Behavioral shifts with urbanization may facilitate biological invasion of a widespread lizard

  • James T. StroudEmail author
  • Marie Colom
  • Pedro Ferrer
  • Nicholas Palermo
  • Veronica Vargas
  • Martina Cavallini
  • Jesus Lopez
  • Ian Jones


Understanding how novel environmental conditions presented by urbanization affect the ecology and behavior of species is an important component of global change biology. Behavior is the first way in which organisms respond to novel conditions. We investigated differences in habitat use, movement, and social behavior of invasive adult male Cuban brown anoles (Anolis sagrei) in natural and urban areas in Miami, FL. We observed that urban lizards used broader perches and frequented more artificial human-made substrates (e.g. walls) than lizards in a natural forest habitat. Extensive behavioral observations (ca. 1200 min) revealed that urban A. sagrei also performed more dewlap displays, changed perches less, and jumped less. Our analysis of the structural environment revealed that urban areas are more open – in other words, have higher visibility at typical lizard perch heights, and have fewer and broader perches than natural areas. An increase in openness may explain why we observed a greater than two-fold increase in the frequency of dewlap displaying – the primary mechanism of visual communication in anoles. Similarly, less perch changes and fewer jumps – a form of locomotion frequently used in perch-perch movement when perches are close – is likely driven by a three-fold decrease in tree density. Understanding how behavior and ecology differ in urban vs. natural ecosystems provides insight into how species persist in urban landscapes, and how such behavioral shifts might facilitate biological invasions.


Anolis sagrei Florida Urbanization Invasive species Behavior Urban ecology 



This manuscript was improved significantly with comments from Jason Kolbe. JTS was supported by a DEA and DYF Fellowship from Florida International University. We would like to thank all students of the Spring 2016 QBIC Ecology Lab for help in collecting data on structural habitat.


  1. Aviles-Rodriguez KJ (2015) Do urban environments influence antipredator and foraging behavior of the lizard Anolis cristatellus? University of Rhode Island; Open Access Master's Theses. Paper 544.
  2. Baeckens S, Driessens T, Van Damme R (2018) The brown anole dewlap revisited: do predation pressure, sexual selection, and species recognition shape among-population signal diversity? PeerJ 6:e4722CrossRefGoogle Scholar
  3. Basquill SP, Grant JW (1998) An increase in habitat complexity reduces aggression and monopolization of food by zebra fish (Danio rerio). Can J Zool 76:770–772CrossRefGoogle Scholar
  4. Battles AC (2018) The Effects of Urbanization on Performance, Habitat Selection, and Persistence of Anolis Lizards. University of Rhode Island; Open Access Dissertations. Paper 731.
  5. Battles AC, Kolbe JJ (2018) Miami heat: urban heat islands influence the thermal suitability of habitats for ectotherms. Glob Chang Biol.
