Marine Biology

, 165:11 | Cite as

Effects of auditory and visual stimuli on shark feeding behaviour: the disco effect

  • Laura A. Ryan
  • Lucille Chapuis
  • Jan M. Hemmi
  • Shaun P. Collin
  • Robert D. McCauley
  • Kara E. Yopak
  • Enrico Gennari
  • Charlie Huveneers
  • Ryan M. Kempster
  • Caroline C. Kerr
  • Carl Schmidt
  • Channing A. Egeberg
  • Nathan S. Hart
Original paper

Abstract

Sensory systems play a central role in guiding animal behaviour. They can be manipulated to alter behavioural outcomes to limit negative interactions between humans and animals. Sharks are often seen as a threat to humans and there has been increasing interest in developing shark mitigation devices. Previous research has concentrated on stimulating the electrosensory and olfactory systems of sharks, whereas the influence of light and sound on their behaviour has received little attention. In this study, the effects of an intense strobe light and a loud, artificial sound composed of mixed frequencies and intensities on shark behaviour were assessed. We tested these stimuli individually and in combination on wild-caught captive Port Jackson (Heterodontus portusjacksoni) and epaulette (Hemiscyllium ocellatum) sharks in aquaria and on wild great white sharks (Carcharodon carcharias) in the field. When presented alone and in combination with sound, the lights reduced the number of times that the bait was taken by both H. portusjacksoni and H. ocellatum in captivity. The strobe light alone, however, did not affect the behaviour of white sharks, but when presented in combination with sound, white sharks spent significantly less time in proximity to the bait. As the lights and sound presented in this study did not show a pronounced deterrent effect on C. carcharias, we do not advise their use as a strategy for mitigating shark–human interactions. However, due to the potential effectiveness of strobe lights in deterring other species of sharks, there may be applications for this approach in the reduction of fisheries bycatch.

Notes

Acknowledgements

We would like to acknowledge the financial support of the Western Australian State Government to NSH and SPC and Sea World Research & Rescue Foundation (Grant SWR/6/2014 to NSH, LAR, JMH and SPC and Grant SWR/3/2013 to SPC, LC, RDM and NSH). The UWA Neuroecology Group would also like to express sincere gratitude and appreciation for the continued support and generous financial assistance provided by Craig and Katrina Burton. We thank all the staff and volunteers at Oceans Research who helped us in Mossel Bay. We are grateful to Friedrich Ladich, Christopher Braun, Timothy Tricas, Neil Hammerschlag, Richard Brill and Tamara Frank for their comments on an earlier version of the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

All applicable international, national, and/or institutional guidelines for the care and use of the animals were followed. This article does not contain any studies with human participants performed by any of the authors.

Supplementary material

227_2017_3256_MOESM1_ESM.pdf (273 kb)
Supplementary material 1 (PDF 272 kb)

