Skip to main content

Advertisement

Log in

Breeding consequences for a songbird nesting in Argentine ant’ invaded land

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

The consequences of ant invasions on ecosystems may only become apparent after long periods. In addition, predicting how sensitive native fauna will respond is only possible if the underlying proximate mechanisms of their impact are identified. We studied the attraction of the native and invasive ant community to artificial bird nests. Further, we studied reproduction of a wild native songbird over five consecutive breeding seasons in relation to the presence of an invasive ant species. We analysed biometric, reproductive and individual blood parameters of great tits Parus major breeding in invaded as compared to uninvaded sites by Argentine ants Linepithema humile. Great tits bred preferably in uninvaded territories by the Argentine ant. Moreover, Argentine ants were more abundant at nests in invaded sites, than any native ant species were at uninvaded sites. Further, Argentine ants recruited at the artificial nests more intensively and responded to a larger variety of nest contents than native species. Although breeding success and adult condition did not vary in relation to invasion status, offspring quality was negatively affected by the presence of Argentine ants. Nestlings reared in invaded sites were lighter, with lower wing/tarsus length ratio and had a reduced nutritional condition and altered oxidative stress balance as measured from several blood parameters. The interspersed distribution and small distance between invaded versus uninvaded territories suggest that ant presence affects nestling condition through direct interference at the nest. Our results highlight the importance of evaluating the proximate effects like physiological parameters of the native fauna, when studying invasive ant-native bird interactions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

Availability data and material

Data will be made available upon reasonable request.

References

  • Abril S, Oliveras J, Gomez C (2007) Foraging activity and dietary spectrum of the Argentine ant (Hymenoptera: Formicidae) in invaded natural areas of the Northeast Iberian Peninsula. Environ Entomol 36:1166–1173

    CAS  PubMed  Google Scholar 

  • Aho T, Kuitunen M, Suhonen J, Jäntti A, Hakkari T (1997) Behavioural responses of Eurasian treecreepers, Certhia familiaris, to competition with ants. Anim Behav 54:1283–1290

    CAS  PubMed  Google Scholar 

  • Aho T, Kuitunen M, Suhonen J, Jäntti A, Hakkari T (1999) Reproductive success of Eurasian treecreepers, Certhia familiaris, lower in territories with wood ants. Ecology 80:998–1007

    Google Scholar 

  • Allen C, Epperson D, Garmestani A (2004) Red imported fire ant impacts on wildlife: a decade of research. Am Mid Nat 152:88–103

    Google Scholar 

  • Alvarez-Blanco P, Caut S, Cerdá X, Angulo E (2017) Native predators living in invaded areas: responses of terrestrial amphibian species to an Argentine ant invasion. Oecologia 185:95–106

    PubMed  Google Scholar 

  • Alvarez-Blanco P, Cerdá X, Hefetz A, Boulay R, Bertó-Moran A, Díaz-Paniagua C, Lenoir A, Billen J, Liedtke C, Chauhan KR, Bhagavathy G, Angulo E (2020) Effects of the Argentine ant venom on terrestrial amphibian. Conserv Biol (in press)

  • Angulo E, Caut S, Cerdá X (2011) Scavenging in Mediterranean ecosystems: effect of the invasive Argentine ant. Biol Invasion 13:1183–1194

    Google Scholar 

  • Ardia DR, Pérez JH, Clotfelter ED (2006) Nest box orientation affects internal temperature and nest site selection by Tree Swallows. J Field Ornithol 77:339–344

    Google Scholar 

  • Bates D, Maechler M, Bolker B et al (2015) Fitting linear mixed-effects models using lme4. J Stat Soft 67:1–48

    Google Scholar 

  • Boieiro M, Catry P, Jardim CS, Menezes D, Silva I, Coelho N, Oliveira P, Gatt MC, Pedro P, Granadeiro JP (2018) Invasive Argentine ants prey on Bulwer’s petrels nestlings on the Desertas Islands (Madeira) but do not depress seabird breeding success. J Nat Conserv 43:35–38

    Google Scholar 

  • Brightwell RJ, Silverman J (2011) The Argentine ant persists through unfavorable winters via a mutualism facilitated by a native tree. Environ Entomol 40:1019–1026

    PubMed  Google Scholar 

  • Buege JA, Aust SD (1978) Microsomal lipid peroxidation. In: Fleischer S, Packer L (eds) Methods in enzymology. Academic Press, New York, pp 302–310