  6. Battles AC, Moniz M, Kolbe JJ (2018) Living in the big city: preference for broad substrates results in niche expansion for urban Anolis lizards. Urban Ecosyst 21:1087–1095CrossRefGoogle Scholar
  7. Blamires SJ (1999) Factors influencing the escape response of an arboreal agamid lizard of tropical Australia (Lophognathus temporalis) in an urban environment. Can J Zool 77:1998–2003CrossRefGoogle Scholar
  8. Butler MA, Schoener TW, Losos JB (2000) The relationship between sexual size dimorphism and habitat use in greater Antillean Anolis lizards. Evolution 54:259–272PubMedGoogle Scholar
  9. Chejanovski ZA, Avilés-Rodríguez KJ, Lapiedra O, Preisser EL, Kolbe JJ (2017) An experimental evaluation of foraging decisions in urban and natural forest populations of Anolis lizards. Urban Ecosyst 20:1011–1018CrossRefGoogle Scholar
  10. Ditchkoff SS, Saalfeld ST, Gibson CJ (2006) Animal behavior in urban ecosystems: modifications due to human induced stress. Urban Ecosyst 9:5–12CrossRefGoogle Scholar
  11. Driessens T, Vanhooydonck B, Van Damme R (2013) Deterring predators, daunting opponents or drawing partners? Signaling rates across diverse contexts in the lizard Anolis sagrei. Behav Ecol Sociobiol 68:173–184CrossRefGoogle Scholar
  12. Driessens T, Huyghe K, Vanhooydonck B, Van Damme R (2015) Messages conveyed by assorted facets of the dewlap, in both sexes of Anolis sagrei. Behav Ecol Sociobiol 69:1251–1264CrossRefGoogle Scholar
  13. Eason PK, Stamps JA (1992) The effect of visibility on territory size and shape. Behav Ecol 3:166–172CrossRefGoogle Scholar
  14. Edwards JR, Lailvaux SP (2012) Display behavior and habitat use in single and mixed populations of Anolis carolinensis and Anolis sagrei lizards. Ethology 118:494–502CrossRefGoogle Scholar
  15. Fischer JD, Cleeton SH, Lyons TP, Miller JR (2012) Urbanization and the predation paradox: the role of trophic dynamics in structuring vertebrate communities. Bioscience 62:809–818CrossRefGoogle Scholar
  16. Giery ST, Layman CA (2015) Interpopulation variation in a condition-dependent signal: predation regime affects signal intensity and reliability. Am Nat 186:187–195CrossRefGoogle Scholar
  17. Greenberg R, Mettke-Hofmann C (2001) Ecological aspects of neophobia and neophilia in birds. Curr Ornithol 16:119–178Google Scholar
  18. Greggor AL, Clayton NS, Fulford A, Thornton A (2016) Street smart: faster approach towards litter in urban areas by highly neophobic corvids and less fearful birds. Anim Behav 117:123–133CrossRefGoogle Scholar
  19. Gunderson AR, Leal M (2015) Patterns of thermal constraint on ectotherm activity. Am Nat 185:653–664CrossRefGoogle Scholar
  20. Hasegawa K, Ishiyama N, Kawai H (2014) Replacement of nonnative rainbow trout by nonnative brown trout in the Chitose River system, Hokkaido, northern Japan. Aquat Invasions 9:221–226CrossRefGoogle Scholar
  21. Helmus MR, Mahler DL, Losos JB (2014) Island biogeography of the Anthropocene. Nature 513:543–546CrossRefGoogle Scholar
  22. Henderson RW, Powell R (2001) Responses by the west Indian herpetofauna to human-influenced resources. Caribb J Sci 37:41–54Google Scholar
  23. Irschick DJ, Losos JB (1998) A comparative analysis of the ecological significance of maximal locomotor performance in Caribbean Anolis lizards. Evolution 52:219–226CrossRefGoogle Scholar
  24. Johnson MA, Wade J (2010) Behavioural display systems across nine Anolis lizard species: sexual dimorphisms in structure and function. Proc Biol Sci 277:1711–1719CrossRefGoogle Scholar
  25. Johnson MA, Revell LJ, Losos JB (2010) Behavioral convergence and adaptive radiation: effects of habitat use on territorial behavior in Anolis lizards. Evolution 64:1151–1159CrossRefGoogle Scholar
  26. Kenneth BH, Innes JL, Martin K, Klinkenberg B (2005) Forest loss with urbanization predicts bird extirpations in Vancouver. Biol Conserv 126:410–419CrossRefGoogle Scholar
