Urban Ecosystems

, Volume 20, Issue 5, pp 1011–1018 | Cite as

An experimental evaluation of foraging decisions in urban and natural forest populations of Anolis lizards

  • Zachary A. Chejanovski
  • Kevin J. Avilés-Rodríguez
  • Oriol Lapiedra
  • Evan L. Preisser
  • Jason J. Kolbe


Foraging decisions reflect a trade-off between the benefits of acquiring food and the costs of movement. Changes in the biotic and abiotic environment associated with urbanization can alter this trade-off and modify foraging decisions. We experimentally manipulated foraging opportunities for two Anolis lizard species – the brown anole (A. sagrei) in Florida and the crested anole (A. cristatellus) in Puerto Rico – to assess whether foraging behavior differs between habitats varying in their degree of urbanization. In both urban and natural forest habitats, we measured the latency of perched anoles to feed from an experimental feeding tray. We manipulated perch availability and predator presence, while also taking into account population (e.g., conspecific density) and individual-level factors (e.g., body temperature) to evaluate whether and how these contribute to between-habitat differences in foraging behavior. In both species, urban anoles had longer latencies to feed and lower overall response rates compared to lizards from forests. Urban anoles were also larger (i.e., snout-vent length and mass) in both species and urban A. sagrei were in better body condition than the natural forest population. We postulate that the observed patterns in foraging behavior are driven by differences in perceived predation risk, foraging motivation, or neophobia. Although we are unable to identify the mechanism(s) driving these differences, the substantial differences in urban versus forest anole foraging behavior emphasizes the importance of understanding how urbanization influences animal populations and their persistence in anthropogenically-modified environments.


Foraging behavior Motivation Predation risk Structural habitat Urbanization 



This research was funded by a grant from the National Science Foundation (DEB-1354897) and funds from the University of Rhode Island. Protocols for use of vertebrate animals in this study were approved by the Institutional Animal Care and Use Committee at the University of Rhode Island (AN11-09-005). Permits were provided by Broward County Parks and Recreation (Florida) (ES01152015-001). We thank the University of Puerto Rico for permission to conduct this study on their property and the staff of the Museum of Zoology at the University of Puerto Rico for laboratory space and logistical support. Christopher Thawley provided important suggestions for our body condition analysis.


