessons from theory and experimental evidence. Biol Rev 89(4):932–949
Catford JA, Jansson R, Nilsson C (2009) Reducing redundancy in invasion ecology by integrating hypotheses into a single theoretical framework. Divers Distrib 15(1):22–40
Caut S, Angulo E, Courchamp F (2008) Dietary shift of an invasive predator: rats, seabirds and sea turtles. J Appl Ecol 45:428–437
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):443–453
Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7:721–733
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, Spain
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):41–58
Estany-Tigerström D, Bas JM, Pons P (2010) Does Argentine ant invasion affect prey availability for foliage-gleaning birds? Biol Invasions 12:827–839
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 15:2013–2027
Fisher RN, Suarez AV, Case TJ (2002) Spatial patterns in the abundance of the coastal horned lizard. Conserv Biol 16:205–215
Glenn S, Holway D (2008) Consumption of introduced prey by native predators: Argentine ants and pit-building ant lions. Biol Invasions 10:273–280
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 19:103–110
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):187–195
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
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 330:1503–1509
Holway DA, Suarez AV (2006) Homogenization of ant communities in mediterranean California: the effects of urbanization and invasion. Biol Conserv 127(3):319–326
Holway DA, Lach L, Suarez AV, Ysutsui ND, Case TJ (2002) The causes and consequences of ant invasions. Annu Rev Ecol Syst 33:181–233
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 43:401–418
Isacch JP, Barg M (2002) Are bufonid toads specialized ant-feeders? A case test from the Argentinian flooding pampa. J Nat Hist 36:2005–2012
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 12:35–39
Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170
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 282:361–378
Lach L, Parr C, Abbott K (2010) Ant ecology. Oxford University Press, Oxford
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):e24299
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 113:188–198
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 Zealand
Luque GM, Bellard C, Bertelsmeier C, Bonnaud E, Genovesi P, Simberloff D, Courchamp F (2013) The 100th among some of the worst. Biol Invasions 16:981–985
Maerz JC, Karuzas JM, Madison DM, Blossey B (2005) Introduced invertebrates are important prey for a generalist predator. Divers Distrib 11:83–90
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 21:357–370
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 15:89–100
Oliver JA (1955) The natural history of North American amphibians and reptiles. Princeton, New Jersey
Pekár S, Mayntz D (2014) Comparative analysis of the macronutrient content of Central European ants (Formicidae): implications for ant-eating predators. J Insect Physiol 62:32–38
Pintor LM, Byers JE (2015) Do native predators benefit from non-native prey? Ecol Lett 18:1174–1180
Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83(3):703–718
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):237–244
R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed 16 Aug 2017
Ricciardi A, Hoopes MF, Marchetti MP, Lockwood JL (2013) Progress toward understanding the ecological impacts of nonnative species. Ecol Monogr 83:263–282
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 15:407–415
SAS Institute Inc® (2008) 9.2 User Guide. SAS Inst, Cary, NC, USA
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):465–471
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 119:610–621
Sockman KW (1997) Variation in life-history traits and nest-site selection affects risk of nest predation in the California gnatcatcher. Auk 114:324–332
Suarez AV, Case TJ (2002) Bottom-up effects on persistence of a specialist predator: ant invasions and horned lizards. Ecol Appl 12:291–298
Suarez AV, Bolger DT, Case TJ (1998) Effects of fragmentation and invasion on native ant communities in coastal southern California. Ecology 79(6):2041–2056
Suarez AV, Richmond JQ, Case TJ (2000) Prey selection in horned lizards following the invasion of Argentine ants in southern California. Ecol Appl 10:711–725
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 98:1095–1100
Suarez A, Yeh P, Case TJ (2005) Impacts of Argentine ants on avian nesting success. Insect Soc 52:378–382
Therneau TM (2015) coxme: Mixed Effects Cox Models. R package version 2.2-5. https://CRAN.R-project.org/package=coxme. Accessed 16 Aug 2017
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 55:144–146
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):1162–1171
Vanderklift MA, Ponsard S (2003) Sources of variation in consumer-diet δN-15 enrichment: a meta-analysis. Oecologia 136(2):169–182
Vogel V, Pedersen JS, Giraud T, Krieger MJ, Keller L (2010) The worldwide expansion of the Argentine ant. Divers Distrib 16(1):170–186
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 278:690–694
Wetterer JK, Wild AL, Suarez AV, Roura-Pascual N, Espadaler X (2009) Worldwide spread of the Argentine ant, Linepithema humile (Hymenoptera: Formicidae). Mirmecol News 12:187–194
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.
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.
All applicable institutional and national guidelines for the care and use of animals were followed.
Communicated by Peter Banks.
Electronic supplementary material
Below is the link to the electronic supplementary material.
About this article
Cite this article
Alvarez-Blanco, P., Caut, S., Cerdá, X. et al. Native predators living in invaded areas: responses of terrestrial amphibian species to an Argentine ant invasion. Oecologia 185, 95–106 (2017). https://doi.org/10.1007/s00442-017-3929-x
- Biotic resistance
- Enemy release
- Exotic prey naïveté
- Invasive prey
- Linepithema humile