References

  1. Anderson JJ, Puckett KJ, Nemeth RS (1998) Studies on the effect of behavior on fish guidance efficiency at the Rocky Reach Dam: Avoidance to strobe light and other stimuli. Fisheries Research Institute of the University of Washington, SeattleGoogle Scholar
  2. Anderson SD, Chapple TK, Jorgensen SJ, Klimley AP, Block BA (2011) Long-term individual identification and site fidelity of white sharks, Carcharodon carcharias, off California using dorsal fins. Mar Biol 158:1233–1237CrossRefGoogle Scholar
  3. Baldridge HD (1996) Comments on means for avoidance or deterrence of white-shark attacks on humans. In: Klimley AP, Ainley DG (eds) Great white sharks: the biology of Carcharodon carcharias. Academic Press, San Diego, pp 447–479Google Scholar
  4. Banner A (1967) Evidence of sensitivity to acoustic displacements in the lemon shark, Negaprion brevirostris (Poey). In: Cahn PH (ed) Lateral line detectors. Indiana University Press, Bloomington, pp 265–273Google Scholar
  5. Banner A (1972) Use of sound in predation by young lemon sharks, Negaprion brevirostris (Poey). Bull Mar Sci 22:251–283Google Scholar
  6. Barley SC, Meeka MG, Meeuwig JJ (2017) Species diversity, abundance, biomass, size and trophic structure of fish on coral reefs in relation to shark abundance. Mar Ecol Prog Ser 565:163–179CrossRefGoogle Scholar
  7. Bates D, Maechler M, Bolker B, Walker S (2013) lme4: Linear mixed-effects models using Eigen and S4. R package version 1. http://lme4.r-forge.r-project.org/
  8. Bedore CN, Kajiura SM (2013) Bioelectric fields of marine organisms: voltage and frequency contributions to detectability by electroreceptive predators. Physiol Biochem Zool 86:298–311CrossRefGoogle Scholar
  9. Block BA, Carey FG (1985) Warm brain and eye temperatures in sharks. J Comp Physiol B 156:229–236CrossRefGoogle Scholar
  10. Brill R, Bushnell P, Smith L, Speaks C, Sundaram R, Stroud E, Wang J (2009) The repulsive and feeding-deterrent effects of electropositive metals on juvenile sandbar sharks (Carcharhinus plumbeus). Fish Bull 107:298–307Google Scholar
  11. Bullock TH, Corwin JT (1979) Acoustic evoked activity in the brain in sharks. J Comp Physiol 129:223–234CrossRefGoogle Scholar
  12. Byrnes EE, Brown C (2016) Individual personality differences in Port Jackson sharks Heterodontus portusjacksoni. J Fish Biol 89:1142–1157CrossRefGoogle Scholar
  13. Camhi MD, Valenti SV, Fordham SV (2007) The conservation status of pelagic sharks and rays. University of Oxford, Tubney HouseGoogle Scholar
  14. Campbell NA, Reece JB, Meyers N (2005) Sensory and motor mechanisms: the vertebrate visual system. Biology, 7th edn. Pearson Education, Sydney, pp 1060–1065Google Scholar
  15. Casper BM (2006) The hearing abilities of elasmobranch fishes. PhD Thesis, Department of Marine Science, University of South FloridaGoogle Scholar
  16. Casper BM, Mann DA (2006) Evoked potential audiograms of the nurse shark (Ginglymostoma cirratum) and the yellow stingray (Urobatis jamaicensis). Environ Biol Fishes 76:101–108CrossRefGoogle Scholar
  17. Casper BM, Mann DA (2007a) Dipole hearing measurements in elasmobranch fishes. J Exp Biol 210:75–81CrossRefGoogle Scholar
  18. Casper BM, Mann DA (2007b) The directional hearing abilities of two species of bamboo sharks. J Exp Biol 210:505–511CrossRefGoogle Scholar
  19. Casper BM, Lobel PS, Yan HY (2003) The hearing sensitivity of the little skate, Raja erinacea: a comparison of two methods. Environ Biol Fishes 68:371–379CrossRefGoogle Scholar
  20. Chalupa LM, Werner JS (2004) The visual neurosciences. MIT press, CambridgeGoogle Scholar
  21. Clarke MR, Pascoe P (1985) The influence of an electric light on the capture of deep-sea animals by a midwater trawl. J Mar Biol Assoc UK 65:373–393CrossRefGoogle Scholar
  22. Collin SP (2012) The neuroecology of cartilaginous fishes: sensory strategies for survival. Brain Behav Evol 80:80–96CrossRefGoogle Scholar
