Behavioral Ecology and Sociobiology

, Volume 63, Issue 11, pp 1563–1572 | Cite as

Body size and reserve protection affect flight initiation distance in parrotfishes

  • Kiyoko M. Gotanda
  • Katrine Turgeon
  • Donald L. KramerEmail author
Original Paper


Flight initiation distance (FID), the distance at which an organism begins to flee an approaching threat, is an important component of antipredator behavior and a potential indicator of an animal’s perception of threat. In a field study on parrotfishes, we tested the predictions that FID in response to a diver will increase with body size, a correlate of reproductive value, and with experience of threat from humans. We studied a broad size range in four species on fringing reefs inside and outside the Barbados Marine Reserve. We used the Akaike's Information Criterion modified for small sample sizes (AICc) and model averaging to select and assess alternative models. Body size, reserve protection, and distance to a refuge, but not species, had strong support in explaining FID. FID increased with body size and generally remained two to ten times fish total length. FID was greater outside the reserve, especially in larger fish. Although we were not able to completely rule out other effects of size or reserve, this study supports predictions of an increase in FID with reproductive value and threat from humans.


Marine protected area Reaction distance Scarus Sparisoma Spearfishing 



We gratefully acknowledge the Bellairs Research Institute and High Tide Watersports in Barbados for help and support during this study. We also thank the McGill Behavioural Ecology Discussion Group, Bob Warner, and Larry Dill for helpful suggestions on various versions of this manuscript. The insights of W. E. Cooper and two anonymous referees were very helpful. This work was supported by the Natural Sciences and Engineering Research Council of Canada (NSERC) [RGPIN/213-2003 to D.L.K; an Undergraduate Science Research Award to K.M.G.; a postgraduate scholarship to K.T.]. Our research complied with the ABS/ASAB Guidelines for the Treatment of Animals in Behavioral Research and Teaching and was approved by the McGill University Animal Care Committee, Animal Use Protocol 5039.


