Where Dolphins Sleep: Resting Areas in the Red Sea

  • Maddalena FumagalliEmail author
  • Amina Cesario
  • Marina Costa
Part of the Springer Oceanography book series (SPRINGEROCEAN)


Periods of physiological quiescence are ubiquitous in animals. Resting is a vital, vulnerable and delicate phase of reduced vigilance to external stimuli that, in all animals, includes sleep components. In dolphins, resting is characterised by low activity and mobility, and sleep is exclusively unihemispheric slow wave sleep (USWS), an arrangement compatible with the voluntary respiratory function. Physiological needs and ecological conditions affect the way individuals arrange their behaviour during the photoperiod in order to accommodate the desirable but incompatible resting, foraging, mating, travelling needs and opportunities, to optimise benefits and minimise fitness costs. The duration and quality of rest strictly depend on the surrounding environmental conditions and the phase is susceptible to interruptions and disruptions. If animals are chronically deprived of rest and sleep, the cumulative effects of the deprivation can impact individual physiology and cognitive abilities, to the extent that the viability of individuals and their populations may be compromised. Dolphin-based tourism operations affect resting and sleeping patterns in a number of species and can lead to short-term behavioural responses, as well as long-term detrimental consequences, on wild dolphin populations. Among the Red Sea species, the spinner and Indo-Pacific bottlenose dolphins display diurnal resting patterns inside, or in proximity to, coastal reefs. This generates a situation of high conservation concern as these species become not only more accessible for the tourism industry, but also more heavily exposed to it during a critical phase. In these circumstances, a precautionary approach is required. The spinner dolphin resting behaviour is well described and provides an interesting and comprehensive case study on the management of human interactions on resting dolphins. The island-associated ecotype of the spinner dolphin (Stenella longirostris) feeds exclusively at night and retreats to bays and lagoons to rest during the daytime. Resting areas have been reported in Hawaii, Brazil, Fiji, and in the Red Sea off Egypt, Sudan and Saudi Arabia. The spatial-temporal constraints on resting and the scarce behavioural plasticity make the spinner dolphin particularly vulnerable to rest disruptions. Indeed, the long-established tourism industry was held responsible for population decline and changes in habitat use in the Hawaiian dolphin population. In the Red Sea, the scientific investigation of impacts is still preliminary, but the establishment and success of the Samadai Reef specially managed area in Egypt shows that science-informed, precautionary and pragmatic management of dolphin-based activities is possible even in data poor contexts. Rest being a vital life function and given the dependence of dolphins on specific selected sites, resting areas surge to a status of highly critical habitats. Adequate investigation of impacts and management of anthropogenic activities inside resting areas and in their proximity are therefore priorities and key actions for the conservation of wild dolphin populations.



The authors would like to thank the Hurghada Environmental Protection and Conservation Association (HEPCA), the Universities of Otago, Hong Kong, and St. Andrews, the Earthwatch Institute, the Italian Cooperation in Egypt, the Rufford Small Grant Foundation, and Boomerang for Earth Conservation for their financial, logistic and scientific support during the fieldwork in Egypt. We acknowledge the important contribution of Dr. Giuseppe Notarbartolo di Sciara, Amr Ali, and Dr. Mahmoud Hanafy in advancing our understanding of the scientific, economic and social implications of the Egyptian case study, and the broader Red Sea scenario. We are thankful to Angela Ziltener for sharing her research experience with the authors, and to field assistants and volunteers who helped with to the data collection or contributed their observations. Editors and reviewers’ comments on earlier drafts greatly enhanced the quality of this work. This chapter is dedicated to Amr Ali (1971–2016), whose brilliant visions and passionate approaches revolutionised the field of marine resources conservation in Egypt.


  1. Aldabal L, Bahammam AS (2011) Metabolic, endocrine, and immune consequences of sleep deprivation. Open Respir Med J 5:31–43. Scholar
  2. Altman J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267CrossRefGoogle Scholar
  3. Anderson RC (2005) Observations of cetaceans in the Maldives, 1990-2002. J Cetacean Res Manag 7:119Google Scholar
  4. Au WWL (1993) The sonar of dolphins. Springer, New YorkCrossRefGoogle Scholar
  5. Au WWL (2009) Echolocation. In: Perrin WF, Würsig B (eds) Encyclopedia of marine mammals, 2nd edn. Academic Press, San Diego, pp 328–357Google Scholar
  6. Ayres KL, Booth RK, Hempelmann JA, Koski KL, Emmons CK, Baird RW, Balcomb-Bartok K, Hanson MB, Ford MJ, Wasser SK (2012) Distinguishing the impacts of inadequate prey and vessel traffic on an endangered killer whale (Orcinus orca) population. PLoS ONE 7:e36842CrossRefGoogle Scholar
