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Oecologia

, Volume 183, Issue 3, pp 909–917 | Cite as

Individual-level behavioral responses of immature green turtles to snorkeler disturbance

  • Lucas P. Griffin
  • Jacob W. Brownscombe
  • Tyler O. Gagné
  • Alexander D. M. Wilson
  • Steven J. Cooke
  • Andy J. Danylchuk
Conservation ecology – original research

Abstract

Despite many positive benefits of ecotourism, increased human encounters with wildlife may have detrimental effects on wild animals. As charismatic megafauna, nesting and foraging sea turtles are increasingly the focus of ecotourism activities. The purpose of our study was to quantify the behavioral responses of immature green turtles (Chelonia mydas) to disturbance by snorkelers, and to investigate whether turtles have individual-level responses to snorkeler disturbance. Using a standardized disturbance stimulus in the field, we recorded turtle behaviors pre- and post-disturbance by snorkelers. Ninety percent of turtles disturbed by snorkeler (n = 192) initiated their flights at distances of ≤3 m. Using principal component analysis, we identified two distinct turtle personality types, ‘bold’ and ‘timid’, based upon 145 encounters of 19 individually identified turtles and five disturbance response variables. There was significant intra-individual repeatability in behavioral responses to disturbance, but bolder turtles had more behavioral plasticity and less consistent responses than more timid individuals. Bolder individuals with reduced evasion responses might be at a higher risk of shark predation, while more timid turtles might have greater energetic consequences due to non-lethal predator effects and repeated snorkeler disturbance. Over the longer term, a turtle population with a mix of bold and timid individuals may promote more resilient populations. We recommend that snorkelers maintain >3 m distance from immature green turtles when snorkeling, and that ecotourism activities be temporally and spatially stratified. Further, turtle watching guidelines need to be communicated to both tour operators and independent snorkelers to reduce the disturbance of turtles.

Keywords

Ecotourism Flight initiation distance Principal component analysis Personality Repeatability 

Notes

Acknowledgements

We like to thank Dr. Craig Lilyestrom and Carlos Diez (Department of Natural and Environmental Resources, Commonwealth of Puerto Rico), Ricardo Colón-Merced and Ana Roman (Culebra National Wildlife Refuge, US Fish and Wildlife Service), and Todd Plaia (Culebra Divers) for logistical support. We thank Diego Morell Parea (Culebra Adventures) for his support and additional data collection. Further, we would like to thank Chris Haak and Sarah Becker for field assistance. We would also like to thank Dr. Curtice Griffin for writing assistance and Dr. Kevin McGarigal, Blake Massey, and Dr. Chi-Yun Kuo for assistance with statistical analyses. Finally, we would like to thank the Associate Editor, Dr. Aaron Wirsing, and all of the anonymous reviewers for their time and insightful comments on the manuscript.

Author contribution statement

LPG and AJD conceived the study. LPG, JWB, TOG, SJC, ADMW, and AJD designed the methodology. LPG, JWB, and TOG conducted the fieldwork. LPG analyzed the data and wrote the manuscript. All authors provided editorial advice and assisted with revisions.

Compliance with ethical standards

Conflict of interest

The authors declare that no conflict of interest exists. Funding source had no involvement in study design collection, and analysis and interpretation of data; in the writing of the report; and in the decision to submit the article for publication. LG was partially supported by the University of Massachusetts Intercampus Marine Science Graduate Program and the Allen Family Foundation. JB is supported by the Natural Sciences and Engineering Research Council of Canada and the Berkeley Marine Conservation Fellowship from the American Fisheries Society. TG was partially supported by the University of Massachusetts Environmental Conservation Department. AD was partially supported by UPR Sea Grant.