  23. Compagno LJV (1990) Alternative life-history styles of cartilaginous fishes in time and space. Environ Biol Fishes 28:33–75CrossRefGoogle Scholar
  24. Corwin J (1978) The relation of inner ear structure to the feeding behavior in sharks and rays. Scanning Electron Microsc 2:1105–1112Google Scholar
  25. Corwin JT (1989) Functional anatomy of the auditory system in sharks and rays. J Exp Zool 252:62–74. https://doi.org/10.1002/jez.1402520408 CrossRefGoogle Scholar
  26. Curtis TH, Bruce BD, Cliff C et al (2012) Responding to the risk of white shark attack: updated statistics, prevention, control methods and recommendations. In: Domeier M (ed) Global perspectives on the biology and life history of the white shark. CRC Press, Boca Raton, pp 477–510CrossRefGoogle Scholar
  27. Domeier ML, Nasby-Lucas N (2007) Annual re-sightings of photographically identified white sharks (Carcharodon carcharias) at an eastern Pacific aggregation site (Guadalupe Island, Mexico). Mar Biol 150:977–984CrossRefGoogle Scholar
  28. Dulvy NK et al (2008) You can swim but you can’t hide: the global status and conservation of oceanic pelagic sharks and rays. Aquat Conserv 18:459–482. https://doi.org/10.1002/aqc.975 CrossRefGoogle Scholar
  29. Evangelista C, Mills M, Siebeck UE, Collin SP (2010) A comparison of the external morphology of the membranous inner ear in elasmobranchs. J Morphol 271:483–495Google Scholar
  30. Ferretti F, Worm B, Britten GL, Heithaus MR, Lotze HK (2010) Patterns and ecosystem consequences of shark declines in the ocean. Ecol Lett 13:1055–1071. https://doi.org/10.1111/j.1461-0248.2010.01489.x Google Scholar
  31. Fritsches KA, Brill RW, Warrant EJ (2005) Warm eyes provide superior vision in swordfishes. Curr Biol 15:55–58CrossRefGoogle Scholar
  32. Froese R, Pauly D (2013) FishBase. http://www.fishbase.org
  33. Fuss T, Bleckmann H, Schluessel V (2014) Place learning prior to and after telencephalon ablation in bamboo and coral cat sharks (Chiloscyllium griseum and Atelomycterus marmoratus). J Comp Physiol A 200:37–52CrossRefGoogle Scholar
  34. Gacic Z, Milosevic M, Mickovic B, Nikcevic M, Damjanovic I (2015) Effects of acute cooling on fish electroretinogram: a comparative study. Comp Biochem Physiol Part A 184:150–155CrossRefGoogle Scholar
  35. Gardiner JM, Hueter RE, Maruska KP, Sisneros JA, Casper BM, Mann DA, Demski LS (2012) Sensory physiology and behavior of elasmobranchs. Biology of sharks and their relatives, vol 1. CRC Press, Boca RatonGoogle Scholar
  36. Gardiner JM, Atema J, Hueter RE, Motta PJ (2014) Multisensory integration and behavioral plasticity in sharks from different ecological niches. PLoS One 9:e93036CrossRefGoogle Scholar
  37. Gilbert PW (1970) Studies on the anatomy, physiology, and behavior of sharks. Final report office of naval research, WashingtonGoogle Scholar
  38. Gilman E et al (2007) Shark depredation and unwanted bycatch in pelagic longline fisheries: industry practices and attitudes, and shark avoidance strategies. Western Pacific Regional Fishery Management Council, HonoluluGoogle Scholar
  39. Gilman E et al (2008) Shark interactions in pelagic longline fisheries. Mar Policy 32:1–18CrossRefGoogle Scholar
  40. Godin AC, Wimmer T, Wang JH, Worm B (2013) No effect from rare-earth metal deterrent on shark bycatch in a commercial pelagic longline trial. Fish Res 143:131–135CrossRefGoogle Scholar
  41. Gribble N, McPherson G, Lane B (1998) Effect of the Queensland Shark Control Program on non-target species: whale, dugong, turtle and dolphin: a review. Mar Freshw Res 49:645–651CrossRefGoogle Scholar
  42. Gruber SH, Cohen JL (1985) Visual system of the white shark, Carcharodon carcharias, with emphasis on retinal structure. Mem South Calif Acad Sci 9:61–72Google Scholar