  7. Ball NJ (1992) The phasing of sleep in animals. In: Stampi C (ed) Why we nap. Birkhaüser, Boston, pp 31–49CrossRefGoogle Scholar
  8. Banks S, Dorrian J, Basner M, Dinges DF (2016) Sleep deprivation. In: Kryger M, Roth T (eds) Principles and practice of sleep medicine, 6th edn. Elsevier, Philadelphia, pp 49–55Google Scholar
  9. Bazúa-Durán C, Valiente NVL (2008) Effect of vessels and swimmers on the behavior of spinner dolphins (Stenella longirostris) off the Big Island of Hawai’i. Contributed paper 1pAB2. J Acoust Soc Am 123:2984CrossRefGoogle Scholar
  10. Beadon JJ (1991) A note on cetaceans seen and live-captured in the Gulf of Aqaba and the Gulf of Suez, 15 September 1980 through 1 September 1981. UNEP Marine Mammal Technical Report 3Google Scholar
  11. Bearzi G, Reeves RR, Remonato E, Pierantonio N, Airoldi S (2011) Risso’s dolphin Grampus griseus in the Mediterranean Sea. Mamm Biol für Säugetierkd 76:385–400CrossRefGoogle Scholar
  12. Bejder L, Samuels AM (2003) Evaluating the effects of nature-based tourism on cetacean. In: Gales N, Hindell M, Kirkwood R (eds) Marine mammals: fisheries. CSIRO Publishing, Tourism and Management Issues, pp 229–256Google Scholar
  13. Bejder L, Samuels AM, Whitehead HA, Gales N, Mann J, Connor R, Heithaus M, Watson-Capps JA, Flaherty C, Kruetzen M (2006) Decline in relative abundance of Bottlenose dolphins exposed to long-term disturbance. Conserv Biol 20:1791–1798CrossRefGoogle Scholar
  14. Bejder L, Samuels A, Whitehead H, Finn H, Allen S (2009) Impact assessment research: use and misuse of habituation, sensitisation and tolerance in describing wildlife responses to anthropogenic stimuli. Mar Ecol Prog Ser 395:177–185CrossRefGoogle Scholar
  15. Benoit-Bird KJ, Au WWL (2003) Prey dynamics affect foraging by a pelagic predator (Stenella longirostris) over a range of spatial and temporal scales. Behav Ecol Sociobiol 53:364–373Google Scholar
  16. Benoit-Bird KJ, Au WWL (2004) Diel migration dynamics of an island-associated sound-scattering layer. Deep Res Part I Oceanogr Res Pap 51:707–719CrossRefGoogle Scholar
  17. Benoit-Bird KJ, Au WWL (2009) Cooperative prey herding by the pelagic dolphin, Stenella longirostris. J Acoust Soc Am 125:125–137CrossRefGoogle Scholar
  18. Benoit-Bird KJ, Au WWL, Brainard RE, Lammers MO (2001) Diel horizontal migration of the Hawaiian mesopelagic boundary community observed acoustically. Mar Ecol Prog Ser 217:1–14CrossRefGoogle Scholar
  19. Berggren P, Amir OA (2007) Sustainable dolphin tourism in East Africa. MASMA Technical Report, WIOMSA, ZanzibarGoogle Scholar
  20. Borbély AA (1982) A two process model of sleep regulation. Hum Neurobiol 1:195–204Google Scholar
  21. Borbély AA, Tobler I (1985) Homeostatic and circadian principles in sleep regulation in the rat. In: McGinty D (ed) Brain mechanisms of sleep. Raven Press, New York, pp 35–44Google Scholar
  22. Brakes P, Dall SRX (2016) Marine mammal behavior: a review of conservation implications. Front Mar Sci 3:87CrossRefGoogle Scholar
  23. Cagnazzi D, Harrison PL, Ross GJB, Lynch P (2011) Abundance and site fidelity of Indo-Pacific Humpback dolphins in the Great Sandy Strait, Queensland, Australia. Mar Mammal Sci 27:255–281CrossRefGoogle Scholar
  24. Campbell SS, Tobler I (1984) Animal sleep: a review of sleep duration across phylogeny. Neurosci Biobehav Rev 8:269–300CrossRefGoogle Scholar
  25. Cantor M, Wedekin LL, Daura-Jorge FG, Rossi-Santos MR, Simões-Lopes PC (2012) Assessing population parameters and trends of Guiana dolphins (Sotalia guianensis): an eight-year mark-recapture study. Mar Mammal Sci 28(1):63–83CrossRefGoogle Scholar
  26. Carlson, C. (2012). A review of whale watch guidelines and regulations around the world: version 2012. International Whaling Commission WWREGS 2013Google Scholar
  27. Carskadon MA, Dement WC (2011) Monitoring and staging human sleep. In: Kryger MH, Roth T, Dement WC (eds) Principles and practice of sleep medicine. Elsevier Saunders, pp 16–26Google Scholar
  28. Cesario A (2017) Population ecology of spinner dolphin (Stenella longirostris) in an offshore resting habitat in the Red Sea. PhD thesis, University of Hong KongGoogle Scholar
  29. Cesario A (2008) Uso dell’habitat e abitudini alimentari di Stenella longirostris (Gray, 1828) nel Mar Rosso egiziano. MSc thesis, Università degli Studi di MilanoGoogle Scholar
  30. Cesario A, Costa M, Fumagalli M, Notarbartolo di Sciara G, Karczmarski L (2015) Female reproductive success and post-natal growth in spinner dolphins through underwater photo-identification and photogrammetry. In: 22nd biennial conference on the biology of marine mammals. The Society for Marine Mammalogy, San FranciscoGoogle Scholar
  31. Cesario A, Costa M, Fumagalli M, Chang WL, Notarbartolo di Sciara G, Karczmarski L (2013) Evidence of male alliances in spinner dolphins off Samadai reef, Red Sea, Egypt. In: 20th biennial conference of the society for marine mammology, DunedinGoogle Scholar
  32. Christiansen F, Lusseau D, Stensland E, Berggren P (2010) Effects of tourist boats on the behaviour of Indo-Pacific bottlenose dolphins off the south coast of Zanzibar. Endanger Species Res 11:91–99CrossRefGoogle Scholar
