Abstract
Biological invasions are a contemporary global threat because invasive species can have substantial negative economic and ecological impacts. Invasive species can outcompete native species through two main mechanisms: interference competition (direct, negative interactions like aggression) and/or exploitative competition (indirect, negative interactions resulting from species using the same, limited resources like food). The invasive Italian wall lizard (Podarcis siculus) was introduced into Lisbon, Portugal, 20 years ago, and is believed to be locally displacing the native green Iberian wall lizard (Podarcis virescens). We experimentally tested for competition between these two lizard species by establishing heterospecific (one pair of each species) and conspecific (two pairs of the same species; control) treatments in enclosures containing a high- and a low-quality refuge. Lizards were fed from food dishes every other day. We tested if species showed interference (aggressive behaviour, stealing food and shelter exclusion) or exploitative competition (tolerance between species but differences in food consumption efficiency). We found evidence for exploitative competition: the invasive species arrived first at food stations, consumed more food and gained more weight than the native species. We suggest that exploitative competition may, in part, explain the observed displacement of P. virescens from contact areas with the invasive P. siculus. Deciphering the competitive mechanisms between invasive and native species is vital for understanding the invasion process.
Significance statement
To become successful invaders, alien species must often outcompete native species they encounter in a new location. But how can an alien species outcompete a resident with a long evolutionary history in an environment in which the resident is expected to be better adapted? We studied an invasive and native congeneric pair of sympatric lizards to understand how they interact and potentially compete in a controlled environment. The invasive Italian wall lizard and a native congener were very tolerant of each other; however, the invasive species was first to arrive at food, ate more and grew faster, suggesting exploitative competition. This contrasts with previous studies in other introduced locations where the Italian wall lizard was more aggressive towards native lizards, suggestive of interference competition. Our results help explain why the Italian wall lizard is so successful and suggests it may compete in different ways, possibly in response to local environmental conditions and which species it may be competing with, but with the same outcome: the displacement of native species.
Graphical abstract
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data and code availability
Data and code are available at OSF doi:10.17605/OSF.IO/9YX5H.
References
Amarasekare P (2002) Interference competition and species coexistence. Proc R Soc Lond B 269:2541–2550. https://doi.org/10.1098/rspb.2002.2181
Anderson CB, Griffith CR, Rosemond AD, Rozzi R, Dollenz O (2006) The effects of invasive North American beavers on riparian plant communities in Cape Horn, Chile: do exotic beavers engineer differently in sub-Antarctic ecosystems? Biol Conserv 128:467–474. https://doi.org/10.1016/j.biocon.2005.10.011
Baker MC, Belcher CS, Deutsch LC, Sherman GL, Thompson DB (1981) Foraging success in junco flocks and the effects of social hierarchy. Anim Behav 29:137–142. https://doi.org/10.1016/s0003-3472(81)80160-1
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48 arXiv:1406.5823v1
Beauchamp G (2013) Social predation: how group living benefits predators and prey. Academic Press Elsevier, UK
Burke RL, Hussain AA, Storey JM, Storey KB (2002) Freeze tolerance and supercooling ability in the Italian wall lizard, Podarcis sicula, introduced to Long Island, New York. Copeia 2002:836–842. https://doi.org/10.1643/0045-8511(2002)002[0836:FTASAI]2.0.CO;2
CABI (2020) Podarcis sicula [original text by Silva-Rocha I]. In: Invasive species compendium. CAB International, Wallingford, UK, www.cabi.org/isc