  27. Klomp DA, Ord TJ, Das I, Diesmos A, Ahmad N, Stuart-Fox D (2016) Ornament size and colour as alternative strategies for effective communication in gliding lizards. J Evol Biol 29:1689–1700CrossRefGoogle Scholar
  28. Kolbe JJ, Larson A, Losos JB (2007) Differential admixture shapes morphological variation among invasive populations of the lizard Anolis sagrei. Mol Ecol 16:1579–1591CrossRefGoogle Scholar
  29. Kolbe JJ, Leal M, Schoener TW, Spiller DA, Losos JB (2012) Founder effects persist despite adaptive differentiation: a replicated field experiment in lizards. Science 335:1086–1089CrossRefGoogle Scholar
  30. Kolbe JJ, Battles AC, Avilés-Rodríguez KJ (2016a) City slickers: poor performance does not deter Anolis lizards from using artificial substrates in human-modified habitats. Funct Ecol 30:1418–1429CrossRefGoogle Scholar
  31. Kolbe JJ, VanMiddlesworth P, Battles AC, Stroud JT, Buffum B, Forman RTT, Losos JB (2016b) Determinants of spread in an urban landscape by an introduced lizard. Landsc Ecol 31:1795–1813CrossRefGoogle Scholar
  32. Kolbe JJ, Wegener JE, Stuart YE, Milstead U, Boronow KE, Harrison AS, Losos JB (2017) An incipient invasion of brown anole lizards (Anolis sagrei) into their own native range in the Cayman Islands: a case of cryptic back-introduction. Biol Invasions 19:1989–1998CrossRefGoogle Scholar
  33. Kühn I, Klotz S (2006) Urbanization and homogenization–comparing the floras of urban and rural areas in Germany. Biol Conserv 127:292–300CrossRefGoogle Scholar
  34. Lapiedra O, Chejanovski Z, Kolbe JJ (2017) Urbanization and biological invasion shape animal personalities. Glob Chang Biol 23:592–603CrossRefGoogle Scholar
  35. Leal M, Fleishman LJ (2003) Differences in visual signal design and detectability between allopatric populations of Anolis lizards. Am Nat 163:26–39CrossRefGoogle Scholar
  36. Lee JC, Clayton D, Eisenstein S, Perez I (1989) The reproductive cycle of Anolis sagrei in southern Florida. Copeia 1989:930–937CrossRefGoogle Scholar
  37. Losos JB (2009) Lizards in an evolutionary tree: ecology and adaptive radiation of anoles. University of California Press, BerkeleyGoogle Scholar
  38. Losos JB, Warheit KI, Schoener TW (1997) Adaptive differentiation following experimental island colonization in Anolis lizards. Nature 387:70–73CrossRefGoogle Scholar
  39. Marnocha E, Pollinger J, Smith TB (2011) Human-induced morphological shifts in an island lizard. Evol Appl 4:388–396CrossRefGoogle Scholar
  40. Marzluff JM et al (2001) In: Marzluff JM, Bowman R, Donelly R (eds) Avian ecology and conservation in an urbanizing world. Kluwer Academic Press, Norwell, pp 332–363CrossRefGoogle Scholar
  41. McDonnell MJ, Hahs AK (2015) Adaptation and adaptedness of organisms to urban environments. Annu Rev Ecol Evol Syst 46:261–280CrossRefGoogle Scholar
  42. McKinney ML (2002) Urbanization, biodiversity, and conservation. Bioscience 52:883–890CrossRefGoogle Scholar
  43. Meshaka WE Jr (2011) A runaway train in the making: the exotic amphibians, reptiles, turtles, and crocodilians of Florida. Herpetol Conserv Biol 6:1–101Google Scholar
  44. Nemeth E, Brumm H (2009) Blackbirds sing higher-pitched songs in cities: adaptation to habitat acoustics or side-effect of urbanization? Anim Behav 78:637–641CrossRefGoogle Scholar
  45. Nicholson KE, Harmon LJ, Losos JB (2007) Evolution of Anolis lizard dewlap diversity. PLoS One 2:e274CrossRefGoogle Scholar
  46. Niemelä J (1999) Ecology and urban planning. Biodivers Conserv 8:119–131CrossRefGoogle Scholar
  47. Parmley D (2002) Northernmost record of the brown anole (Anolis sagrei) in Georgia. Ga J Sci 60:191–193Google Scholar