  33. Cirelli C (2006) Cellular consequences of sleep deprivation in the brain. Sleep Med Rev 10:307–321CrossRefGoogle Scholar
  34. Cirelli C, Tononi G (2008) Is sleep essential? PLoS Biol 6:1605–1611CrossRefGoogle Scholar
  35. Cisneros-Montemayor AM, Sumaila UR, Kaschner K, Pauly D (2010) The global potential for whale watching. Mar Policy 34:1273–1278CrossRefGoogle Scholar
  36. Condet M, Dulau-Drouot V (2016) Habitat selection of two island-associated dolphin species from the south-west Indian Ocean. Cont Shelf Res 125:18–27CrossRefGoogle Scholar
  37. Constantine R, Brunton DH, Dennis T (2004) Dolphin-watching tour boats change bottlenose dolphin (Tursiops truncatus) behaviour. Biol Conserv 117:299–307CrossRefGoogle Scholar
  38. Corkeron PJ (2004) Whale watching, iconography, and marine conservation. Conserv Biol 18:847–849CrossRefGoogle Scholar
  39. Costa M (2015) Abundance and distribution of Delphinids in the Red Sea (Egypt). PhD thesis, University of St AndrewsGoogle Scholar
  40. Costa M, Cesario A, Notarbartolo G, Fumagalli M (2012) Site fidelity and relative abundance of spinner dolphins resting in Samadai reef (Egypt—Red Sea). In: Proceedings of the 26th European cetacean society conference, GalwayGoogle Scholar
  41. Costa M, Fumagalli M, Cesario A (this volume) Review of cetaceans in the Red SeaGoogle Scholar
  42. Courbis S (2004) Behavior of Hawaiian spinner dolphins (Stenella longirostris) in response to vessels/swimmers. MSc thesis, San Francisco State UniversityGoogle Scholar
  43. Courbis SS, Timmel G (2009) Effects of vessels and swimmers on behavior of Hawaiian spinner dolphins (Stenella longirostris) in Kealake’akua, Honaunau, and Kauhako bays, Hawai’i. Mar Mammal Sci 25:430–440CrossRefGoogle Scholar
  44. Cribb N, Miller C, Seuront L (2012) Site fidelity and behaviour of spinner dolphins (Stenella longirostris) in Moon Reef, Fiji Islands: Implications for conservation. J Mar Biol Assoc UK 92:1793–1798CrossRefGoogle Scholar
  45. Danil K, Maldini D, Marten K (2005) Patterns of use of Maku’a Beach, O’ahu, Hawai’i, by Spinner dolphins (Stenella longirostris) and potential effects of swimmers on their behavior. Aquat Mamm 31:403–412CrossRefGoogle Scholar
  46. Davis RW, Fargion GS, May N, Leming TD, Baumgartner M, Evans WE, Hansen LJ, Mullin K (1998) Physical habitat of cetaceans along the continental slope in the north-central and western Gulf of Mexico. Mar Mammal Sci 14:490–507CrossRefGoogle Scholar
  47. De Montpellier G (2007) Eco-ethological approaches of the spinner dolphin (Stenella longirostris, Gray, 1828) in southern Red Sea (Egypt) with a view of improving management of the Marine Protected Area Sha’ab Samadai reef. MSc thesis, Université Catholique de LouvainGoogle Scholar
  48. Delfour F (2007) Hawaiian spinner dolphins and the growing dolphin watching activity in Oahu. J Mar Biol Assoc UK 87:109–112CrossRefGoogle Scholar
  49. Dement W, Kleitman N (1957) Cyclic variations in EEG during sleep and their relation to eye movements, body motility, and dreaming. Electroencephalogr Clin Neurophysiol 9:673–690CrossRefGoogle Scholar
  50. Dijk DJ, Shanahan TL, Duffy JF, Ronda JM, Czeisler CA (1997) Variation of electroencephalographic activity during non-rapid eye movement and rapid eye movement sleep with phase of circadian melatonin rhythm in humans. J Physiol 505:851–858CrossRefGoogle Scholar
  51. Dolar MLL, Walker A, Kooyman L, Perrin F (2003) Comparative feeding ecology of spinner dolphins (Stenella longirostris) and Fraser’s dolphins (Lagenodelphis hosei) in the Sulu Sea. Mar Mammal Sci 19:1–19CrossRefGoogle Scholar
  52. Drummond SP, Bischoff-Grethe A, Dinges DF, Ayalon L, Mednick SC, Meloy MJ (2005) The neural basis of the psychomotor vigilance task. Sleep 28:1059–1068Google Scholar
  53. Dudzinski KM, Thomas JA, Gregg JD (2009) Communication in marine mammals. In: Perrin WF, Würsig B (eds) Encyclopedia of marine mammals, 2nd edn. Academic Press, San Diego, pp 260–269CrossRefGoogle Scholar
  54. Dukas R, Clark CW (1995) Sustained vigilance and animal performance. Anim Behav 49:1259–1267CrossRefGoogle Scholar
  55. Dulau-Drouot V, Boucaud V, Rota B (2008) Cetacean diversity off La Réunion Island (France). J Mar Biol Assoc UK 88:1263–1272CrossRefGoogle Scholar
  56. Elgar MA, Pagel MD, Harvey PH (1988) Sleep in mammals. Anim Behav 36:1407–1419CrossRefGoogle Scholar
  57. Eyre FJ, Frizell J (2012) A note on observations of cetaceans in the Indian Ocean Sanctuary, Australia to Israel, April 1995. J Cetacean Res Manag 12:277–285Google Scholar
  58. Forest AM (1999) The Hawaiian spinner dolphin (Stenella longirostris): effects of tourism. In: Proceedings of 13th Biennial conference on the biology of marine mammals—wild dolphin swim program workshop. The Society for Marine Mammalogy, MauiGoogle Scholar
  59. Forrest TG, Miller GL, Zagar JR (1993) Sound propagation in shallow water: implications for acoustic communication by aquatic animals. Bioacoustics 4:259–270CrossRefGoogle Scholar
  60. Frid A, Dill L (2002) Human-caused disturbance stimuli as a form of predation risk. Conserv Ecol 6:11CrossRefGoogle Scholar
  61. Fumagalli M (2016) Conservation of the spinner dolphin in the Egyptian Red Sea. PhD thesis, University of OtagoGoogle Scholar