References

  1. Arthur KE, Boyle MC, Limpus CJ (2008) Ontogenetic changes in diet and habitat use in green sea turtle (Chelonia mydas) life history. Mar Ecol Prog Ser 362:303–311CrossRefGoogle Scholar
  2. Ashley C, Roe D (1998) Enhancing community involvement in wildlife tourism: issues and challenges. Wildlife and Development Series: No. 11, International Institute for Environment and Development, LondonGoogle Scholar
  3. Balazs GH, Forsyth RG, Kam AKH (1987) Preliminary assessment of habitat utilization by Hawaiian green turtles in their resident foraging pastures. NOAA Technical Memorandum NMFS-SWFC-71, pp 1–107Google Scholar
  4. Ballantyne R, Packer J, Sutherland LA (2011) Visitors’ memories of wildlife tourism: implications for the design of powerful interpretive experiences. Tour Manag 32:770–779CrossRefGoogle Scholar
  5. Bejder L (2005) Linking short and long-term effects of nature-based tourism on cetaceans. PhD dissertation, Dalhousie University, Halifax, CanadaGoogle Scholar
  6. Bejder L, Samuels A, Whitehead H, Gales N (2006) Interpreting short-term behavioural responses to disturbance within a longitudinal perspective. Anim Behav 72:1149–1158CrossRefGoogle Scholar
  7. Bell AM, Hankison SJ, Laskowski KL (2009) The repeatability of behaviour: a meta-analysis. Anim Behav 77:771–783CrossRefPubMedPubMedCentralGoogle Scholar
  8. Biro PA, Beckmann C, Stamps JA (2010) Small within-day increases in temperature affects boldness and alters personality in coral reef fish. R Soc B 277:71–77CrossRefGoogle Scholar
  9. Bjorndal KA, Bolten AB, Chaloupka MY (2000) Green turtle somatic growth model: evidence for density dependence. Ecol Appl 10:269–282Google Scholar
  10. Bolten A (2003) Variation in sea turtle life history patterns: neritic versus oceanic developmental stages. In: Lutz PL, Musick J, Wyneken J (eds) The Biology of Sea Turtles II. CRC Press, Boca Raton, pp 243–257Google Scholar
  11. Bonte D, Bossuyt B, Lens L (2007) Aerial dispersal plasticity under different wind velocities in a salt marsh wolf spider. Behav Ecol 18:438–443CrossRefGoogle Scholar
  12. Bostwick A, Higgins BM, Landry AM Jr, McCracken ML (2014) Novel use of a shark model to elicit innate behavioral responses in sea turtles: application to by catch reduction in commercial fisheries. Chelonian Conserv Biol 13:237–246CrossRefGoogle Scholar
  13. Bowen BW, Karl SA (2007) Population genetics and phylogeography of sea turtles. Mol Ecol 16:4886–4907CrossRefPubMedGoogle Scholar
  14. Bresette MJ, Witherington BE, Herren RM, Bagley DA, Gorham JC, Traxler SL, Crady CK, Hardy R (2010) Size-class partitioning and herding in a foraging group of green turtles Chelonia mydas. Endanger Species Res 9:105–116CrossRefGoogle Scholar
  15. Briffa M, Rundle SD, Fryer A (2008) Comparing the strength of behavioural plasticity and consistency across situations: animal personalities in the hermit crab Pagurus bernhardus. Proc Biol Sci 275:1305–1311CrossRefPubMedPubMedCentralGoogle Scholar
  16. Brooks JS, Franzen MA, Holmes CM, Grote MN, Mulder MB (2006) Testing hypotheses for the success of different conservation strategies. Conserv Biol 20:1528–1538CrossRefPubMedGoogle Scholar
  17. Campbell LM (1999) Ecotourism in rural developing communities. Ann Tourism Res 26:534–553CrossRefGoogle Scholar
  18. Carere C, Drent PJ, Privitera L, Koolhaas JM, Groothuis TG (2005) Personalities in great tits, Parus major: stability and consistency. Anim Behav 70:795–805CrossRefGoogle Scholar
  19. Cisneros-Montemayor AM, Barnes-Mauthe M, Al-Abdulrazzak D, Navarro-Holm E, Sumaila UR (2013) Global economic value of shark ecotourism: implications for conservation. Oryx 47:381–388CrossRefGoogle Scholar
  20. Conrad JL, Weinersmith KL, Brodin T, Saltz J, Sih A (2011) Behavioural syndromes in fishes: a review with implications for ecology and fisheries management. J Fish Biol 78:395–435CrossRefPubMedGoogle Scholar