  1. Abrahams MV (1995) The interaction between antipredator behaviour and antipredator morphology: experiments with fathead minnows and brook sticklebacks. Can J Zool 73:2209–2215CrossRefGoogle Scholar
  2. Anderson DR, Link WA, Johnson DH, Burnham KP (2001) Suggestions for presenting the results of data analyses. J Wildl Manag 65:373–378CrossRefGoogle Scholar
  3. Baudains TP, Lloyd P (2007) Habituation and habitat changes can moderate the impacts of human disturbance on shorebird breeding performance. Anim Conserv 10:400–407CrossRefGoogle Scholar
  4. Berger S, Wikelski M, Romero LM, Kalko EK, Roedl T (2007) Behavioral and physiological adjustments to new predators in an endemic island species, the Galápagos marine iguana. Horm Behav 52:653–663PubMedCrossRefGoogle Scholar
  5. Blumstein DT (2003) Flight-initiation distance in birds is dependent on intruder starting distance. J Wildl Manag 67:852–857CrossRefGoogle Scholar
  6. Blumstein DT (2006) Developing an evolutionary ecology of fear: how life history and natural history traits affect disturbance tolerance in birds. Anim Behav 71:389–399CrossRefGoogle Scholar
  7. Booth CL (1990) Evolutionary significance of ontogenic color-change in animals. Biol J Linn Soc 40:125–163CrossRefGoogle Scholar
  8. Breck JE, Gitter MJ (1983) Effect of fish size on the reactive distance of bluegill (Lepomis macrochirus) sunfish. Can J Fish Aquat Sci 40:162–167CrossRefGoogle Scholar
  9. Brown GE (2003) Learning about danger: chemical alarm cues and local risk assessment in prey fishes. Fish Fish 4:227–234Google Scholar
  10. Bulova SJ (1994) Ecological correlates of population and individual variation in antipredator behavior of 2 species of desert lizards. Copeia 1994:980–992CrossRefGoogle Scholar
  11. Burger J (1991) Foraging behavior and the effect of human disturbance on the piping plover (Charadrius melodus). J Coast Res 7:39–52Google Scholar
  12. Burger J, Gochfeld M (1990) Risk discrimination of direct versus tangential approach by basking black iguanas (Ctenosaura similis): variation as a function of human exposure. J Comp Psychol 104:388–394CrossRefGoogle Scholar
  13. Burger J, Gochfeld M, Murray BG (1991) Role of a predator's eye size in risk perception by basking black iguana, Ctenosaura similis. Anim Behav 42:471–476CrossRefGoogle Scholar
  14. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New YorkGoogle Scholar
  15. Chapman MR, Kramer DL (1999) Gradients in coral reef fish density and size across the Barbados Marine Reserve boundary: effects of reserve protection and habitat characteristics. Mar Ecol Prog Ser 181:81–96CrossRefGoogle Scholar
  16. Chapman MR, Kramer DL (2000) Movements of fishes within and among fringing coral reefs in Barbados. Environ Biol Fishes 57:11–24CrossRefGoogle Scholar
  17. Clark CW (1994) Antipredator behavior and the asset-protection principle. Behav Ecol 5:159–170CrossRefGoogle Scholar
  18. Cooper WE (2005) When and how do predator starting distances affect flight initiation distances? Can J Zool 83:1045–1050CrossRefGoogle Scholar
  19. Cooper WE (2008) Strong artifactual effect of starting distance on flight initiation distance in the actively foraging lizard Aspidoscelis exsanguis. Herpetologica 64:200–206CrossRefGoogle Scholar
  20. Cooper WE, Frederick WG (2007) Optimal flight initiation distance. J Theor Biol 244:59–67PubMedCrossRefGoogle Scholar
  21. Cooper WE, Whiting MJ (2007) Effects of risk on flight initiation distance and escaped tactics in two southern African lizard species. Acta Zool Sin 53:446–453Google Scholar
  22. Deecke VB, Slater PJB, Ford JKB (2002) Selective habituation shapes acoustic predator recognition in harbour seals. Nature 420:171–173PubMedCrossRefGoogle Scholar
  23. Domenici P (2002) The visually mediated escape response in fish: predicting prey responsiveness and the locomotor behaviour of predators and prey. Mar Freshw Behav Physiol 35:87–110CrossRefGoogle Scholar
  24. Fernandez-Juricic E, Blumstein DT, Abrica G, Manriquez L, Adams LB, Adams R, Daneshrad M, Rodriguez-Prieto I (2006) Relationships of anti-predator escape and post-escape responses with body mass and morphology: a comparative avian study. Evol Ecol Res 8:731–752Google Scholar
  25. Fisher RA (1930) The genetical theory of natural selection. Clarendon, OxfordGoogle Scholar
  26. Frid A, Dill L (2002) Human-caused disturbance stimuli as a form of predation risk. Conserv Ecol 6:11Google Scholar