  62. Fumagalli M (2008) Socio-ecologia di Stenella longirostris nel Mar Rosso egiziano. MSc thesis, Unversità degli Studi di MilanoGoogle Scholar
  63. Fumagalli M, Cesario A, Costa M, Notarbartolo di Sciara G, Slooten E, Higham J (2015) When inclusion in a national park limits conservation: spinner dolphin tourism in Egypt analysed in a social-ecological system framework. In: Proceedings of the 22nd Biennial conference on the biology of marine mammals. The Society for Marine Mammalogy, San FranciscoGoogle Scholar
  64. Fumagalli M, Cesario A, Costa M, Notarbartolo di Sciara G, Slooten E (2013) Dolphins, research and tourism in Samadai Reef: is there enough room for everybody? In: Proceedings of the 20th biennial conference of the society for marine mammalogy, DunedinGoogle Scholar
  65. Gailey G, Karczmarski L (2012) Discovery: photo-identification data-management system for individually recognizable animalsGoogle Scholar
  66. Gannier A, Petiau E (2006) Environmental variables affecting the residence of spinner dolphins (Stenella longirostris) in a Bay of Tahiti (French Polynesia). Aquat Mamm 32:202–211CrossRefGoogle Scholar
  67. Gladstone W, Fisher PR (2000) Status and ecology of cetaceans in the Farasan Islands Marine Protected Area. Fauna Arab 18:385–396Google Scholar
  68. Goley PD (1999) Behavioral aspects of sleep in Pacific white-sided dolphins (Lagenorhynchus obliquidens, Gill 1865). Mar Mammal Sci 15:1054–1064CrossRefGoogle Scholar
  69. Gormley AM, Slooten E, Dawson S, Barker RJ, Rayment W, du Fresne S, Bräger S (2012) First evidence that marine protected areas can work for marine mammals. J Appl Ecol 49:474–480CrossRefGoogle Scholar
  70. Gowans S, Würsig B, Karczmarski L (2008) The social structure and strategies of delphinids: predictions based on an ecological framework. Adv Mar Biol 53:195–294CrossRefGoogle Scholar
  71. Green M, Calvez L (1999) Research on Hawaiian spinner dolphins in Kealakekua Bay, Hawaii. In: Dudzinski KM, Frohoff TG, Spradlin TR (eds) Proceedings of the wild dolphin swim program workshop. Maui, HawaiiGoogle Scholar
  72. Hammond PS, Bearzi G, Bjørge A, et al. (2012) Tursiops aduncus. The IUCN Red List of Threatened Species 2012. (Downloaded on 18 October 2016)
  73. Hammond PS, Mizroch SA, Donovan GP (1990) Individual recognition of cetaceans: use of photo-identification and other techniques to estimate population parameters. International Whaling Commission, Cambridge, UKGoogle Scholar
  74. Hanlon RT, Messinger JB (1996) Cephalopod behaviour. Cambridge University Press, CambridgeGoogle Scholar
  75. Hanson MT, Defran RH (1993) The behaviour and feeding ecology of the Pacific coast bottlenose dolphin, Tursiops truncatus. Aquat Mamm 19:127–142Google Scholar
  76. Harrison Y, Horne JA (2000) The impact of sleep deprivation on decision making: a review. J Exp Psychol 6:236–249Google Scholar
  77. Hartse KM (1989) Sleep in insects and nonmammalian vertebrates. In: Kryger MK, Roth T, Dement WC (eds) Principles and practice of sleep medicine. Saunders, W.B, pp 95–104Google Scholar
  78. Heithaus MR, Dill LM (2002) Food availability and tiger shark predation risk influence bottlenose dolphin habitat use. Ecology 83:480–491CrossRefGoogle Scholar
  79. Higham JES, Bejder L, Lusseau D (2009) An integrated and adaptive management model to address the long-term sustainability of tourist interactions with cetaceans. Environ Conserv 35:294–302CrossRefGoogle Scholar
  80. Higham JES, Bedjer L, Allen SJ, Corkeron P, Lusseau D (2016) Managing whale-watching as a non-lethal consumptive activity. J Sust Tour 24:73–90Google Scholar
  81. Hoyt E (2001) Whale watching 2001: worldwide tourism numbers, expenditures, and expanding socioeconomic benefits. International Fund for Animal Welfare, Yarmouth PortGoogle Scholar
  82. Hoyt E, Iñíguez M (2008) The state of whale watching in Latin America. WDCS, ChippenhamGoogle Scholar
  83. Jackson JA, Carroll EL, Smith TD, Zerbini AN, Patenaude NJ, Baker CS (2016) An integrated approach to historical population assessment of the great whales: case of the New Zealand southern right whale. R Soc Open Sci 3:150669CrossRefGoogle Scholar
  84. Jefferson TA, Rosenbaum HC (2014) Taxonomic revision of the humpback dolphins (Sousa spp.), and description of a new species from Australia. Mar Mammal Sci 30:1494–1541CrossRefGoogle Scholar
  85. Johnston DW (2014) Vigilance, resilience and failures of science and management: spinner dolphins and tourism in Hawai’i. In: Higham JES, Bejder L, Williams R (eds) Whale-watching. Cambridge University Press, Cambridge, Sustainable tourism and ecological management, pp 275–292CrossRefGoogle Scholar
  86. Karczmarski L, Cockcroft VG (1999) Daylight behaviour of humpback dolphins Sousa chinensis in Algoa Bay, South Africa. Z Saugetierkd 64:19–29Google Scholar
  87. Karczmarski L, Würsig B, Gailey G, Larson KW, Vanderlip C (2005) Spinner dolphins in a remote Hawaiian atoll: social grouping and population structure. Behav Ecol 16:675–685CrossRefGoogle Scholar
  88. Kiszka J, Perrin WF, Pusineri C, Ridoux V (2011) What drives island-associated tropical dolphins to form mixed-species associations in the southwest Indian Ocean? J Mammal 92:1105–1111CrossRefGoogle Scholar