Capula M, Luiselli L, Bologna MA, Ceccarelli A (2002) The decline of the Aeolian wall lizard, Podarcis raffonei: causes and conservation proposals. Oryx 36:66–72. https://doi.org/10.1017/s0030605302000108
Carmo RF, Vasconcelos SD, Brundage AL, Tomberlin JK (2018) How do invasive species affect native species? Experimental evidence from a carrion blowfly (Diptera: Calliphoridae) system. Ecol Entomol 43:483–493. https://doi.org/10.1111/een.12524
Carretero MA (2015) Examining the ecophysiology of Mediterranean lizards with evolutionary, biogeographic and conservation eyes. Invited plenary lecture at 18th European Congress of Herpetology, Wroclaw, Poland
Carretero MA, Salvador A (2016) Lagartija verdosa—Podarcis virescens. In: Salvador A, Marco A (eds) Enciclopedia Virtual de los Vertebrados Españoles. Museo Nacional de Ciencias Naturales, Madrid, http://www.vertebradosibericos.org/reptiles/podvir.html
Carretero MA, Silva-Rocha I (2015) La lagartija italiana (Podarcis sicula) en la península ibérica e islas Baleares (The Italian lizard (Podarcis sicula) in the Iberian Peninsula and Balearic islands). Bol Asoc Herpetol Esp 26:71–75
Case TJ, Bolger DT, Petren K (1994) Invasions and competitive displacement among house geckos in the tropical Pacific. Ecology 75:464–477. https://doi.org/10.2307/1939550
Crawley MJ (2012) The R book. John Wiley & Sons Ltd, Hoboken, NJ, USA
Crooks JA (2002) Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers. Oikos 97:153–166. https://doi.org/10.1034/j.1600-0706.2002.970201.x
Damas-Moreira I, Riley JL, Harris DJ, Whiting MJ (2019) Can behaviour explain invasion success? A comparison between sympatric invasive and native lizards. Anim Behav 151:195–202. https://doi.org/10.1016/j.anbehav.2019.03.008
Downes S, Bauwens D (2002) An experimental demonstration of direct behavioural interference in two Mediterranean lacertid lizard species. Anim Behav 63:1037–1046. https://doi.org/10.1006/anbe.2002.3022
Elton CS (1958) The ecology of invasions by animals and plants. Methuen and Co Ltd, London
Garcia-Porta J, Irisarri I, Kirchner M et al (2019) Environmental temperatures shape thermal physiology as well as diversification and genome-wide substitution rates in lizards. Nat Commun 10:4077. https://doi.org/10.1038/s41467-019-11943-x
Gérard A, Jourdan H, Millon A, Vidal E (2016) Knocking on heaven’s door: are novel invaders necessarily facing naïve native species on islands? PLoS One 11:e0151545. https://doi.org/10.1371/journal.pone.0151545
González de la Vega JP, González-García JP, García-Pulido T, González-García G (2001) Podarcis sicula (Lagartija italiana), primera cita para Portugal. Bol Asoc Herpetol Esp 12:9
Grether GF, Peiman KS, Tobias JA, Robinson BW (2017) Causes and consequences of behavioral interference between species. Trends Ecol Evol 32:760–772. https://doi.org/10.1016/j.tree.2017.07.004
Gurnell J, Wauters LA, Lurz PWW, Tosi G (2004) Alien species and interspecific competition: effects of introduced eastern grey squirrels on red squirrel population dynamics. J Anim Ecol 73:26–35. https://doi.org/10.1111/j.1365-2656.2004.00791.x
Herrel A, Huyghe K, Vanhooydonck B, Backeljau T, Breugelmans K, Grbac I, van Damme R, Irschick DJ (2008) Rapid large-scale evolutionary divergence in morphology and performance associated with exploitation of a different dietary resource. P Natl Acad Sci USA 105:4792–4795. https://doi.org/10.1073/pnas.0711998105
Holdridge EM, Cuellar-Gempeler C, terHorst CP (2016) A shift from exploitation to interference competition with increasing density affects population and community dynamics. Ecol Evol 6:5333–5341. https://doi.org/10.1002/ece3.2284
Holway DA (1999) Competitive mechanisms underlying the displacement of native ants by the invasive Argentine ant. Ecology 80:238–251. https://doi.org/10.2307/176993
Hulme PE (2007) Biological invasions in Europe: drivers, pressures, states, impacts and responses. In: Hester RE, Harrison RM (eds) Biodiversity under threat, vol 25. Cambridge University Press, Cambridge, pp 56–80