  21. Constantine R, Bejder L (2008) Managing the whale-and dolphin-watching industry: time for a paradigm shift. In: Higham J, Lück M (eds) Marine wildlife and tourism management: insights from the natural and social sciences. CABI, Oxford, pp 321–333Google Scholar
  22. Cote J, Fogarty S, Weinersmith K, Brodin T, Sih A (2010) Personality traits and dispersal tendency in the invasive mosquitofish (Gambusia affinis). Proc R Soc B 277:1571–1579CrossRefPubMedPubMedCentralGoogle Scholar
  23. Creel S (2011) Toward a predictive theory of risk effects: hypotheses for prey attributes and compensatory mortality. Ecology 9:2190–2195CrossRefGoogle Scholar
  24. Creel S, Christianson D (2008) Relationships between direct predation and risk effects. Trends Ecol Evol 23:194–201CrossRefPubMedGoogle Scholar
  25. David JT, Cervantes MC, Trosky KA, Salinas JA, Delville Y (2004) A neural network underlying individual differences in emotion and aggression in male golden hamsters. Neuroscience 126:567–578CrossRefPubMedGoogle Scholar
  26. Development Core Team, R (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  27. Dingemanse NJ, Wright J, Kazem AJ, Thomas DK, Hickling R, Dawnay N (2007) Behavioural syndromes differ predictably between 12 populations of three-spined stickleback. J Anim Ecol 76:1128–1138CrossRefPubMedGoogle Scholar
  28. Dingemanse NJ, Bouwman KM, van de Pol M, van Overveld T, Patrick SC, Matthysen E, Quinn JL (2012) Variation in personality and behavioural plasticity across four populations of the great tit Parus major. J Anim Ecol 81:116–126CrossRefPubMedGoogle Scholar
  29. Fennell DA (2015) Ecotourism, 4th edn. Routledge, New YorkGoogle Scholar
  30. Gabrielsen GW, Smith EN (1995) Physiological responses of wildlife to disturbance. In: Knight RL, Gutzwiller KJ (eds) Wildlife and Recreationists. Island Press, Washington, DC, pp 95–107Google Scholar
  31. Gallagher AJ, Hammerschlag N (2011) Global shark currency: the distribution, frequency, and economic value of shark ecotourism. Curr Issues Tour 14:797–812CrossRefGoogle Scholar
  32. Geffroy B, Samia DS, Bessa E, Blumstein DT (2015) How nature-based tourism might increase prey vulnerability to predators. TREE 30:755–765PubMedGoogle Scholar
  33. Gosling SD (2001) From mice to men: what can we learn about personality from animal research? Psychol Bull 127:45–86CrossRefPubMedGoogle Scholar
  34. Green R, Higginbottom K (2001) The negative effects of wildlife tourism on wildlife. Wildlife Tourism Research Report Series: No. 5, Status Assessment of Wildlife Tourism in Australia Series, CRC for Sustainable Tourism, Gold CoastGoogle Scholar
  35. Hayes CT, Baumbach DS, Juma D, Dunbar SG (2016) Impacts of recreational diving on hawksbill sea turtle (Eretmochelys imbricata) behavior in a marine protected area. J Sustain Tour 25:1–17Google Scholar
  36. Heithaus MR (2013) Predators, prey, and the ecological roles of sea turtles. In: Wyneken J, Lohmann KJ, Musick JA (eds) The biology of sea turtles III. CRC Press, Boca Raton, pp 249–284CrossRefGoogle Scholar
  37. Heithaus MR, Frid A, Wirsing AJ, Dill LM, Fourqurean JW, Burkholder D, Thomson J, Bejder L (2007) State-dependent risk-taking by green sea turtles mediates top-down effects of tiger shark intimidation in a marine ecosystem. J Anim Ecol 76:837–844CrossRefPubMedGoogle Scholar
  38. Heithaus MR, Wirsing AJ, Thomson JA, Burkholder DA (2008) A review of lethal and non-lethal effects of predators on adult marine turtles. J Exp Mar Biol Ecol 356:43–51CrossRefGoogle Scholar
  39. Heppell S, Snover M, Crowder L (2003) Sea turtle population ecology. In: Lutz PL, Musick J, Wyneken J (eds) The biology of sea turtles II. CRC Press, Boca Raton, pp 275–306Google Scholar
  40. Higginbottom K, Northrope C, Green R (2001) Positive effects of wildlife tourism on wildlife. Wildlife Tourism Research Report Series: No. 5, Status Assessment of Wildlife Tourism in Australia series, CRC for Sustainable Tourism, Gold CoastGoogle Scholar
  41. Highcock L, Carter AJ (2014) Intraindividual variability of boldness is repeatable across contexts in a wild lizard. PLoS One 9:e95179CrossRefPubMedPubMedCentralGoogle Scholar