  89. Kogi K, Hishii T, Imamura A, Iwatani T, Dudzinski KM (2004) Demographic parameters of Indo-Pacific bottlenose dolphins (Tursiops aduncus) around Mikura Island, Japan. Mar Mammal Sci 20:510–526CrossRefGoogle Scholar
  90. Kooyman GL (2009) Diving physiology. In: Perrin WF, Würsig B, Thewissen JGM (eds) Encyclopedia of marine mammals, 2nd edn. Accademic Press, San Diego, pp 327–332CrossRefGoogle Scholar
  91. Lammers MO (2004) Occurrence and behavior of Hawaiian Spinner dolphins (Stenella longirostris) along Oahu’s leeward and south shores. Aquat Mamm 30:237–250CrossRefGoogle Scholar
  92. Lilly JC (1964) Animals in aquatic environments: adaptation of mammals to the ocean. In: Dill DB, Adolph EF, Wilber CG (eds) Handbook of physiology: adaptation to the environment. American Physiological Society, Washington, pp 741–747Google Scholar
  93. Lima SL (1998) Non-lethal effects in the ecology of predator–prey interactions. Bioscience 48:25–34CrossRefGoogle Scholar
  94. Lima SL, Rattenborg NC, Lesku JA, Amlaner CJ (2005) Sleeping under the risk of predation. Anim Behav 70:723–736CrossRefGoogle Scholar
  95. Lundquist D, Gemmell NJ, Würsig B (2012) Behavioural responses of dusky dolphin groups (Lagenorhynchus obscurus) to tour vessels off Kaikoura. New Zealand. PLoS One 7:e41969CrossRefGoogle Scholar
  96. Lusseau D (2003) Male and female bottlenose dolphins Tursiops spp. have different strategies to avoid interactions with tour boats in Doubtful Sound. New Zealand. Mar Ecol Prog Ser 257:267–274CrossRefGoogle Scholar
  97. Lusseau D (2004) The hidden cost of tourism: detecting long-term effects of tourism using behavioral information. Ecol Soc 9:2CrossRefGoogle Scholar
  98. Lusseau D (2006) Why do dolphins jump? Interpreting the behavioural repertoire of bottlenose dolphins (Tursiops sp.) in Doubtful Sound. New Zealand. Behav Processes 73:257–265CrossRefGoogle Scholar
  99. Lusseau D (2007) Evidence for social role in a dolphin social network. Evol Ecol 21:357–366CrossRefGoogle Scholar
  100. 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
  101. Lusseau D, Higham JES (2004) Managing the impacts of dolphin-based tourism through the definition of critical habitats: the case of bottlenose dolphins (Tursiops spp.) in Doubtful Sound. New Zealand. Tour Manag 25:657–667CrossRefGoogle Scholar
  102. Lusseau D, Schneider K, Boisseau OJ, Haase P, Slooten E, Dawson SM (2003) The bottlenose dolphin community of Doubtful Sound features a large proportion of long-lasting associations. Can geographic isolation explain this unique trait? Behav Ecol Sociobiol 54:396–405CrossRefGoogle Scholar
  103. Lusseau D, Slooten L, Currey RJC (2006) Unsustainable dolphin-watching tourism in Fiordland, New Zealand. Tour Mar Environ 3:173–178CrossRefGoogle Scholar
  104. Lyamin OI, Mukhametov LM, Siegel JM, Nazarenko EA, Polyakova IG, Shpak OV (2002) Unihemispheric slow wave sleep and the state of the eyes in a white whale. Behav Brain Res 129:125–129CrossRefGoogle Scholar
  105. Lyamin OI, Mukhametov LM, Siegel JM (2004) Relationship between sleep and eye state in Cetaceans and Pinnipeds. Arch Ital Biol 142:557–568Google Scholar
  106. Mann J (1999) Behavioral sampling methods for cetaceans: a review and critique. Mar Mammal Sci 15:102–122CrossRefGoogle Scholar
  107. Mann J, Würsig B (2014) Observing and quantifying cetacean behavior in the wild: current problems, limitations, and future directions. In: Yamagiwa J, Karczmarski L (eds) Primates and cetaceans: field research and conservation of complex mammalian societies. Springer, New York, pp 335–344CrossRefGoogle Scholar
  108. Martinez E, Orams MB, Stockin KA (2011) Swimming with an endemic and endangered species: effects of tourism on Hector’s dolphins in Akaroa Harbour, Banks Peninsula, New Zealand. Tour Rev Int 14:99–115CrossRefGoogle Scholar
  109. Mellinger DK, Stafford KM, Moore S, Dziak RP, Matsumoto H (2007) An overview of fixed passive acoustic observation methods for cetaceans. Oceanography 20:36–45CrossRefGoogle Scholar
  110. Mukhametov LM, Lyamin OI, Shpak OV, Manger P, Siegel JM (2002) Swimming styles and their relationship to rest and activity states in captive Commerson’s dolphins. In: Proceedings of the 14th Biennial conference on the biology of marine mammals, Vancouver, p 152Google Scholar
  111. Mukhametov LM, Supin AY, Polyakova IG (1977) Interhemispheric asymmetry of the electroencephalographic sleep patterns in dolphins. Brain Res 134:581–584CrossRefGoogle Scholar
  112. Neves K (2010) Cashing in on cetourism: a critical ecological engagement with dominant E-NGO discourses on whaling, cetacean conservation, and whale watching. Antipode 42:719–741CrossRefGoogle Scholar
  113. New LF, Hall AJ, Harcourt R, Kaufman G, Parsons EC, Pearson HC, Cosentino AM, Schick RS (2015) The modelling and assessment of whale-watching impacts. Ocean Coast Manage 115:10–16CrossRefGoogle Scholar
  114. Newton SF (1995) Kingdom of Saudi Arabia. In: Scott DA (ed) A directory of wetlands in the Middle East. IUCN and IWRB, Gland, Switzerland and Slimbridge, pp 1–51Google Scholar
  115. Ng SL, Leung S (2003) Behavioral response of Indo-Pacific humpback dolphin (Sousa chinensis) to vessel traffic. Mar Environ Res 56:555–567CrossRefGoogle Scholar