  27. Fuiman LA (1993) Development of predator evasion in Atlantic herring, Clupea harengus L. Anim Behav 45:1101–1116CrossRefGoogle Scholar
  28. Glaudas X, Winne CT, Fedewa LA (2006) Ontogeny of anti-predator behavioral habituation in cottonmouths (Agkistrodon piscivorus). Ethology 112:608–615CrossRefGoogle Scholar
  29. Grafen A (2006) A theory of Fisher's reproductive value. J Math Biol 53:15–60PubMedCrossRefGoogle Scholar
  30. Grant JWA, Noakes DLG (1987) Escape behaviour and use of cover by young-of-the-year brook trout, Salvelinus fontinalis. Can J Fish Aquat Sci 44:1390–1396CrossRefGoogle Scholar
  31. Guidetti P, Vierucci E, Bussotti S (2008) Differences in escape response of fish in protected and fished Mediterranean rocky reefs. J Mar Biol Assoc U K 88:625–627CrossRefGoogle Scholar
  32. Halpern BS (2003) The impact of marine reserves: do reserves work and does reserve size matter? Ecol Appl 13:S117–S137CrossRefGoogle Scholar
  33. Hawkins JP, Roberts CM (2004) Effects of fishing on sex-changing Caribbean parrotfishes. Biol Conserv 115:213–226CrossRefGoogle Scholar
  34. Heatwole H (1968) Relationship of escape behavior and camouflage in anoline lizards. Copeia 1968:109–113CrossRefGoogle Scholar
  35. Helfman GS (1989) Threat-sensitive predator avoidance in damselfish-trumpetfish interactions. Behav Ecol Sociobiol 24:47–58CrossRefGoogle Scholar
  36. Helfman GS, Winkelman DL (1997) Threat sensitivity in bicolor damselfish: effects of sociality and body size. Ethology 103:369–383CrossRefGoogle Scholar
  37. Humann P, DeLoach N (2002) Reef fish identification: Florida, Caribbean, Bahamas. New World Publications, Jacksonville (FL)Google Scholar
  38. Hurvich CM, Tsai CL (1990) The impact of model selection on inference in linear regression. Am Stat 44:214–217CrossRefGoogle Scholar
  39. Hutchings MR, Harris S (1995) Does hunting pressure affect the flushing behaviour of brown hares (Lepus europaeus)? J Zool 237:663–667CrossRefGoogle Scholar
  40. Johnson JB, Omland KS (2004) Model selection in ecology and evolution. Trends Ecol Evol 19:101–108PubMedCrossRefGoogle Scholar
  41. Knight RL, Temple SA (1995) Origin of wildlife responses to recreationists. In: Knight RL, Gutzwiller KJ (eds) Wildlife and Recreationists. Island, Washington DC, pp 81–91Google Scholar
  42. Lewis JB (1960) The coral reefs and coral communities of Barbados WI. Can J Zool 38:1133–1145CrossRefGoogle Scholar
  43. Madsen J, Fox AD (1995) Impacts of hunting disturbance on waterbirds—a review. Wildl Biol 1:193–207Google Scholar
  44. Martín J, López P (1995) Escape behaviour of juvenile Psammodromus algirus lizards: constraint of or compensation for limitations of body size? Behaviour 132:181–192CrossRefGoogle Scholar
  45. McGill BJ, Mittelbach GG (2006) An allometric vision and motion model to predict prey encounter rates. Evol Ecol Res 8:691–701Google Scholar
  46. Møller AP, Nielsen JT, Garamzegi LZ (2008) Risk taking by singing males. Behav Ecol 19:41–53CrossRefGoogle Scholar
  47. Montgomery DC, Peck EA (1982) Introduction to linear regression analysis. Wiley, New YorkGoogle Scholar
  48. Mumby PJ, Dahlgren CP, Harborne AR, Kappel CV, Micheli F, Brumbaugh DR, Holmes KE, Mendes JM, Broad K, Sanchirico JN, Buch K, Box S, Stoffle RW, Gill AB (2006) Fishing, trophic cascades, and the process of grazing on coral reefs. Science 311:98–101PubMedCrossRefGoogle Scholar
  49. Mumby PJ, Wabnitz CCC (2002) Spatial patterns of aggression, territory size, and harem size in five sympatric Caribbean parrotfish species. Environ Biol Fishes 63:265–279CrossRefGoogle Scholar
  50. Mumby PJ, Harborne AR, Williams J, Kappel CV, Brumbaugh DR, Micheli F, Holmes KE, Dahlgren CP, Paris CB, Blackwell PG (2007) Trophic cascade facilitates coral recruitment in a marine reserve. Proc Natl Acad Sci U S A 104:8362–8367PubMedCrossRefGoogle Scholar
  51. Neter J, Wasserman W, Kutner MH (1985) Applied linear statistical models: regression, analysis of variance, and experimental designs. Irwin, Homewood (IL)Google Scholar
  52. Overholtzer KL, Motta PJ (1999) Comparative resource use by juvenile parrotfishes in the Florida Keys. Mar Ecol Prog Ser 177:177–187CrossRefGoogle Scholar
  53. Paglianti A, Domenici P (2006) The effect of size on the timing of visually mediated escape behaviour in staghorn sculpin Leptocottus armatus. J Fish Biol 68:1177–1191CrossRefGoogle Scholar