    Google Scholar 

  • Carmagnol F, Sinet PM, Jerome H (1983) Selenium-dependent and non-selenium-dependent glutathione peroxidases in human tissue extracts. Biochim Biophys Acta (BBA) Gen Subj 759:49–57

    CAS  Google Scholar 

  • Carpintero S, Reyes-López J, De Reyna LA (2005) Impact of Argentine ants (Linepithema humile) on an arboreal ant community in Donana National Park, Spain. Biodivers Conserv 14:151–163

    Google Scholar 

  • 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(5):1100–1111

    CAS  PubMed  Google Scholar 

  • Castro-Cobo S, Carpintero-Ortega S, Reyes-López JL, Sergio F, Angulo E (2019) Humans and scavenging raptors facilitate Argentine ant invasion in Doñana National Park: no counter-effect of biotic resistance. Biol Inv 21:2221–2232

    Google Scholar 

  • Cohen AA, McGraw KJ (2009) No simple measures for antioxidant status in birds: complexity in inter- and intraspecific correlations among circulating antioxidant types. Funct Ecol 23:310–320

    Google Scholar 

  • Cohen G, Somerson NL (1969) Catalase-aminotriazole method for measuring secretion of hydrogen peroxide by microorganisms. J Bacteriol 98:543–546

    CAS  PubMed  PubMed Central  Google Scholar 

  • Costantini D (2008) Oxidative stress in ecology and evolution: lessons from avian studies. Ecol Lett 11:1238–1251

    PubMed  Google Scholar 

  • Cribb AE, Leeder JS, Spielberg SP (1989) Use of a microplate reader in an assay of glutathione reductase using 5, 5′-dithiobis (2-nitrobenzoic acid). Anal Biochem 183:195–196

    CAS  PubMed  Google Scholar 

  • Davis NE, O'Dowd DJ, Green PT, MacNally R (2008) Effects of an alien ant invasion on abundance, behavior, and reproductive success of endemic island birds. Conserv Biol 22:1165–1176

    PubMed  Google Scholar 

  • DeFisher LE, Bonter DN (2013) Effects of invasive European fire ants (Myrmica rubra) on Herring Gull (Larus argentatus) reproduction. PLoS ONE 8:e64185

    CAS  PubMed  PubMed Central  Google Scholar 

  • Delibes M (2005) La naturaleza en peligro: causas y consecuencias de la extinción de especies. Destino

  • Di Giacomo AS, Di Giacomo AG (2006) Observations of strange-tailed Tyrants (Alectrurus risora) and other grassland birds following army ants and armadillos. J Field Ornithol 77:266–268

    Google Scholar 

  • 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 Inv 15:2013–2027

    Google Scholar 

  • Estany-Tigerström D, Bas JM, Pons P (2010) Does Argentine ant invasion affect prey availability for foliage-gleaning birds? Biol Inv 12:827–839

    Google Scholar 

  • Erel O (2004) A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation. Clin Biochem 37:277–285

    CAS  PubMed  Google Scholar 

  • Flores M, Lazo P, Campbell G, Simeone A (2017) Breeding status of the red-tailed tropicbird (Phaethon rubricauda) and threats to its conservation on Easter Island (Rapa Nui). Pac Sci 71:149–160

    Google Scholar 

  • Gibson JC, Suarez AV, Qazi D, Benson TJ, Chiavacci SJ, Merrill L (2019) Prevalence and consequences of ants and other arthropods in active nests of Midwestern birds. Can J Zool 97:696–704

    Google Scholar 

  • Gilardi JD, von Kugelgen K (1991) Bird/ant/acacia symbioses in a mature Neotropical forest. Wilson Bull 103:711–712

    Google Scholar 

  • GISD (2018) Global Invasive Species Database. https://www.iucngisd.org/gisd/

  • Giuliano WM, Allen CR, Lutz RS, Demarais S (1996) Effects of red imported fire ants on northern bobwhite chicks. J Wildl Manag 60:309–313

    Google Scholar 

  • Gosler A (1993) The great tit. Hamlyn, London

    Google Scholar 

  • Grimes L (1973) The breeding of Heuglin's Masked Weaver and its nesting association with the red weaver ant. Ostrich 44:170–175

    Google Scholar 

  • Haemig PD (1996) Interference from ants alters foraging ecology of great tits. Behav Ecol Sociobiol 38:25–29

    Google Scholar 

  • Haemig PD (1999) Predation risk alters interactions among species: competition and facilitation between ants and nesting birds in a boreal forest. Ecol Lett 2:178–184