  116. Norris KS, Dohl TP (1980) Behaviour of the Hawaiian spinner dolphin, Stenella longirostris. Fish Bull 77:821–849Google Scholar
  117. Norris KS, Würsig B, Wells RS, Würsig M (1994) The Hawaiian spinner dolphin. University of California Press, Berkeley and Los AngelesGoogle Scholar
  118. Notarbartolo di Sciara G, Addink M, Baldwin RM, Rudolph P, Smeenk C (2007) A review of cetaceans from the Red Sea. In: Proceedings of the 21st annual conference of the European cetacean society, San SebastianGoogle Scholar
  119. Notarbartolo di Sciara G, Hanafy MH, Fouda MM, Afifi A, Costa M (2009) Spinner dolphin (Stenella longirostris) resting habitat in Samadai Reef (Egypt, Red Sea) protected through tourism management. J Mar Biol Assoc UK 89:211–216CrossRefGoogle Scholar
  120. Notarbartolo di Sciara G, Kerem D, Smeenk C, Rudolph P, Cesario A, Costa M, Elasar M, Feingold D, Fumagalli M, Goffman O, Hadar N, Mebrathu YT, Scheinin A (2017) Cetaceans of the Red Sea. CMS Technical Series 33, 86p. UNEP/CMS SecretariatGoogle Scholar
  121. O’Connor S, Campbell R, Cortez H, Knowles T (2009) Whale watching worldwide. Tourism numbers, expenditures and expanding economic benefits. International Fund for Animal Welfare, Yarmouth, prepared by Economists at LargeGoogle Scholar
  122. Orams MB (1996) Using interpretation to manage nature-based tourism. J Sustain Tour 4:81–94CrossRefGoogle Scholar
  123. Orams MB, Forestell P, Spring J (2014) What’s in for the whales? Exploring the potential contribution of environmental interpretation to conservation. In: Higham J, Bejder L, Williams R (eds) Whale-watching. Cambridge University Press, Cambridge, Sustainable tourism and ecological management, pp 146–162CrossRefGoogle Scholar
  124. Oremus M, Poole M, Steel D, Baker C (2007) Isolation and interchange among insular spinner dolphin communities in the South Pacific revealed by individual identification and genetic diversity. Mar Ecol Prog Ser 336:275–289CrossRefGoogle Scholar
  125. Östman-Lind J (2009) Impacts of human activities on spinner dolphins (Stenella longirostris) in their resting areas. Results from volunteer monitoring between March 2006 and October 2008. National Marine Fisheries Service, Pacific Island Regional OfficeGoogle Scholar
  126. Östman-Lind J, Driscoll-Lind AD, Rickards SH (2004) Delphinid abundance, distribution and habitat use off the western coast of the island of Hawai‘i.LJ-04-02C. National Marine Fisheries Service, Southwest Fisheries Science Center, La Jolla Laboratory, La JollaGoogle Scholar
  127. Parra GJ, Corkeron PJ, Marsh H (2006) Population sizes, site fidelity and residence patterns of Australian snubfin and Indo-Pacific humpback dolphins: implications for conservation. Biol Conserv 129:167–180CrossRefGoogle Scholar
  128. Parsons ECM (2012) The negative impacts of whale-watching. J Mar Biol 2012:ID807294Google Scholar
  129. Perrin WF (2009) Common Dolphins: delphinus delphis and D. capensis. In: Perrin WF, Würsig B, Thewissen JGM (eds) Encyclopedia of marine mammals, 2nd edn. Academic Press, San Diego, pp 255–259CrossRefGoogle Scholar
  130. Perrin WF (2017) World Cetacea Database. (Accessed on 21 June 2017)
  131. Perrin WF, Gilpatrick JWJ (1994) Spinner dolphin Stenella longirostris (Gray, 1828). In: Ridgway SH, Harrison R (eds) Handbook of marine mammals: the first book of dolphins. Academic Press, London, pp 99–128Google Scholar
  132. Perrin WF, Mesnick SL (2003) Sexual ecology of the spinner dolphin, Stenella longirostris: Geographic variation in mating system. Mar Mammal Sci 19:462–483CrossRefGoogle Scholar
  133. Perrin WF, Warner RR, Fiscus CH, Holts DB (1973) Stomach contents of porpoise, Stenella spp., and yellowfin tuna, Thunnus albacares, in mixed-species aggregations. Fish Bull 71:1077–1092Google Scholar
  134. PERSGA Strategic Action Programme Task Force (1998) Strategic action programme for the red sea and gulf of aden. Jeddah, Saudi ArabiaGoogle Scholar
  135. Philpott E, Englund A, Ingram S, Rogan E (2007) Using T-PODs to investigate the echolocation of coastal bottlenose dolphins. J Mar Biol Assoc UK 87:11–17CrossRefGoogle Scholar
  136. Piwetz S, Hung S, Wang J, Lundquist D, Würsig B (2012) Influence of vessel traffic on movements of Indo-Pacific humpback dolphins (Sousa chinensis) off Lantau Island. Hong Kong. Aquat Mamm 38:325CrossRefGoogle Scholar
  137. Ponnampalam LS (2005) Spinner dolphins at Sha’ab Samadai: behaviour and interaction with snorkelers. Cetacean Society InternationalGoogle Scholar
  138. Praca E, Gannier A (2007) Ecological niche of three teuthophageous odontocetes in the northwestern Mediterranean Sea. Ocean Sci Discuss 4:785–815CrossRefGoogle Scholar
  139. Pradel R, Hines JE, Lebreton J-D, Nichols JD (1997) Estimating survival rate and proportion of transients using capture-recapture data from open populations. Biometrics 53:88–99CrossRefGoogle Scholar
  140. Psarakos S, Herzing DL, Marten K (2003) Mixed-species associations between Pantropical spotted dolphins (Stenella attenuata) and Hawaiian spinner dolphins (Stenella longirostris) off Oahu. Hawaii. Aquat Mamm 29:390–395CrossRefGoogle Scholar
  141. Rattenborg NC, Amlaner CJ, Lima SL (2000) Behavioral, neurophysiological and evolutionary perspectives on unihemispheric sleep. Neurosci Biobehav Rev 24:817–842CrossRefGoogle Scholar