  42. Jacobson SK, Lopez AF (1994) Biological impacts of ecotourism: tourists and nesting turtles in Tortuguero National Park, Costa Rica. Wildl Soc Bull 22:414–419Google Scholar
  43. Jones TT, Seminoff JA (2013) Feeding biology: advances from field-based observations, physiological studies and molecular techniques. In: Wyneken J, Lohmann KJ, Musick JA (eds) The biology of sea turtles, vol III. CRC Press, Boca Raton, pp 211–247CrossRefGoogle Scholar
  44. Knight RL, Cole DN (1995) Wildlife responses to recreationists. In: Knight RL, Gutzwiller KJ (eds) Wildlife and recreationists. Island Press, Washington, DC, pp 51–69Google Scholar
  45. Kostas P (2015) In-water behavior of the loggerhead sea turtle (Caretta caretta) under the presence of humans (Homosapiens) in a major Mediterranean nesting site. In: Kaska Y, Sonmez B, Türkecan O, Sezgin Ҫ (eds) Book of abstracts of the 35th annual symposium on sea turtle biology and conservation. MARCAT Press, Denizli, p 250Google Scholar
  46. Kuo CY, Irschick DJ, Lailvaux SP (2015) Trait compensation between boldness and the propensity for tail autotomy under different food availabilities in similarly aged brown anole lizards. Funct Ecol 29:385–392CrossRefGoogle Scholar
  47. Landry MS, Taggart CT (2010) “Turtle watching” conservation guidelines: green turtle (Chelonia mydas) tourism in nearshore coastal environments. Biodivers Conserv 19:305–312CrossRefGoogle Scholar
  48. Lessells C, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121CrossRefGoogle Scholar
  49. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640CrossRefGoogle Scholar
  50. López P, Hawlena D, Polo V, Amo L, Martín J (2005) Sources of individual shy–bold variations in antipredator behaviour of male Iberian rock lizards. Anim Behav 69:1–9CrossRefGoogle Scholar
  51. Lusseau D, Bejder L (2007) The long-term consequences of short-term responses to disturbance experiences from whalewatching impact assessment. Int J Comp Psychol 20:228–236Google Scholar
  52. Martin JG, Réale D (2008) Temperament, risk assessment and habituation to novelty in eastern chipmunks, Tamias striatus. Anim Behav 75:309–318CrossRefGoogle Scholar
  53. Meadows D (2004) Behavior of green sea turtles in the presence and absence of recreational snorkelers. Mar Turtle Newsl 103:1–4Google Scholar
  54. Müllner A, Linsenmair KE, Wikelski M (2004) Exposure to ecotourism reduces survival and affects stress response in hoatzin chicks (Opisthocomus hoazin). Biol Cons 118:549–558CrossRefGoogle Scholar
  55. Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956PubMedGoogle Scholar
  56. Piñeiro A, Barja I, Silván G, Illera JC (2012) Effects of tourist pressure and reproduction on physiological stress response in wildcats: management implications for species conservation. Wildl Res 39:532–539CrossRefGoogle Scholar
  57. Preisser EL, Bolnick DI, Benard MF (2005) Scared to death? The effects of intimidation and consumption in predator–prey interactions. Ecology 86:501–509CrossRefGoogle Scholar
  58. Pulliam HR, Caraco T (1984) Living in groups: is there an optimal group size? In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary approach. Blackwell Science, Oxford, pp 122–147Google Scholar
  59. Quinn JL, Cresswell W (2005) Personality, anti-predation behaviour and behavioural plasticity in the chaffinch Fringilla coelebs. Behaviour 142:1377–1402CrossRefGoogle Scholar
  60. Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318CrossRefPubMedGoogle Scholar
  61. Réale D, Dingemanse NJ, Kazem AJ, Wright J (2010) Evolutionary and ecological approaches to the study of personality. Phil Trans R Soc B 365:3937–3946CrossRefPubMedPubMedCentralGoogle Scholar
  62. Scheyvens R (1999) Ecotourism and the empowerment of local communities. Tour Manag 20:245–249CrossRefGoogle Scholar
  63. Schindler DE, Hilborn R, Chasco B, Boatright CP, Quinn TP, Rogers LA, Webster MS (2010) Population diversity and the portfolio effect in an exploited species. Nature 465:609–612CrossRefPubMedGoogle Scholar