    Google Scholar 

  • Haemig PD (2001) Symbiotic nesting of birds with formidable animals: a review with applications to biodiversity conservation. Biodivers Conserv 10:527–554

    Google Scholar 

  • Harrell FE, Dupont MC (2017) Hmisc: Harrell Miscellaneous. R package 4.0-3. R Foundation for Statistical Computing, Vienna, Austria

  • Helms JA, Godfrey AP, Ames T, Bridge ES (2016) Are invasive fire ants kept in check by native aerial insectivores? Biol lett 12:20160059

    PubMed  PubMed Central  Google Scholar 

  • Helms KR, Vinson SB (2002) Widespread association of the invasive ant Solenopsis invicta with an invasive mealybug. Ecology 83:2425–2438

    Google Scholar 

  • Holway DA, Lach L, Suarez AV, Tsutsui ND, Case TJ (2002) The causes and consequences of ant invasions. Ann Rev Ecol Syst 33:181–233

    Google Scholar 

  • Hooper-Bui L, Rust M, Reierson D (2004) Predation of the endangered California Least Tern, Sterna antillarum browni by the southern fire ant, Solenopsis xyloni (Hymenoptera, Formicidae). Sociobiology 43:401–418

    Google Scholar 

  • Janzen DH (1969) Birds and the ant× acacia interaction in Central America, with notes on birds and other myrmecophytes. Condor 71:240–256

    Google Scholar 

  • Jenni-Eiermann S, Jenni L (1998) What can plasma metabolites tell us about the metabolism, physiological state and condition of individual birds? An overview. Biol Cons Fauna 102:312–319

    Google Scholar 

  • Jäntti A, Suorsa P, Hakkarainen H et al (2007) Within territory abundance of red wood ants Formica rufa is associated with the body condition of nestlings in the Eurasian treecreeper Certhia familiaris. J Avian Biol 38:619–624

    Google Scholar 

  • Karvonen J, Orell M, Rytkönen S, Broggi J, Belda E (2012) Population dynamics of an expanding passerine at the distribution margin. J Avian Biol 43:102–108

    Google Scholar 

  • Krushelnycky PD, Hodges CS, Medeiros AC, Loope LL (2001) Interaction between the Hawaiian dark-rumped petrel and the Argentine ant in Haleakala National Park, Maui Hawaii. Stud Avian Biol Ser 22:243–246

    Google Scholar 

  • Krushelnycky PD, Loope LL, Reimer RJ (2005) The ecology, policy, and management of ants in Hawaii. Proc Hawaii Entomol Soc 37:1–25

    Google Scholar 

  • Lach L, Hooper-Bui LM (2010) Consequences of ant invasion. In: Lach L, Parr CL, Abbott KL (eds) Ant Ecology. Oxford University Press, New York, pp 261–286

    Google Scholar 

  • Lambrechts MM, Schatz B (2014) Ants and Paridae share nesting boxes in continental Mediterranean habitat. Folia Zool 63:63–66

    Google Scholar 

  • Lambrechts MM, Schatz B, Bourgault P (2008) Interactions between ants and breeding Paridae in two distinct Corsican oak habitats. Folia Zool 57:264–268

    Google Scholar 

  • Ligon RA, Siefferman L, Hill GE (2012) Invasive ants alter foraging and parental behaviors of a native bird. Ethology 118:858–866

    PubMed  PubMed Central  Google Scholar 

  • Lindström J (1999) Early development and fitness in birds and mammals. Trend Ecol Evol 14:343–348

    Google Scholar 

  • Lowe S, Browne M, Boudjelas S et al (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

    Google Scholar 

  • Maceda-Veiga A, Figuerola J, Martínez-Silvestre A, Viscor G, Ferrari N, Pacheco M (2015) Inside the Redbox: applications of haematology in wildlife monitoring and ecosystem health assessment. Sci Total Environ 514:322–332

    CAS  PubMed  Google Scholar 

  • Marshall MR, Cooper RJ (2004) Territory size of a migratory songbird in response to caterpillar density and foliage structure. Ecology 85:432–445

    Google Scholar 

  • Matsui S, Kikuchi T, Akatani K, Horie S, Takagi M (2009) Harmful effects of invasive yellow crazy ant Anoplolepis gracilipes on three land bird species of Minami-daito Island. Ornithol Sci 8:81–86

    Google Scholar 

  • McCord JM, Fridovich I (1969) Superoxide dismutase: an enzymatic function for erythrocuprein (hemocuprein). J Biol Chem 244:6049–6055