  142. Rayment W, Dawson S, Slooten L (2009) Use of T-PODs for acoustic monitoring of Cephalorhynchus dolphins: a case study with Hector’s dolphins in a marine protected area. Endanger Species Res 10:333–339CrossRefGoogle Scholar
  143. Reyes JC (1991) The conservation of small cetaceans: a review. International Whaling Commission SC/43/SM3Google Scholar
  144. Roper CFE, Young R (1975) Vertical distribution of pelagic Cephalopods. Smithson Contrib Zool 209:1–51CrossRefGoogle Scholar
  145. Rosel PE, Mullin KD, Garrison L, Schwacke L, Adams J, Balmer B, Conn P, Conroy MJ, Eguchi T, Gorgone AN, Hohn AL (2011) Photo-identification capture-mark-recapture techniques for estimating abundance of bay, sound and estuary populations of bottlenose dolphins along the U.S. East Coast and Gulf of Mexico: a workshop report. NOAA Technical Memorandum NMFS-SEFSC-621Google Scholar
  146. Samuels A, Bejder L, Constantine R, Heinrich S (2003) A review of swimming with wild cetaceans with a specific focus on the Southern Hemisphere. In: Gales N, Hindell M, Kirkwood R (eds) Marine mammals: fisheries, tourism and management issues. CSIRO Publishing, Collingwood, pp 277–303Google Scholar
  147. Sarhan MI, Hanafy MH, Fouda MM (2004) Economics and sustainable use of Samadai Reef “Dolphin House” Marsa Alam, Red Sea. Egypt, Red Sea Marine Parks and Egyptian Environmental AffairsGoogle Scholar
  148. Senigaglia V, Christiansen F, Bejder L, Gendron D, Lundquist D, Noren DP, Schaffar A, Smith JC, Williams R, Martinez E, Stockin K (2016) Meta-analyses of whale-watching impact studies: comparisons of cetacean responses to disturbance. Mar Ecol Prog Ser 542:251–263CrossRefGoogle Scholar
  149. Serafetinides EA, Shurley JT, Brooks RE (1972) Electroencephalogram of the pilot whale, Globicephala scammoni, in wakefulness and sleep: lateralization aspects. Int J Psychobiol 2:129–135Google Scholar
  150. Shane SH (1995) Behavior patterns of pilot whales and Risso’s dolphins off Santa Catalina Island, California. Aquat Mamm 21:195–197Google Scholar
  151. Shane SH (1990) Behavior and ecology of the bottlenose dolphin at Sanibel Island, Florida. In: Leatherwood S, Reeves RR (eds) The bottlenose dolphin. Academic Press, San Diego, pp 245–265CrossRefGoogle Scholar
  152. Shane SH, Wells RS, Würsig B (1986) Ecology, behavior and social organization of the bottlenose dolphin: a review. Mar Mammal Sci 2:34–63CrossRefGoogle Scholar
  153. Shawky AM, Afifi A (2008) Behaviour of spinner dolphin at Sha’ab Samadai, Marsa Alam, Red Sea. Egypt. Egypt J Biol 10:36–41Google Scholar
  154. Shawky AM, Alwany MA, Zakaria S, El-Etreby SG (2015) Estimation of the abundance of the spinner dolphin Stenella longirostris using photo identification technique in Samadai Reef, Red Sea. Egypt. Catrina Int J Environ Sci 10:61–73Google Scholar
  155. Siegel JM (2005) Clues to the functions of mammalian sleep. Nature 437:1264–1271CrossRefGoogle Scholar
  156. Siegel JM (2008) Do all animals sleep? Trends Neurosci 31:208–213CrossRefGoogle Scholar
  157. Siegel JM (2016) Sleep in animals: a state of adaptive inactivity. In: Kryger M, Roth T (eds) Principles and practice of sleep medicine, 6th edn. Elsevier, Philadelphia, pp 103–114Google Scholar
  158. Sih A (1994) Predation risk and the evolutionary ecology of reproductive behaviour. J Fish Biol 45:111–130CrossRefGoogle Scholar
  159. Silva JM, Silva FJL, Sazima I (2005) Rest, nurture, sex, release, and play: diurnal underwater behaviour of the spinner dolphin at Fernando de Noronha Archipelago, SW Atlantic. Aqua, J Ichthyol Aquat Biol 9:161–176Google Scholar
  160. Smeenk C, Addink MJ, van den Berg AB, Bosman CAW, Cadeé GC (1996) Sightings of Delphinus cf. tropicalis Van Bree, 1971 in the Red Sea. Bonner zoologische Beiträge 46:389–398Google Scholar
  161. Smith HC, Pollock K, Waples K, Bradley S, Bejder L (2013) Use of the robust design to estimate seasonal abundance and demographic parameters of a coastal Bottlenose dolphin (Tursiops aduncus) population. PLoS ONE 8:e76574CrossRefGoogle Scholar
  162. Smith TD, Reeves RR, Josephson EA, Lund JN (2012) Spatial and seasonal distribution of American whaling and whales in the age of sail. PLoS ONE 7:e34905CrossRefGoogle Scholar
  163. Soldevilla MS, Wiggins SM, Hildebrand JA (2010) Spatial and temporal patterns of Risso’s dolphin echolocation in the Southern California Bight. J Acoust Soc Am 127:124–132CrossRefGoogle Scholar
  164. Steckenreuter A, Möller L, Harcourt R (2012) How does Australia’s largest dolphin-watching industry affect the behaviour of a small and resident population of Indo-Pacific bottlenose dolphins? J Environ Manage 97:14–21CrossRefGoogle Scholar
  165. Stensland E, Berggren P (2007) Behavioural changes in female Indo-Pacific bottlenose dolphins in response to boat-based tourism. Mar Ecol Prog Ser 332:225–234CrossRefGoogle Scholar
  166. Stockin KA, Lusseau D, Binedell V, Wiseman N, Orams MB (2008) Tourism affects the behavioural budget of the common dolphin Delphinus sp. in the Hauraki Gulf. New Zealand. Mar Ecol Prog Ser 355:287–295CrossRefGoogle Scholar
  167. Thorne LH, Johnston DW, Urban DL, Tyne J, Bejder L, Baird RW, Yin S, Rickards SH, Deakos MH, Mobley JR, Pack AA (2012) Predictive modeling of Spinner dolphin (Stenella longirostris) resting habitat in the main Hawaiian islands. PLoS ONE 7:e43167CrossRefGoogle Scholar