  1. Adolph SC, Roughgarden J (1983) Foraging by passerine birds and Anolis lizards on St. Eustatius (Neth. Antilles): implications for interclass competition, and predation. Oecologia 56:313–317CrossRefPubMedGoogle Scholar
  2. Angilletta MJ (2009) Thermal adaptation: a theoretical and empirical synthesis. Oxford University PressGoogle Scholar
  3. Audet J-N, Ducatez S, Lefebvre L (2016) The town bird and the country bird: problem solving and immunocompetence vary with urbanization. Behav Ecol 27:637–644CrossRefGoogle Scholar
  4. Bachman GC (1993) The effect of body condition on the trade-off between vigilance and foraging in Belding’s ground squirrels. Anim Behav 46:233–244CrossRefGoogle Scholar
  5. Baker PJ, Bentley AJ, Ansell RJ, Harris S (2005) Impact of predation by domestic cats Felis catus in an urban area. Mamm Rev 35:302–312CrossRefGoogle Scholar
  6. Baker MAA, Emerson SE, Brown JS (2015) Foraging and habitat use of eastern cottontails (Sylvilagus floridanus) in an urban landscape. Urban Ecosyst 18:977–987CrossRefGoogle Scholar
  7. Blair RB (1996) Land use and avian species diversity along an urban gradient. Ecol Appl 6:506–519CrossRefGoogle Scholar
  8. Bouskila A (1995) Interactions between predation risk and competition: a field study of kangaroo rats and snakes. Ecology 76:165–178CrossRefGoogle Scholar
  9. Bowers MA, Breland B (1996) Foraging of gray squirrels on an urban-rural gradient: use of the GUD to assess anthropogenic impact. Ecol Appl 6:1135–1142CrossRefGoogle Scholar
  10. Bowers MA, Jefferson JL, Kuebler MG (1993) Variation in giving-up densities of foraging chipmunks (Tamias striatus) and squirrels (Sciurus carolinensis). Oikos 66:229–236CrossRefGoogle Scholar
  11. Burnham KP, Anderson DR (2004) Multimodel inference: understanding AIC and BIC in model selection. Sociol Methods Res 33:261–304CrossRefGoogle Scholar
  12. Candler S, Bernal XE (2015) Differences in neophobia between cane toads from introduced and native populations. Behav Ecol 26:97–104CrossRefGoogle Scholar
  13. Clergeau P, Savard J-PL, Mennechez G, Falardeau G (1998) Bird abundance and diversity along an urban-rural gradient: a comparative study between two cities on different continents. Condor 100:413–425CrossRefGoogle Scholar
  14. Cooper WE (2006) Risk factors affecting escape behaviour by Puerto Rican Anolis lizards. Can J Zool 84:495–504CrossRefGoogle Scholar
  15. Cooper WE (2010) Escape tactics and effects of perch height and habituation on flight initiation distance in two Jamaican anoles (Squamata: Polychrotidae). Rev Biol Trop 58:1199–1209PubMedGoogle Scholar
  16. Cooper WE, Peréz-Mellado V, Hawlena D (2006) Magnitude of food reward affects escape behavior and acceptable risk in Balearic lizards, Podarcis lilfordi. Behav Ecol 17:554–559CrossRefGoogle Scholar
  17. Croci S, Butet A, Clergeau P (2008) Does urbanization filter birds on the basis of their biological traits? Condor 110:223–240CrossRefGoogle Scholar
  18. Crooks KR, Soule ME (1999) Mesopredator release and avifaunal extinctions in a fragmented system. Nature 400:563–566CrossRefGoogle Scholar
  19. Dall SRX, Giraldeau L-A, Olsson O et al (2005) Information and its use by animals in evolutionary ecology. Trends Ecol Evol 20:187–193CrossRefPubMedGoogle Scholar
  20. Dinno A (2016) Package ‘dunn.test’Google Scholar
  21. Ditchkoff SS, Saalfeld ST, Gibson CJ (2006) Animal behavior in urban ecosystems: modifications due to human-induced stress. Urban Ecosyst 9:5–12CrossRefGoogle Scholar
  22. Drakeley M, Lapiedra O, Kolbe JJ (2015) Predation risk perception, food density and conspecific cues shape foraging decisions in a tropical lizard. PLoS One 10:e0138016CrossRefPubMedPubMedCentralGoogle Scholar
  23. Finke DL, Denno RF (2002) Intraguild predation diminished in complex-structured vegetation: implications for prey suppression. Ecology 83:643–652CrossRefGoogle Scholar
  24. Fischer JD, Cleeton SH, Lyons TP et al (2012) Urbanization and the predation paradox: the role of trophic dynamics in structuring vertebrate communities. Bioscience 62:809–818CrossRefGoogle Scholar
  25. Forman R (2014) Urban ecology: science of cities. Cambridge University PressGoogle Scholar
  26. Greenberg R (1990) Feeding neophobia and ecological plasticity: a test of the hypothesis with captive sparrows. Anim Behav 39:375–379CrossRefGoogle Scholar
  27. Greenberg R, Mettke-Hofmann C (2001) Ecological aspects of neophobia and neophilia in birds. Curr Ornithol 16:119–178Google Scholar