Human KG, Gordon DM (1996) Exploitation and interference competition between the invasive Argentine ant, Linepithema humile, and native ant species. Oecologia 105:405–412. https://doi.org/10.1007/bf00328744
Huxel GR (1999) Rapid displacement of native species by invasive species: effects of hybridization. Biol Conserv 89:143–152. https://doi.org/10.1016/s0006-3207(98)00153-0
Kraus F (2009) Impacts of alien reptiles and amphibians. In: Kraus F (ed) Alien reptiles and amphibians—a scientific compendium and analysis. Springer, Dordrecht, pp 57–93
Kupferberg SJ (1997) Bullfrog (Rana Catesbeiana) invasion of a California river: the role of larval competition. Ecology 78:1736–1751. https://doi.org/10.2307/2266097
Langkilde T, Thawley CJ, Robbins TR (2017) Behavioral adaptations to invasive species. Adv Study Behav 49:199–235. https://doi.org/10.1016/bs.asb.2016.12.003
Lenth RV (2016) Least-squares means: the R package lsmeans. J Stat Softw 69:1–33. https://doi.org/10.18637/jss.v069.i01
Lymbery AJ, Morine M, Kanani HG, Beatty SJ, Morgan DL (2014) Co-invaders: the effects of alien parasites on native hosts. Int J Parasitol Parasites Wildl 3:171–177. https://doi.org/10.1016/j.ijppaw.2014.04.002
Michaud JP (2002) Invasion of the Florida citrus ecosystem by Harmonia axyridis (Coleoptera: Coccinellidae) and asymmetric competition with a native species, Cycloneda sanguinea. Environ Entomol 31:827–835. https://doi.org/10.1603/0046-225x-31.5.827
Miller RS (1967) Pattern and process in competition. Adv Ecol Res 4:1–74. https://doi.org/10.1016/s0065-2504(08)60319-0
Nevo E, Gorman G, Soulé M, Yang SY, Clover R, Jovanović V (1972) Competitive exclusion between insular Lacerta species (Sauria, Lacertidae). Oecologia 10:183–190. https://doi.org/10.1007/bf00347990
Perkins LB, Nowak RS (2013) Invasion syndromes: hypotheses on relationships among invasive species attributes and characteristics of invaded sites. J Arid Land 5:275–283. https://doi.org/10.1007/s40333-013-0161-3
Persson L (1985) Asymmetrical competition: are larger animals competitively superior? Am Nat 126:261–266. https://doi.org/10.1086/284413
Petren K, Case TJ (1996) An experimental demonstration of exploitation competition in an ongoing invasion. Ecology 77:118–132. https://doi.org/10.2307/2265661
Petren K, Bolger DT, Case TJ (1993) Mechanisms in the competitive success of an invading sexual gecko over an asexual native. Science 259:354–358. https://doi.org/10.1126/science.259.5093.354
Pintor LM, Sih A (2009) Differences in growth and foraging behavior of native and introduced populations of an invasive crayfish. Biol Invasions 11:1895–1902. https://doi.org/10.1007/s10530-008-9367-2
Pintor LM, Sih A, Kerby JL (2009) Behavioral correlations provide a mechanism for explaining high invader densities and increased impacts on native prey. Ecology 90:581–587. https://doi.org/10.1890/08-0552.1
R Core Team (2017) A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org
Ribeiro RAV (2017) Avaliação do estádio de introdução da lagartixa italiana Podarcis siculus no Parque da Nações (Lisboa). University of Évora, Master Thesis
Ribeiro RAV, Sá-Sousa P (2018) Where to live in Lisbon: urban habitat used by the introduced Italian wall lizard (Podarcis siculus). Basic Appl Herpetol 32:57–70. https://doi.org/10.11160/bah.101
Roughgarden J (1983) Coevolution between competitors. In: Futuyma DJ, Slatkin MS (eds) Coevolution. Sinauer Associates, Sunderland, MA, USA, pp 388–403
Rowles AD, O’Dowd DJ (2007) Interference competition by Argentine ants displaces native ants: implications for biotic resistance to invasion. Biol Invasions 9:73–85. https://doi.org/10.1007/s10530-006-9009-5
Sannolo M, Carretero MA (2019) Dehydration constrains thermoregulation and space use in lizards. PLoS One 14:e0220384. https://doi.org/10.1371/journal.pone.0220384
Sax DF, Brown JH (2000) The paradox of invasion. Glob Ecol Biogeogr 9:363–371. https://doi.org/10.1046/j.1365-2699.2000.00217.x
Senczuk G, Colangelo P, De Simone E, Aloise G, Castiglia R (2017) A combination of long term fragmentation and glacial persistence drove the evolutionary history of the Italian wall lizard Podarcis siculus. BMC Evol Biol 17:6. https://doi.org/10.1186/s12862-016-0847-1