  168. Timmel G, Courbis S, Sargeant-Green H, Markowitz H (2008) Effects of human traffic on the movement patterns of Hawaiian Spinner dolphins (Stenella longirostris) in Kealakekua Bay. Hawaii. Aquat Mamm 34:402–411CrossRefGoogle Scholar
  169. Tobler I (1989) Napping and polyphasic sleep in mammals. In: Dinges DF, Broughton RJ (eds) Sleep and Alertness: chronobiological, behavioral and medical aspects of napping. Raven Press, New York, pp 9–30Google Scholar
  170. Tyne JA, Johnston DW, Christiansen F, Bejder L (2017) Temporally and spatially partitioned behaviours of spinner dolphins: implications for resilience to human disturbance. Roy Soc Open Sci 4:160626CrossRefGoogle Scholar
  171. Tyne JA, Johnston DW, Rankin R, Loneragan NR, Bejder L (2015) The importance of spinner dolphin (Stenella longirostris) resting habitat: implications for management. J Appl Ecol 52:621–630CrossRefGoogle Scholar
  172. Tyne JA, Pollock KH, Johnston DW, Bejder L (2014) Abundance and survival rates of the Hawai’i Island associated spinner dolphin (Stenella longirostris) stock. PLoS ONE 9:e86132CrossRefGoogle Scholar
  173. Van Dongen H, Maislin G, Mullington J, Dinges D (2003) The cumulative cost of additional wakefulness: dose-response effects on neurobehavioral functions and sleep physiology from chronic sleep restriction and total sleep deprivation. Sleep 26:117–129CrossRefGoogle Scholar
  174. Van Parijs SM, Corkeron PJ (2001) Boat traffic affects the acoustic behaviour of Pacific humpback dolphins, Sousa chinensis. J Mar Biol Assoc UK 81:533–538CrossRefGoogle Scholar
  175. Visser F, Hartman KL, Rood EJ, Hendriks AJ, Zult DB, Wolff WJ, Huisman J, Pierce GJ (2011) Risso’s dolphins alter daily resting pattern in response to whale watching at the Azores. Mar Mammal Sci 27:366–381CrossRefGoogle Scholar
  176. Wang JY, Yang SC (2009) Indo-Pacific bottlenose dolphin, Tursiops aduncus. In: Perrin WF, Würsig B, Thewissen JGM (eds) Encyclopedia of marine mammals, 2nd edn. Academic Press, San Diego, pp 602–608Google Scholar
  177. Wang K, Wang D, Akamatsu T, Li S, Xiao J (2005) A passive acoustic monitoring method applied to observation and group size estimation of finless porpoises. J Acoust Soc Am 118:1180–1185CrossRefGoogle Scholar
  178. Webster I, Cockcroft V, Cadinouche A (2015) Spinner dolphins Stenella longirostris off south-west Mauritius: abundance and residency. African J Mar Sci 37:115–124CrossRefGoogle Scholar
  179. Weitkowitz W (1992) Sightings of whales and dolphins in the Middle East (Cetacea). Zool Middle East 6:5–12CrossRefGoogle Scholar
  180. Whitehead H (2001) Analysis of animal movement using opportunistic individual identifications: application to sperm whales. Ecology 82:1417–1432CrossRefGoogle Scholar
  181. Whitehead H (2007) Selection of models of Lagged Identification Rates and Lagged Association Rates using AIC and QAIC. Commun Stat—Simul Comput 36:1233–1246CrossRefGoogle Scholar
  182. Wijnen H, Young MW (2006) Interplay of circadian clocks and metabolic rhythms. Annu Rev Genet 40:409–448CrossRefGoogle Scholar
  183. Williams R, Lusseau D (2006) A killer whale social network is vulnerable to targeted removals. Biol Lett 2:497–500CrossRefGoogle Scholar
  184. 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
  185. Wilson C, Tisdell C (2001) Sea turtles as a non-consumptive tourism resource especially in Australia. Tour Manag 22:279–288CrossRefGoogle Scholar
  186. Wolpert EA (1969) A manual of standardized terminology, techniques and scoring system for sleep stages of human subjects. Arch Gen Psychiatry 20:246–247CrossRefGoogle Scholar
  187. Würsig B (1996) Swim-with-dolphin activities in nature: weighing the pros and cons. Whalewatcher 30:11–15Google Scholar
  188. Würsig B, Jefferson TA (1990) Methods of photo-identification for small cetaceans. International Whaling Commission, CambridgeGoogle Scholar
  189. Zepelin H, Siegel JM, Tobler I (2005) Mammalian sleep. In: Kryger MH, Roth T, Dement WC (eds) Principles and practice of sleep medicine, 4th edn. Saunders, Philadelphia, W.B, pp 91–100CrossRefGoogle Scholar
  190. Zeppel H, Muloin S (2007) Marine wildlife tours: benefits for participants. In: Higham JES, Luck M (eds) Marine wildlife and tourism management: insights from the natural and social sciences. CABI, Wallingford, pp 19–48CrossRefGoogle Scholar
  191. Ziltener A, Wright AJ, Kreicker S (2015) Sleeping behaviour in Indo-Pacific bottlenose dolphins (Tursiops aduncus) off Hurghada, northern Red Sea, Egypt. In: 22nd Biennial Conference on the biology of marine mammals. The Society for Marine Mammalogy, San FranciscoGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Maddalena Fumagalli
    • 1
    • 2
    Email author
  • Amina Cesario
    • 2
    • 3
  • Marina Costa
    • 2
    • 4
  1. 1.Department of ZoologyUniversity of OtagoDunedinNew Zealand
  2. 2.Tethys Research InstituteMilanoItaly
  3. 3.Swire Institute of Marine Science, School of Biological SciencesUniversity of Hong KongHong Kong SARChina
  4. 4.South Atlantic Environmental Research Institute (SAERI), Stanley CottageStanleyFalkland Islands

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