    CAS  PubMed  Google Scholar 

  • McCue MD (2010) Starvation physiology: reviewing the different strategies animals use to survive a common challenge. Comp Biochem Physiol A 156:1–18

    Google Scholar 

  • Mejías MA, Wingate DB, Madeiros JL, Wiersma YF, Robertson GJ (2017) Nest-cavity selection and nesting success of Bermudian white-tailed Tropicbirds (Phaethon lepturus catesbyi). Wilson J Ornithol 129:586–599

    Google Scholar 

  • Mitrus S, Hebda G, Wesołowski T (2016) Cohabitation of tree holes by ants and breeding birds in a temperate deciduous forest. Scand J Forest Res 31:135–139

    Google Scholar 

  • Monaghan P (2008) Early growth conditions, phenotypic development and environmental change. Phil Trans Royal Soc B 363:1635–1645

    Google Scholar 

  • Monaghan P, Metcalfe NB, Torres R (2009) Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecol Lett 12:75–92

    PubMed  Google Scholar 

  • Moore RP, Robinson WD (2004) Artificial bird nests, external validity, and bias in ecological field studies. Ecology 85:1562–1567

    Google Scholar 

  • Naef-Daenzer B (1994) Radiotracking of great and blue tits: new tools to assess territoriality, home-range use and resource distribution. Ardea 82:335–335

    Google Scholar 

  • Newell W, Barber TC (1913) The Argentine ant. Bulletin Bureau of Entomology U.S. Department of Agriculture 122:1–98

    Google Scholar 

  • Oksanen J, Blanchet GF, Friendly M et al (2016) vegan: Community Ecology Package. R package version 2.4-3. R Foundation for Statistical Computing, Vienna, Austria

    Google Scholar 

  • Pamplona R, Costantini D (2011) Molecular and structural antioxidant defenses against oxidative stress in animals. Am J Physiol Regul Integr Comp Physiol 301:R843–R863

    CAS  PubMed  Google Scholar 

  • Pedersen EK, Grant WE, Longnecker MT (1996) Effects of red imported fire ants on newly-hatched northern bobwhite. J Wild Man 60:164–169

    Google Scholar 

  • Persson L (1985) Asymmetrical competition: are larger animals competitively superior? Am Nat 126:261–266

    Google Scholar 

  • Peterson BL, Kus BE, Deutschman DH (2004) Determining nest predators of the Least Bell's Vireo through point counts, tracking stations, and video photography. J Field Ornithol 75:89–95

    Google Scholar 

  • Philpott SM, Greenberg R, Bichier P (2005) The influence of ants on the foraging behavior of birds in an agroforest. Biotropica 37:468–471

    Google Scholar 

  • Piersma T, van Gils JA (2011) The flexible phenotype: a body-centred integration of ecology, physiology, and behaviour. Oxford University Press, Oxford

    Google Scholar 

  • Plentovich S, Hebshi A, Conant S (2009) Detrimental effects of two widespread invasive ant species on weight and survival of colonial nesting seabirds in the Hawaiian Islands. Biol Inv 11:289–298

    Google Scholar 

  • Plentovich S, Russell T, Fejeran CC (2018) Yellow crazy ants (Anoplolepis gracilipes) reduce numbers and impede development of a burrow-nesting seabird. Biol Inv 20:77–86

    Google Scholar 

  • Pons P, Bas JM, Estany-Tigerström D (2010) Coping with invasive alien species: the Argentine ant and the insectivorous bird assemblage of Mediterranean oak forests. Biodivers Conserv 19:1711–1723

    Google Scholar 

  • Powell BE (2008) Interactions between the ants Linepithema humile, Tapinoma sessile and aphid mutualists. Ph.D. dissertation, North Carolina State University, Raleigh, NC, 167

  • R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rankin DT, Clark CJ, Rankin EEW (2018) Hummingbirds use taste and touch to discriminate against nectar resources that contain Argentine ants. Behav Ecol Sociobiol 72:44

    Google Scholar 

  • Ricklefs RE, Cox GW (1977) Morphological similarity and ecological overlap among passerine birds on St. Kitts. British West Indies Oikos 29:60–66

    Google Scholar 

  • Ridlehuber KT (1982) Fire ant predation on wood duck ducklings and pipped eggs. Southwest Nat 27:222

    Google Scholar 

  • Seymour MA (2007) Effect of Red Imported Fire Ant (Solenopsis invicta Buren) on the Nesting Success of Northern Bobwhite (Colinus virginianus L.). Louisiana State University, Baton Rouge, Master's Theses 42. pp. 12