Short KH, Petren K (2008) Boldness underlies foraging success of invasive Lepidodactylus lugubris geckos in the human landscape. Anim Behav 76:429–437. https://doi.org/10.1016/j.anbehav.2008.04.008
Silva-Rocha I, Salvi D, Carretero MA (2012) Genetic data reveal a multiple origin for the populations of the Italian wall lizard Podarcis sicula (Squamata: Lacertidae) introduced in the Iberian Peninsula and Balearic islands. Ital J Zool 79:502–510. https://doi.org/10.1080/11250003.2012.680983
Strauss SY, Lau JA, Carroll SP (2006) Evolutionary responses of natives to introduced species: what do introductions tell us about natural communities? Ecol Lett 9:357–374. https://doi.org/10.1111/j.1461-0248.2005.00874.x
Vanhooydonck B, Van Damme R, Aerts P (2000) Ecomorphological correlates of habitat partitioning in Corsican lacertid lizards. Funct Ecol 14:358–368. https://doi.org/10.1046/j.1365-2435.2000.00430.x
Vervust B, Grbac I, Van Damme R (2007) Differences in morphology, performance and behaviour between recently diverged populations of Podarcis sicula mirror differences in predation pressure. Oikos 116:1343–1352. https://doi.org/10.1111/j.0030-1299.2007.15989.x
Verwaijen D, Van Damme R (2008) Wide home ranges for widely foraging lizards. Zoology 111:37–47. https://doi.org/10.1016/j.zool.2007.04.001
Walsh JR, Carpenter SR, Vander Zanden MJ (2016) Invasive species triggers a massive loss of ecosystem services through a trophic cascade. P Natl Acad Sci USA 113:4081–4085. https://doi.org/10.1073/pnas.1600366113
Wauters LA, Gurnell J, Martinoli A, Tosi G (2001) Does interspecific competition with introduced grey squirrels affect foraging and food choice of Eurasian red squirrels? Anim Behav 61:1079–1091. https://doi.org/10.1006/anbe.2001.1703
Žagar A, Carretero MA, Osojnik N, Sillero N, Vrezec A (2015) A place in the sun: does interspecific interference affect thermoregulation in coexisting lizards. Behav Ecol Sociobiol 69:1127–1137. https://doi.org/10.1007/s00265-015-1927-8
Zuffi MAL, Giannelli C (2013) Trophic niche and feeding biology of the Italian wall lizard, Podarcis siculus campestris (De Betta, 1857) along western Mediterranean coast. Acta Herpetol 8:35–39
Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14. https://doi.org/10.1111/j.2041-210x.2009.00001.x
Acknowledgements
We deeply thank Bruno Pleno for scoring the videos. We also thank Bernardino Silva, Luís Damas, Amélia Moreira and Cristina Damas for all their assistance and support during this research. We would also like to thank the three anonymous reviewers for their valuable comments to our manuscript.
Funding
This research was funded by Macquarie University and by an IPRS scholarship to IDM. MAC was supported by the project PTDC/BIA-CBI/28014/2017. JLR was supported by an Endeavour postdoctoral fellowship, as well as a Claude Leon Foundation and NSERC postdoctoral fellowships.
Author information
Authors and Affiliations
Contributions
IDM implemented and performed the experiment, and drafted the first manuscript; IDM and JLR analysed the data. All authors conceived and designed the experiment, and substantially contributed to the final version of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethics approval
All applicable institutional and/or national guidelines for the care and use of animals were followed. Research was approved by the Macquarie University Animal Ethics Committee (ARA2017/004) and by the Portuguese Institute for Conservation of Nature and Forests (ICNF) (License 428/2017/CAPT).
Consent for publication
All authors agree with this publication.
Additional information
Communicated by S. Joy Downes
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOCX 263 kb)
Rights and permissions
About this article
Cite this article
Damas-Moreira, I., Riley, J.L., Carretero, M.A. et al. Getting ahead: exploitative competition by an invasive lizard. Behav Ecol Sociobiol 74, 117 (2020). https://doi.org/10.1007/s00265-020-02893-2
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00265-020-02893-2