  43. Hammerschlag N, Martin RA, Fallows C, Collier RS, Lawrence R (2012) Investigatory behavior toward surface objects and nonconsumptive strikes on seabirds by white sharks, Carcharodon carcharias, at Seal Island, South Africa (1997–2010). In: Domeier ML (ed) Global perspectives on the biology and life history of the white shark. CRC Press, Boca RatonGoogle Scholar
  44. Hart NS, Collin SP (2015) Sharks senses and shark repellents. Integr Zool 10:38–64CrossRefGoogle Scholar
  45. Hart NS, Lisney TJ, Collin SP (2006) Visual communication in elasmobranchs. In: Ladich F, Collin SP, Moller P, Kapoor BG (eds) Communication in fishes. Science Publishers Enfield, PlymouthGoogle Scholar
  46. Hobson ES (1963) Feeding behavior in three species of sharks. Pac Sci 17:171–194Google Scholar
  47. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363CrossRefGoogle Scholar
  48. Hueter RE, Mann DA, Maruska KP, Sisneros JA, Demski LS (2004) Sensory biology of elasmobranches. CRC Press, LondonGoogle Scholar
  49. Hutchinson M, Wang JH, Swimmer Y, Holland K, Kohin S, Dewar H, Wraith J, Vetter R, Heberer C, Martinez J (2012) The effects of a lanthanide metal alloy on shark catch rates. Fish Res 131–133:45–51CrossRefGoogle Scholar
  50. Huveneers C, Rogers PJ, Semmens JM, Beckmann C, Kock AA, Page B, Goldsworthy SD (2013a) Effects of an electric field on white sharks: in situ testing of an electric deterrent. PLoS One 8:e62730CrossRefGoogle Scholar
  51. Huveneers C, Rogers PJ, Beckmann C, Semmens JM, Bruc BD, Seuront L (2013b) The effects of cage-diving activities on the fine-scale swimming behaviour and space use of white sharks. Mar Biol 160:2863–2875CrossRefGoogle Scholar
  52. Jacoby DM, Croft DP, Sims DW (2012) Social behaviour in sharks and rays: analysis, patterns and implications for conservation. Fish Fish 13:399–417CrossRefGoogle Scholar
  53. Johnson PN, Bouchard K, Goetz FA (2005) Effectiveness of strobe lights for reducing juvenile salmonid entrainment into a navigation lock. N Am J Fish Manag 25:491–501CrossRefGoogle Scholar
  54. Johnson RL et al. (2005b) Strobe light deterrent efficacy test and fish behavior determination at Grand Coulee Dam third powerplant forebay. Report PNNL-15007, Pacific Northwest National Laboratory, RichlandGoogle Scholar
  55. Kalinoski M, Hirons A, Horodysky A, Brill R (2014) Spectral sensitivity, luminous sensitivity, and temporal resolution of the visual systems in three sympatric temperate coastal shark species. J Comp Physiol A 200:997–1013CrossRefGoogle Scholar
  56. Kelly JC, Nelson DR (1975) Hearing thresholds of the horn shark, Heterodontus francisci. J Acoust Soc Am 58:905–909CrossRefGoogle Scholar
  57. Kempster RM, Garza-Gisholt E, Egeberg CA, Hart NS, O’Shea OR, Collin SP (2014) Sexual dimorphism of the electrosensory system: a quantitative analysis of nerve axons in the dorsal anterior lateral line nerve of the blue- spotted fantail stingray (Taeniura lymma). Brain Behav Evol 81:226–235CrossRefGoogle Scholar
  58. Kempster RM, Egeberg CA, Hart NS, Ryan L, Chapuis L, Kerr CC, Schmidt C, Huveneers C, Gennari E, Yopak KE, Meeuwig JJ, Collin SP (2016) How close is too close? The effect of a non-lethal electric shark deterrent on white shark behaviour. PLoS One 11:e0157717CrossRefGoogle Scholar
  59. Kenyon T, Ladich F, Yan H (1998) A comparative study of hearing ability in fishes: the auditory brainstem response approach. J Comp Physiol A 182:307–318CrossRefGoogle Scholar
  60. Klimley AP, Myrberg AA (1979) Acoustic stimuli underlying withdrawal from a sound source by adult lemon sharks, Negaprion brevirostris (Poey). Bull Mar Sci 29:447–458Google Scholar
  61. Kock A, Johnson R (2006) White shark abundance: not a causative factor in numbers of shark bite incidents. In: Nel DC, Peschak TP (eds) Finding a balance: white shark conservation and recreational safety in the inshore waters of Cape Town, South Africa. South Africa Report Series, Cape Town, pp 1–19Google Scholar
  62. Kritzler H, Wood L (1961) Provisional audiogram for the shark, Carcharhinus leucas. Science 133:1480–1482CrossRefGoogle Scholar