  • Shik JZ, Kay AD, Silverman J (2014) Aphid honeydew provides a nutritionally balanced resource for incipient Argentine ant mutualists. Anim Behav 95:33–39

    Google Scholar 

  • 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

    Google Scholar 

  • Stake MM, Cimprich DA (2003) Using video to monitor predation at Black-capped Vireo nests. Condor 105:348–357

    Google Scholar 

  • Stoddard HL (1936) Bobwhite quail; Its habits, preservation and increase. Scribner, New York

    Google Scholar 

  • Strong AM (2000) Divergent foraging strategies of two Neotropical migrant warblers: implications for winter habitat use. Auk 117:381–392

    Google Scholar 

  • Suarez AV, Yeh P, Case TJ (2005) Impacts of Argentine ants on avian nesting success. Insect Soc 52:378–382

    Google Scholar 

  • Tillberg CV, Holway DA, LeBrun EG, Suarez AV (2007) Trophic ecology of invasive Argentine ants in their native and introduced ranges. Proc Nat Acad Sci 104:20856–20861

    CAS  PubMed  Google Scholar 

  • Varela AI, Luna N, Luna-Jorquera G (2018) Assessing potential Argentine Ant recruitment to pipping eggs in the Red-tailed Tropicbird on Rapa Nui (Easter Island). Emu 118:381–385

    Google Scholar 

  • Welzel KF, Lee SH, Dossey AT, Chauhan KR, Choe DH (2018) Verification of Argentine ant defensive compounds and their behavioral effects on heterospecific competitors and conspecific nestmates. Sc Rep 8:1–15

    Google Scholar 

  • Wetterer JK, Wild AL, Suarez AV, Roura-Pascual N, Espadaler X (2009) Worldwide spread of the Argentine ant, Linepithema humile (Hymenoptera: Formicidae). Myrmecol News 12:187–194

    Google Scholar 

  • Wiebe KL, Gow EA (2013) Choice of foraging habitat by northern flickers reflects changes in availability of their ant prey linked to ambient temperature. Ecoscience 20:122–130

    Google Scholar 

  • Young BE, Kaspari M, Martin TE (1990) Species-specific nest selection by birds in ant-acacia trees. Biotropica 22:310–315

    Google Scholar 

Download references

Acknowledgements

Special thanks to Benjamin Carbonne, María Riesco Malho, Cristela Sánchez, Francisco Chicano, Sara Castro-Cobo, Sophie Le Hesran, Eduardo Rodríguez-Expósito, Marçal Pla for their help in the field. Jordi Figuerola and Jaime Potti kindly supplied the nestboxes for the study. We are indebted with Olivier Blight and Raphaël Boulay for their scientific input. We are also grateful to ICTS-RBD for allowing us to use their field facilities; and laboratory facilities at EBD (LAST, LEA and LPM). We are in debt with Manolo Vázquez for help provided with artificial nest experiment, Francisco Miranda and Olaya García for their help with blood analyses and David Aragonés for his help with the mapsy. Comments by two anonymous reviewers improved earlier versions of the manuscript

Funding

This research was funded by the Spanish MINECO and FEDER (Consolider MONTES CSD2008-00040, CGL2012-36181 CGL2015-65807-P to XC, and CGL2013-43660-P to EA). Spanish MINECO also funded E.A. (postdoctoral Ramón y Cajal contract, RYC-2010-06663), J.B. (postdoctoral contracts JAE-DOC [E-41-2009-0724722] and Juan de la Cierva) and P.A-B. (predoctoral contract [BES-2013-064713]).

Author information

Authors and Affiliations

Authors

Contributions

PAB, JB, XC and EA designed the experiment. PAB and OGJ collected the data. PAB, JB and EA analysed the data and wrote the manuscript. All authors critiqued the manuscript for intellectual content.

Corresponding author

Correspondence to Juli Broggi.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures were conducted according to local ethical committee guidelines. The experimental procedures were approved by the national authorities (CEBA-EBD 11-36b, CSD2008-00040, 1043/MDCG/mect, 2014-1073-00000613-FQH/MDCG/mect, 2015-1073-00001494-FQH/MDCG/mect and 2015–1073-00003362-JPCD/MDCG/mes).

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 3832 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alvarez-Blanco, P., Broggi, J., Cerdá, X. et al. Breeding consequences for a songbird nesting in Argentine ant’ invaded land. Biol Invasions 22, 2883–2898 (2020). https://doi.org/10.1007/s10530-020-02297-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-020-02297-3

Keywords

Profiles

  1. Elena Angulo