  64. Schofield G, Katselidis KA, Dimopoulos P, Pantis JD (2008) Investigating the viability of photo-identification as an objective tool to study endangered sea turtle populations. J Exp Mar Biol Ecol 360:103–108CrossRefGoogle Scholar
  65. Schuett W, Dall SR, Baeumer J, Kloesener MH, Nakagawa S, Beinlich F, Eggers T (2011) Personality variation in a clonal insect: the pea aphid, Acyrthosiphon pisum. Dev Psychobiol 53:631–640CrossRefPubMedGoogle Scholar
  66. Seminoff JA, Allen CD, Balazs GH, Dutton PH, Eguchi T, Haas HL, Hargrove SA, Jensen MP, Klemm DL, Lauritsen AM, MacPherson SL, Opay P, Possardt EE, Pultz SL, Seney EE, Van Houtan KS, Waples RS (2015) Status review of the green turtle (Chelonia mydas) under the Endangered Species Act. NOAA Technical Memorandum NOAA-TM-NMFS-SWFSC-539, pp 1–571Google Scholar
  67. Sih A, Bell AM, Johnson JC, Ziemba RE (2004) Behavioral syndromes: an integrative overview. Q Rev Biol 79:241–277CrossRefPubMedGoogle Scholar
  68. Slater K (2014) CEA/Operating Wallacea immature green sea turtle monitoring report 2014. http://opwall.com/wp-content/uploads/2014-Turtle-Monitoring-Report.pdf. Accessed 10 Aug 2016
  69. Sokal R, Rohlf F (1981) Biometry: the principles and practice of statistics in biological research, 3rd edn. Sage Publications, LondonGoogle Scholar
  70. Svartberg K, Tapper I, Temrin H, Radesäter T, Thorman S (2005) Consistency of personality traits in dogs. Anim Behav 69:283–291CrossRefGoogle Scholar
  71. Taquet C, Taquet M, Dempster T, Soria M, Ciccione S, Roos D, Dagorn L (2006) Foraging of the green sea turtle Chelonia mydas on seagrass beds at Mayotte Island (Indian Ocean), determined by acoustic transmitters. Mar Ecol Prog Ser 306:295–302CrossRefGoogle Scholar
  72. The International Ecotourism Society (2006) TIES global ecotourism fact sheet. https://ibgeography-lancaster.wikispaces.com/file/view/TIES+GLOBAL+ECOTOURISM+FACT+SHEET.PDF. Accessed 04 Apr 2016
  73. Tisdell C, Wilson C (2002) Ecotourism for the survival of sea turtles and other wildlife. Biodivers Conserv 11:1521–1538CrossRefGoogle Scholar
  74. Wang JH, Fisler S, Swimmer Y (2010) Developing visual deterrents to reduce sea turtle bycatch in gill net fisheries. Mar Ecol Prog Ser 408:241–250CrossRefGoogle Scholar
  75. Werner EE, Peacor SD (2003) A review of trait-mediated indirect interactions in ecological communities. Ecology 84:1083–1100CrossRefGoogle Scholar
  76. Williams R, Lusseau D, Hammond PS (2006) Estimating relative energetic costs of human disturbance to killer whales (Orcinus orca). Biol Conserv 133:301–311CrossRefGoogle Scholar
  77. Wilson DS, Clark AB, Coleman K, Dearstyne T (1994) Shyness and boldness in humans and other animals. Trends Ecol Evol 9:442–446CrossRefGoogle Scholar
  78. Wilson ADM, Godin JGJ, Ward AJW (2010) Boldness and reproductive fitness correlates in the eastern mosquitofish (Gambusia holbrooki). Ethology 116:96–104CrossRefGoogle Scholar
  79. Wolf M, Weissing FJ (2012) Animal personalities: consequences for ecology and evolution. Trends Ecol Evol 27:452–461CrossRefPubMedGoogle Scholar
  80. Ydenberg RC, Dill LM (1986) The economics of fleeing from predators. Adv Stud Behav 16:229–249CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Lucas P. Griffin
    • 1
  • Jacob W. Brownscombe
    • 2
  • Tyler O. Gagné
    • 3
  • Alexander D. M. Wilson
    • 2
    • 4
  • Steven J. Cooke
    • 2
  • Andy J. Danylchuk
    • 1
  1. 1.Department of Environmental Conservation and Intercampus Marine Science Graduate ProgramUniversity of Massachusetts AmherstAmherstUSA
  2. 2.Fish Ecology and Conservation Physiology Laboratory, Ottawa-Carleton Institute for BiologyCarleton UniversityOttawaCanada
  3. 3.Department of Environmental ConservationUniversity of Massachusetts AmherstAmherstUSA
  4. 4.School of Life and Environmental SciencesUniversity of SydneySydneyAustralia

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