  28. Gunderson AR, Leal M (2015) Patterns of thermal constraint on ectotherm activity. Am Nat 185:653–664CrossRefPubMedGoogle Scholar
  29. Harwood RH (1979) The effect of temperature on the digestive efficiency of three species of lizards, Cnemidophorus tigris, Rrhonotus multicarinatus, and Sceloporus occidentalis. Comp Biochem Physiol Part A Physiol 63:417–433CrossRefGoogle Scholar
  30. Hendry AP, Farrugia TJ, Kinnison MT (2008) Human influences on rates of phenotypic change in wild animal populations. Mol Ecol 17:20–29CrossRefPubMedGoogle Scholar
  31. Hertz PE (1992) Temperature regulation in Puerto Rican Anolis lizards: a field test using null hypotheses. Ecology 73:1405–1417CrossRefGoogle Scholar
  32. Hodgson P, French K, Major RE (2006) Comparison of foraging behaviour of small, urban-sensitive insectivores in continuous woodland and woodland remnants in a suburban landscape. Wildl Res 33:591–603CrossRefGoogle Scholar
  33. Irschick DJ, Losos JB (1999) Do lizards avoid habitats in which performance is submaximal? The relationship between sprinting capabilities and structural habitat use in Caribbean anoles. Am Nat 154:293–305CrossRefPubMedGoogle Scholar
  34. Jakob EM, Marshall SD, Uetz GW (1996) Estimating fitness: a comparison of body condition indices. Oikos 77:61–67CrossRefGoogle Scholar
  35. Jokimäki J, Huhta E (2000) Artificial nest predation and abundance of birds along an urban gradient. Condor 102:838–847CrossRefGoogle Scholar
  36. Kolbe JJ, Battles AC, Avilés-Rodríguez KJ (2015) City slickers: poor performance does not deter Anolis lizards from using artificial substrates in human-modified habitats. Funct Ecol doi. doi: 10.1111/1365-2435.12607 Google Scholar
  37. Kotler BP, Brown JS, Bouskila A (2004) Apprehension and time allocation in gerbils: the effects of predatory risk and energetic state. Ecology 85:917–922CrossRefGoogle Scholar
  38. Lapiedra O, Chejanovski ZA, Kolbe JJ (2017) Urbanization and biological invasion shape animal personalities. Glob Change Biol 23:592–603. doi: 10.1111/gcb.13395 CrossRefGoogle Scholar
  39. Leal M (1999) Honest signalling during prey–predator interactions in the lizard Anolis cristatellus. Anim Behav 58:521–526CrossRefPubMedGoogle Scholar
  40. Lepczyk C (2003) Landowners and cat predation across rural-to-urban landscapes. Biol Conserv 115:191–201CrossRefGoogle Scholar
  41. Lima SL, Bednekoff PA (1999) Temporal variation in danger drives antipredator behavior: the predation risk allocation hypothesis. Am Nat 153:649–659CrossRefGoogle Scholar
  42. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640CrossRefGoogle Scholar
  43. Losos JB (1990) Ecomorphology, performance capability, and scaling of west Indian Anolis lizards: an evolutionary analysis. Ecol Monogr 60:369–388CrossRefGoogle Scholar
  44. Losos JB (2009) Lizards in an evolutionary tree: ecology and adaptive radiation of anoles. University of California PressGoogle Scholar
  45. Losos JB, Sinervo B (1989) The effects of morphology and perch diameter on sprint performance of Anolis lizards. J Exp Biol 145:23–30Google Scholar
  46. Losos JB, Schoener TW, Spiller DA (2004) Predator-induced behaviour shifts and natural selection in field-experimental lizard populations. Nature 432:505–508CrossRefPubMedGoogle Scholar
  47. Martin J, López P (1995) Influence of habitat structure on the escape tactics of the lizard Psammodromus algirus. Can J Zool 73:129–132CrossRefGoogle Scholar
  48. Møller AP (2008) Flight distance of urban birds, predation, and selection for urban life. Behav Ecol Sociobiol 63:63–75CrossRefGoogle Scholar
  49. Moulé H, Michelangeli M, Thompson MB, Chapple DG (2015) The influence of urbanization on the behaviour of an Australian lizard and the presence of an activity-exploratory behavioural syndrome. J Zool 298:103–111CrossRefGoogle Scholar
  50. Oke TR (1973) City size and the urban heat island. Atmos Environ 7:769–779CrossRefGoogle Scholar
  51. Ordeñana MA, Crooks KR, Boydston EE et al (2010) Effects of urbanization on carnivore species distribution and richness. J Mammal 91:1322–1331CrossRefGoogle Scholar
  52. Peig J, Green AJ (2009) New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118:1883–1891Google Scholar
  53. Prange S, Gehrt SD, Wiggers EP (2004) Influences of anthropogenic resources on raccoon (Procyon lotor) movements and spatial distribution. J Mammal 85:483–490CrossRefGoogle Scholar