  63. Land MF, Nilsson D (2012) Animal eyes. Oxford University Press, New YorkCrossRefGoogle Scholar
  64. Last PR, Stevens JD (2009) Sharks and rays of Australia. CSIRO Publishing, Collingwood, Victoria, AustraliaGoogle Scholar
  65. Letessier TB et al (2013) Assessing pelagic fish populations: the application of demersal video techniques to the mid-water environment. Methods Oceanogr 8:41–55CrossRefGoogle Scholar
  66. Lewison RL, Crowder LB, Read AJ, Freeman SA (2004) Understanding impacts of fisheries bycatch on marine megafauna. Trends Ecol Evol 19:598–604CrossRefGoogle Scholar
  67. Lisney TJ, Collin SP (2007) Relative eye size in elasmobranchs. Brain Behav Evol 69:266–279CrossRefGoogle Scholar
  68. Lisney TJ, Bennett MB, Collin SP (2007) Volumetric analysis of sensory brain areas indicates ontogenetic shifts in the relative importance of sensory systems in elasmobranchs. Raffles Bull Zool 14:7–15Google Scholar
  69. Lisney TJ, Yopak KE, Camilieri-Asch V, Collin SP (2017) Ontogenetic shifts in brain organization in the bluespotted stingray Neotrygon kuhlii (Chondrichthyes: Dasyatidae). Brain Behav Evol 89:68–83CrossRefGoogle Scholar
  70. Litherland L, Collin SP (2008) Comparative visual function in elasmobranchs: spatial arrangement and ecological correlates of photoreceptor and ganglion cell distributions. Vis Neurosci 25:549–561CrossRefGoogle Scholar
  71. Madliger CL (2012) Toward improved conservation management: a consideration of sensory ecology. Biodivers Conserv 21:3277–3286. https://doi.org/10.1007/s10531-012-0363-6 CrossRefGoogle Scholar
  72. Marchesan M, Spoto M, Verginella L, Ferrero EA (2005) Behavioural effects of artificial light on fish species of commercial interest. Fish Res 73:171–185CrossRefGoogle Scholar
  73. Marcotte MM, Lowe CG (2008) Behavioral responses of two species of sharks to pulsed, direct current electrical fields: testing a potential shark deterrent. Mar Technol Soc J 42:53–61CrossRefGoogle Scholar
  74. Martin RA (2007) A review of shark agonistic displays: comparison of display features and implications for shark–human interactions. Mar Freshw Behav Physiol 40:3–34CrossRefGoogle Scholar
  75. McComb DM, Frank TM, Hueter RE, Kajiura SM (2010) Temporal resolution and spectral sensitivity of the visual system of three coastal shark species from different light environments. Physiol Biochem Zool 83:299–307CrossRefGoogle Scholar
  76. McFarland W (1990) Light in the sea: the optical world of elasmobranchs. J Exp Zool 256:3–12CrossRefGoogle Scholar
  77. McIninch S, Hocutt C (1987) Effects of turbidity on estuarine fish response to strobe lights. J Appl Ichthyol 3:97–105CrossRefGoogle Scholar
  78. Mettke-Hofmann C, Winkler H, Leisler B (2002) The significance of ecological factors for exploration and neophobia in parrots. Ethology 108:249–272CrossRefGoogle Scholar
  79. Meyer CG, Holland KN, Papastamatiou YP (2005) Sharks can detect changes in the geomagnetic field. J R Soc Interface 2:129–130CrossRefGoogle Scholar
  80. Mills M, Rasch R, Siebeck UE, Collin SP (2011) Exogenous material in the inner ear of the adult Port Jackson shark, Heterodontus portusjacksoni (Elasmbranchii). Anat Rec 294:373–378CrossRefGoogle Scholar
  81. Myrberg AA (2001) The acoustical biology of elasmobranchs. Environ Biol Fishes 60:31–45CrossRefGoogle Scholar
  82. Myrberg A, Banner A, Richard J (1969) Shark attraction using a video-acoustic system. Mar Biol 2:264–276CrossRefGoogle Scholar
  83. Myrberg AA, Ha SJ, Walewski S, Banbury JC (1972) Effectiveness of acoustic signals in attracting epipelagic sharks to an underwater sound source. Bull Mar Sci 22:926–949Google Scholar
  84. Myrberg AA, Gordon CR, Klimley AP (1978) Rapid withdrawal from a sound source by open-ocean sharks. J Acoust Soc Am 64:1289–1297CrossRefGoogle Scholar