  48. Perry G, Buchanan BW, Fisher RN, Salmon M, Wise SE (2008) Effects of artificial night lighting on amphibians and reptiles in urban environments. In: Mitchell JC, Brown RE, Bartholomew B (eds) Urban Herpetology. Herpetological Conservation, Number 3, Society for the Study of Amphibians and reptiles, Salt Lake City, pp 239–256Google Scholar
  49. Prum RO (2012) Aesthetic evolution by mate choice: Darwin's really dangerous idea. Philos Trans R Soc B: Biol Sci 367:2253–2265CrossRefGoogle Scholar
  50. Prum RO (2017) The evolution of beauty: how Darwin’s forgotten theory of mate choice shapes theanimal kingdom—and us. Doubleday, New YorkGoogle Scholar
  51. Rand AS, Williams EE (1970) An estimation of redundancy and information content of anole dewlaps. Am Nat 104:99–103CrossRefGoogle Scholar
  52. R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL Accessed 07/15/2018
  53. Rodda GH, Tyrrell CL (2008) Introduced species that invade and species that thrive in town: are these two groups cut from the same cloth? Urban herpetology: herpetological conservation, Vol. 3 (ed. by J.C. Mitchell, R.E. Jung Brown and B. Bartholomew), 327–341. Society for the Study of Amphibians & Reptiles, Salt Lake CityGoogle Scholar
  54. RStudio Team (2015) RStudio: Integrated Development for R. RStudio, Inc., Boston, MA URL Accessed 07/15/2018
  55. Scott MP (1984) Agonistic and courtship displays of male Anolis sagrei. Breviora 479:1–22Google Scholar
  56. Shochat E, Warren PS, Faeth SH, McIntyre NE, Hope D (2006) From patterns to emerging processes in mechanistic urban ecology. Trends Ecol Evol 21:186–191CrossRefGoogle Scholar
  57. Simberloff D, Rejmánek M (eds) (2011) Encyclopedia of biological invasions. University ofCalifornia Press, BerkeleyGoogle Scholar
  58. Simon VB (2007) Not all signals are equal: male Brown Anole lizards (Anolis sagrei) selectively decrease pushup frequency following a simulated predatory attack. Ethology 113:793–801CrossRefGoogle Scholar
  59. Snell-Rood EC (2013) An overview of the evolutionary causes and consequences of behavioural plasticity. Anim Behav 85:1004–1011CrossRefGoogle Scholar
  60. Sol D, Lapiedra O, González-Lagos C (2013) Behavioural adjustments for a life in the city. Anim Behav 85:1101–1112CrossRefGoogle Scholar
  61. Stamps JA (1977) Social behavior and spacing patterns in lizards. In: Gans C, Tinkle DW (eds) Biology of the Reptilia, vol 7. Academic Press, London, pp 265–334Google Scholar
  62. Steinberg DS, Losos JB, Schoener TW, Spiller DA, Kolbe JJ, Leal M (2014) Predation-associated modulation of movement-based signals by a Bahamian lizard. Proc Natl Acad Sci U S A 111:9187–9192CrossRefGoogle Scholar
  63. Stroud JT, Giery ST, Outerbridge ME (2017) Establishment of Anolis sagrei on Bermuda represents a novel ecological threat to critically endangered Bermuda skinks (Plestiodon longirostris). Biol Invasions 19:1723–1731CrossRefGoogle Scholar
  64. Tyler KR, Winchell KM, Revell LJ (2016) Tails of the City: caudal autotomy in the tropical lizard, Anolis cristatellus, in urban and natural areas of Puerto Rico. J Herpetol 50:435–441CrossRefGoogle Scholar
  65. Winchell KM, Reynolds RG, Prado-Irwin SR, Puente-Rolón AR, Revel LJ (2016) Phenotypic shifts in urban areas in the tropical lizard Anolis cristatellus. Evolution 70:1009–F1022CrossRefGoogle Scholar
  66. Winchell KM, Maayan I, Fredette JR, Revell LJ (2018) Linking locomotor performance to morphological shifts in urban lizards. Proc R Soc B 285:20180229CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of BiologyWashington University in St. LouisSt. LouisUSA
  2. 2.Quantifying Biology In the Classroom (QBIC)Florida International UniversityMiamiUSA
  3. 3.Department of BiologyFlorida International UniversityMiamiUSA
  4. 4.ARS-USDA Invasive Plant Research LaboratoryFort LauderdaleUSA

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