  54. R Development Core Team (2015) R: A language and environment for statistical computing.Google Scholar
  55. Roberts G (1996) Why individual vigilance declines as group size increases. Anim Behav 51:1077–1086CrossRefGoogle Scholar
  56. Rodewald AD, Kearns LJ, Shustack DP (2011) Anthropogenic resource subsidies decouple predator–prey relationships. Ecol Appl 21:936–943CrossRefPubMedGoogle Scholar
  57. Rogers CM, Caro MJ (1998) Song sparrows, top carnivores and nest predation: a test of the mesopredator release hypothesis. Oecologia 116:227–233CrossRefPubMedGoogle Scholar
  58. Schoener TW, Spiller DA, Losos JB (2002) Predation on a common Anolis lizard: can the food-web effects of a devastating predator be reversed? Ecol Monogr 72:383–407CrossRefGoogle Scholar
  59. Scott NJ, Wilson DE, Jones C, Andrews RM (1976) The choice of perch dimensions by lizards of the genus Anolis (Reptilia, Lacertilia, Iguanidae). J Herpetol 10:75–84CrossRefGoogle Scholar
  60. Shepard DB (2007) Habitat but not body shape affects predator attack frequency on lizard models in the Brazilian Cerrado. Herpetologica 63:193–202CrossRefGoogle Scholar
  61. Shochat E, Lerman SB, Katti M, Lewis DB (2004) Linking optimal foraging behavior to bird community structure in an urban-desert landscape: field experiments with artificial food patches. Am Nat 164:232–243PubMedGoogle Scholar
  62. Shochat E, Warren PS, Faeth SH et al (2006) From patterns to emerging processes in mechanistic urban ecology. Trends Ecol Evol 21:186–191CrossRefPubMedGoogle Scholar
  63. Sims V, Evans KL, Newson SE et al (2008) Avian assemblage structure and domestic cat densities in urban environments. Divers Distrib 14:387–399CrossRefGoogle Scholar
  64. Smith MM, Smith HT, Engeman RM (2004) Extensive contiguous north–south range expansion of the original population of an invasive lizard in Florida. Int Biodeterior Biodegradation 54:261–264CrossRefGoogle Scholar
  65. Sol D, Griffin AS, Bartomeus I, Boyce H (2011) Exploring or avoiding novel food resources? The novelty conflict in an invasive bird. PLoS One 6:e19535CrossRefPubMedPubMedCentralGoogle Scholar
  66. Sol D, Lapiedra O, González-Lagos C (2013) Behavioural adjustments for a life in the city. Anim Behav 85:1101–1112CrossRefGoogle Scholar
  67. Sorace A (2002) High density of bird and pest species in urban habitats and the role of predator abundance. Ornis Fenn 79:60–71Google Scholar
  68. Sorace A, Gustin M (2009) Distribution of generalist and specialist predators along urban gradients. Landsc Urban Plan 90:111–118CrossRefGoogle Scholar
  69. Soulé ME, Bolger DT, Alberts AC et al (1988) Reconstructed dynamics of rapid extinctions of chaparral-requiring birds in urban habitat islands. Conserv Biol 2:75–92CrossRefGoogle Scholar
  70. Stamps JA (1977) The function of the survey posture in Anolis lizards. Copeia 1977:756–758CrossRefGoogle Scholar
  71. Stamps JA (1987) Conspecifics as cues to territory quality: a preference of juvenile lizards (Anolis aeneus) for previously used territories. Am Nat 129:629–642CrossRefGoogle Scholar
  72. Stephens DW, Krebs JR (1986) Foraging theory. Princeton University PressGoogle Scholar
  73. Therneau TM, Lumley T (2015) Package 'survival'Google Scholar
  74. Tokarz RR (1985) Body size as a factor determining dominance in staged agonistic encounters between male brown anoles (Anolis sagrei). Anim Behav 33:746–753CrossRefGoogle Scholar
  75. Valcarcel A, Fernández-Juricic E (2009) Antipredator strategies of house finches: are urban habitats safe spots from predators even when humans are around? Behav Ecol Sociobiol 63:673–685CrossRefGoogle Scholar
  76. Verdolin JL (2006) Meta-analysis of foraging and predation risk trade-offs in terrestrial systems. Behav Ecol Sociobiol 60:457–464CrossRefGoogle Scholar
  77. Whittingham MJ, Evans KL (2004) The effects of habitat structure on predation risk of birds in agricultural landscapes. Ibis 146:210–220CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  • Zachary A. Chejanovski
    • 1
  • Kevin J. Avilés-Rodríguez
    • 1
    • 2
  • Oriol Lapiedra
    • 1
    • 3
  • Evan L. Preisser
    • 1
  • Jason J. Kolbe
    • 1
  1. 1.Department of Biological SciencesUniversity of Rhode IslandKingstonUSA
  2. 2.Department of BiologyUniversity of Massachusetts BostonBostonUSA
  3. 3.Department of Organismic and Evolutionary BiologyHarvard UniversityCambridgeUSA

Personalised recommendations