  85. Neff CL, Yang JY (2013) Shark bites and public attitudes: policy implications from the first before and after shark bite survey. Mar Policy 38:545–547CrossRefGoogle Scholar
  86. Nelson DR, Gruber SH (1963) Sharks: attraction by low-frequency sounds. Science 142:975–977CrossRefGoogle Scholar
  87. Newton KC, Kajiura SM (2017) Magnetic field discrimination, learning, and memory in the yellow stingray (Urobatis jamaicensis). Anim Cogn 20:603–614CrossRefGoogle Scholar
  88. Parker G (1910) Influence of the eyes, ears, and other allied sense organs on the movements of the dogfish, Mustelus canis (Mitchill). US Government Printing Office, Washington, D.CGoogle Scholar
  89. Parvulescu A (1967) The acoustics of small tanks. In: Tavolga WN (ed) Marine bioacoustics II. Pergamon, Oxford, pp 7–13Google Scholar
  90. Pascoe P (1990) Light and the capture of marine animals. Light and life in the sea. Cambridge University Press, CambridgeGoogle Scholar
  91. Patrick PH, Christie A, Sager D, Hocutt C, Stauffer J (1985) Responses of fish to a strobe light/air-bubble barrier. Fish Res 3:157–172CrossRefGoogle Scholar
  92. Peschak TP, Scholl MC (2006) South Africa’s great white shark. Struik Publishers, Cape TownGoogle Scholar
  93. Ploskey G, Nestler J, Weeks G (1995) Evaluation of an integrated fish-protection system. American Society of Civil Engineers, New YorkGoogle Scholar
  94. Popper AN, Fay R (1997) Evolution of the ear and hearing: issues and questions. Brain Behav Evol 50:213–221CrossRefGoogle Scholar
  95. Reid DD, Robbins WD, Peddemors VM (2011) Decadal trends in shark catches and effort from the New South Wales, Australia, Shark Meshing Program 1950–2010. Mar Freshw Res 62:676–693. https://doi.org/10.1071/Mf10162 CrossRefGoogle Scholar
  96. Ritter EK, Godknecht AJ, Ross S (2000) Agonistic displays in the blacktip shark (Carcharhinus limbatus). Copeia 2000:282–284CrossRefGoogle Scholar
  97. Rizzari JR, Frisch AJ, Connolly SR (2014) How robust are estimates of coral reef shark depletion? Biol Conserv 176:39–47CrossRefGoogle Scholar
  98. Robbins W, Peddemors V, Kennelly S (2011) Assessment of permanent magnets and electropositive metals to reduce the line-based capture of Galapagos sharks, Carcharhinus galapagensis. Fish Res 109:100–106CrossRefGoogle Scholar
  99. Rogers PH, Hawkins AD, Popper AN, Fay RR, Gray MD (2016) Parvulescu revisited: small tank acoustics for bioacousticinas. In: Popper AN, Hawkins A (eds) The effects of noise on aquatic life II. Springer, New York, USA, pp 933–941CrossRefGoogle Scholar
  100. Ryan LA, Hemmi JM, Collin SP, Hart NS (2017) Electrophysiological measures of temporal resolution, contrast sensitivity and spatial resolving power in sharks. J Comp Physiol A 203:197–210CrossRefGoogle Scholar
  101. Sager DR, Hocutt CH, Stauffer JR (1987) Estuarine fish responses to strobe light, bubble curtains and strobe light/bubble-curtain combinations as influenced by water flow rate and flash frequencies. Fish Res 5:383–399CrossRefGoogle Scholar
  102. Schieber NL, Collin SP, Hart NS (2012) Comparative retinal anatomy in four species of elasmobranch. J Morphol 273:423–440CrossRefGoogle Scholar
  103. Sih A, Bell A, Johnson JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:372–378CrossRefGoogle Scholar
  104. Sneddon LU, Braithwaite VA, Gentle MJ (2003) Novel object test: examining nociception and fear in the rainbow trout. J Pain 4:431–440CrossRefGoogle Scholar
  105. Southwood A, Fritsches K, Brill R, Swimmer Y (2008) Sound, chemical, and light detection in sea turtles and pelagic fishes: sensory-based approaches to bycatch reduction in longline fisheries. Endanger Species Res 5:225–238CrossRefGoogle Scholar
  106. Stein BE, Wallace MT, Stanford TR (2008) Brain mechanisms for synthesizing information from different sensory modalities. In: Goldstein E (ed) Blackwell handbook of sensation and perception. Blackwell Publishing Ltd, Malden, USA, pp 709–736Google Scholar