  54. Peters RH (1983) The ecological implications of body size. Cambridge University Press, CambridgeGoogle Scholar
  55. Plasman M, Duchateau M, Macedonia JM (2007) Anti-predation behaviour of Dickerson's collared lizard, Crotaphytus dickersonae. Anim Biol 57:231–246CrossRefGoogle Scholar
  56. Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, New YorkGoogle Scholar
  57. Rakitin A, Kramer DL (1996) Effect of a marine reserve on the distribution of coral reef fishes in Barbados. Mar Ecol Prog Ser 131:97–113CrossRefGoogle Scholar
  58. Reinhardt UG (2002) Asset protection in juvenile salmon: how adding biological realism changes a dynamic foraging model. Behav Ecol 13:94–100CrossRefGoogle Scholar
  59. Robertson DR, Warner RR (1978) Sexual patterns in the labroid fishes of the Western Caribbean, II, the parrotfishes (Scaridae). Smithsonian Institution, WashingtonGoogle Scholar
  60. Rogers L, Sargent RC (2001) A dynamic model of size-dependent reproductive effort in a sequential hermaphrodite: a counterexample to Williams's conjecture. Am Nat 158:543–552PubMedCrossRefGoogle Scholar
  61. Runyan AM, Blumstein DT (2004) Do individual differences influence flight initiation distance? J Wildl Manag 68:1124–1129CrossRefGoogle Scholar
  62. Scrimgeour GJ, Cash KJ, Culp JM (1997) Size-dependent flight initiation by a lotic mayfly in response to a predatory fish. Freshw Biol 37:91–98CrossRefGoogle Scholar
  63. Setsaas TH, Holmern T, Mwakalebe G, Stokke S, Roskaft E (2007) How does human exploitation affect impala populations in protected and partially protected areas?—a case study from the Serengeti ecosystem, Tanzania. Biol Conserv 136:563–570CrossRefGoogle Scholar
  64. Sogard SM (1997) Size-selective mortality in the juvenile stage of teleost fishes: a review. Bull Mar Sci 60:1129–1157Google Scholar
  65. Stankowich T (2008) Ungulate flight responses to human disturbance: a review and meta-analysis. Biol Conserv 141:2159–2173CrossRefGoogle Scholar
  66. Stankowich T, Blumstein DT (2005) Fear in animals: a meta-analysis and review of risk assessment. Proc R Soc Lond B Biol Sci 272:2627–2634CrossRefGoogle Scholar
  67. Stankowich T, Coss RG (2006) Effects of predator behavior and proximity on risk assessment by Columbian black-tailed deer. Behav Ecol 17:246–254CrossRefGoogle Scholar
  68. Stearn CW, Scoffin TP, Martindale W (1977) Calcium-carbonate budget of a fringing reef on west coast of Barbados. 1. Zonation and productivity. Bull Mar Sci 27:479–510Google Scholar
  69. Stephens PA, Buskirk SW, del Rio CM (2007) Inference in ecology and evolution. Trends Ecol Evol 22:192–197PubMedCrossRefGoogle Scholar
  70. Stephens PA, Buskirk SW, Hayward GD, Del Rio CM (2005) Information theory and typothesis testing: a call for pluralism. J Appl Ecol 41:4–12CrossRefGoogle Scholar
  71. Tabachnick BG, Fidell LS (2001) Using multivariate statistics. Allyn and Bacon, BostonGoogle Scholar
  72. Thiel D, Menoni E, Brenot JF, Jenni L (2007) Effects of recreation and hunting on flushing distance of Capercaillie. J Wildl Manag 71:1784–1792CrossRefGoogle Scholar
  73. Tupper M, Juanes F (1999) Effects of a marine reserve on recruitment of grunts (Pisces: Haemulidae) at Barbados, West Indies. Environ Biol Fishes 55:53–63CrossRefGoogle Scholar
  74. Warner RR (1998) The role of extreme iteroparity and risk avoidance in the evolution of mating systems. J Fish Biol 53:82–93CrossRefGoogle Scholar
  75. Webb PW (1981) Responses of northern anchovy, Engraulis moedax, larvae to predation by a biting planktivore, Amphiprion percula. Fish Bull 79:727–735Google Scholar
  76. Whittingham MJ, Stephens PA, Bradbury RB, Freckleton RP (2006) Why do we still use stepwise modeling in ecology and behaviour? J Anim Ecol 75:1182–1189PubMedCrossRefGoogle Scholar
  77. Wintle BA, McCarthy MA, Volinsky CT, Kavanagh RP (2003) The use of Bayesian model averaging to better represent uncertainty in ecological models. Conserv Biol 17:1579–1590CrossRefGoogle Scholar
  78. Wootton RJ (1990) Ecology of teleost fishes. Chapman and Hall, LondonGoogle Scholar
  79. Ydenberg RC, Dill LM (1986) The economics of fleeing from predators. Adv Study Behav 16:229–249CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Kiyoko M. Gotanda
    • 1
  • Katrine Turgeon
    • 1
  • Donald L. Kramer
    • 1
    Email author
  1. 1.Department of BiologyMcGill UniversityMontrealCanada

Personalised recommendations