  107. Stell WK (1972) The structure and morphologic relations of rods and cones in the retina of the spiny dogfish, Squalus. Comp Biochem Physiol A Physiol 42:141–151. https://doi.org/10.1016/0300-9629(72)90374-x CrossRefGoogle Scholar
  108. Stoner AW, Kaimmer SM (2008) Reducing elasmobranch bycatch: laboratory investigation of rare earth metal and magnetic deterrents with spiny dogfish and Pacific halibut. Fish Res 92:162–168CrossRefGoogle Scholar
  109. Strong WR (1996) Shape discrimination and visual predatory tactics in white sharks. In: Klimley P, Ainley DG (eds) Great white sharks: the biology of Carcharodon carcharias. Academic Press, New York, pp 229–240CrossRefGoogle Scholar
  110. Tallack SM, Mandelman JW (2009) Do rare-earth metals deter spiny dogfish? A feasibility study on the use of electropositive “mischmetal” to reduce the bycatch of Squalus acanthias by hook gear in the Gulf of Maine. ICES J Mar Sci 66:315–322CrossRefGoogle Scholar
  111. R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  112. 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
  113. Wearmouth VJ, Sims DW (2008) Sexual segregation in marine fish, reptiles, birds and mammals: behaviour patterns, mechanisms and conservation implications. Adv Mar Biol 54:107–170CrossRefGoogle Scholar
  114. West JG (2011) Changing patterns of shark attacks in Australian waters. Mar Freshw Res 62:744–754CrossRefGoogle Scholar
  115. Wetherbee BM, Lowe CG, Crow GL (1994) A review of shark control in Hawaii with recommendations for future research. Pac Sci 48:95–115Google Scholar
  116. Wetherbee BM, Cortés E, Bizzarro JJ (2012) Food consumption and feeding habits. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives. CRC Press, Baco Raton, pp 239–264CrossRefGoogle Scholar
  117. Wiebe PH, Ashjian CJ, Gallager SM, Davis CS, Lawson GL, Copley NJ (2004) Using a high-powered strobe light to increase the catch of Antarctic krill. Mar Biol 144:493–502CrossRefGoogle Scholar
  118. Winer BJ (1962) Latin squares and related designs. In: Winer BJ (ed) Statistical principles in experimental design. McGraw-Hill Book Company, New York, pp 514–577CrossRefGoogle Scholar
  119. Yopak KE, Lisney TJ (2012) Allometric scaling of the optic tectum in cartilaginous fishes. Brain Behav Evol 80:108–126CrossRefGoogle Scholar
  120. Yopak KE, Montgomery JC (2008) Brain organization and specialization in deep-sea chondrichthyans. Brain Behav Evol 71:287–304CrossRefGoogle Scholar
  121. Yopak KE, Lisney TJ, Collin SP (2015) Not all sharks are ‘swimming noses’. Variation in olfactory bulb size in cartilaginous fishes. Brain Struct Funct 220:1127–1143CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Laura A. Ryan
    • 1
    • 2
    • 3
  • Lucille Chapuis
    • 1
    • 2
  • Jan M. Hemmi
    • 1
    • 2
  • Shaun P. Collin
    • 1
    • 2
  • Robert D. McCauley
    • 4
  • Kara E. Yopak
    • 1
    • 2
    • 5
  • Enrico Gennari
    • 6
    • 7
    • 8
  • Charlie Huveneers
    • 9
  • Ryan M. Kempster
    • 1
    • 2
  • Caroline C. Kerr
    • 1
    • 2
  • Carl Schmidt
    • 1
    • 2
  • Channing A. Egeberg
    • 1
    • 2
  • Nathan S. Hart
    • 1
    • 2
    • 3
  1. 1.School of Biological SciencesThe University of Western AustraliaCrawleyAustralia
  2. 2.The UWA Oceans Institute, The University of Western AustraliaCrawleyAustralia
  3. 3.Department of Biological SciencesMacquarie UniversityNorth RydeAustralia
  4. 4.Centre for Marine Science and TechnologyCurtin UniversityPerthAustralia
  5. 5.School of Biology and Marine Biology and the Center for Marine ScienceUniversity of North Carolina WilmingtonWilmingtonUSA
  6. 6.Oceans ResearchMossel BaySouth Africa
  7. 7.South African Institute for Aquatic BiodiversityGrahamstownSouth Africa
  8. 8.Department of Ichthyology and Fisheries ScienceRhodes UniversityGrahamstownSouth Africa
  9. 9.School of Biological SciencesFlinders UniversityBedford ParkAustralia

Personalised recommendations