Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

The distribution and abundance of electrosensory pores in two benthic sharks: a comparison of the wobbegong shark, Orectolobus maculatus, and the angel shark, Squatina australis

Channing A. Egeberg A , Ryan M. Kempster A C , Susan M. Theiss B , Nathan S. Hart A and Shaun P. Collin A

A The UWA Oceans Institute and the School of Animal Biology, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.

B Fisheries Queensland, Department of Agriculture, Fisheries and Forestry, GPO Box 46, Brisbane, Queensland 4001, Australia.

C Corresponding author. Email: ryankempster@supportoursharks.com

Marine and Freshwater Research 65(11) 1003-1008 http://dx.doi.org/10.1071/MF13213
Submitted: 8 August 2013  Accepted: 10 February 2014   Published: 17 October 2014

Abstract

Electroreception is an ancient sense found in many aquatic animals, including sharks, which may be used in the detection of prey, predators and mates. Wobbegong sharks (Orectolobidae) and angel sharks (Squatinidae) represent two distantly related families that have independently evolved a similar dorso-ventrally compressed body form to complement their benthic ambush feeding strategy. Consequently, these groups represent useful models in which to investigate the specific morphological and physiological adaptations that are driven by the adoption of a benthic lifestyle. In this study, we compared the distribution and abundance of electrosensory pores in the spotted wobbegong shark (Orectolobus maculatus) with the Australian angel shark (Squatina australis) to determine whether both species display a similar pattern of clustering of sub-dermal electroreceptors and to further understand the functional importance of electroreception in the feeding behaviour of these benthic sharks. Orectolobus maculatus has a more complex electrosensory system than S. australis, with a higher abundance of pores and an additional cluster of electroreceptors positioned in the snout (the superficial ophthalmic cluster). Interestingly, both species possess a cluster of pores (the hyoid cluster, positioned slightly posterior to the first gill slit) more commonly found in rays, but which may be present in all benthic elasmobranchs to assist in the detection of approaching predators.

Additional keywords: ambush feeding behaviour, ampullae of Lorenzini, Elasmobranch, electroreception, predator avoidance.


References

Bodznick, D., and Schmidt, A. (1984). Somatotopy within the medullary electrosensory nucleus of the little skate, Raja erinacea. The Journal of Comparative Neurology 225, 581–590.
Somatotopy within the medullary electrosensory nucleus of the little skate, Raja erinacea.CrossRef | 1:STN:280:DyaL2c3ktVeltQ%3D%3D&md5=642b24180840c984c8015000715c7c02CAS | 6736290PubMed | open url image1

Bratton, B., and Ayers, J. (1987). Observations on the electric organ discharge of two skate species (Chondrichthyes: Rajidae) and its relationship to behaviour. Environmental Biology of Fishes 20, 241–254. open url image1

Camilieri-Asch, V., Kempster, R. M., Collin, S. P., Johnstone, R., and Theiss, S. M. (2013). A comparison of the electrosensory morphology of a euryhaline and a marine stingray. Zoology (Jena, Germany) 116, 270–276.
A comparison of the electrosensory morphology of a euryhaline and a marine stingray.CrossRef | open url image1

Chidlow, J. A. (2007) The biology of wobbegong sharks (Family: Orectolobidae) from south-western Australian waters. PhD, James Cook University.

Chu, Y. T., and Wen, M. C. (1979). ‘Monograph of Fishes of China (No. 2): a Study of the Lateral-line Canals System and that of Lorenzini ampullae and Tubules of Elasmobranchiate Fishes of China.’ (Science and Technology Press: Shanghai.)

Collin, S. P. (2010). Electroreception in vertebrates and invertebrates. In ‘The Encyclopedia of Animal Behaviour’. (Eds M. D. Breed and J. Moore.) pp. 611–620. (Academic Press: Oxford, UK.)

Collin, S. P., and Whitehead, D. (2004). The functional roles of passive electroreception in non-electric fishes. Animal Biology 54, 1–25.
The functional roles of passive electroreception in non-electric fishes.CrossRef | open url image1

Compagno, L. J. V. (1984). FAO species catalogue. Vol. 4. Sharks of the world. An annotated and illustrated catalogue of shark species known to date. FAO Fisheries Synopsis 125(4).

Compagno, L. J. V., Dando, M., and Fowler, S. (2005). ‘Sharks of the World.’ (Princeton University Press: Princeton, NJ.)

Cortés, E. (1999). Standardized diet compositions and trophic levels of sharks. ICES Journal of Marine Science 56, 707.
Standardized diet compositions and trophic levels of sharks.CrossRef | open url image1

Fouts, W. R., and Nelson, D. R. (1999). Prey capture by the pacific angel shark, Squatina californica: Visually mediated strikes and ambush-site characteristics. Copeia , 304–312.
Prey capture by the pacific angel shark, Squatina californica: Visually mediated strikes and ambush-site characteristics.CrossRef | open url image1

Heinicke, M. P., Naylor, G. J. P., and Hedges, S. B. (2009). Cartilaginous fishes (Condrichthyes). In ‘The Timetree of Life’. (Eds S. B. Hedges and S. Kumer.) pp. 320–327. (Oxford University Press: London.)

Himstedt, W., Kopp, J., and Schmidt, W. (1982). Electroreception guides feeding behaviour in amphibians. Naturwissenschaften 69, 552–553.
Electroreception guides feeding behaviour in amphibians.CrossRef | open url image1

Huveneers, C., Otway, N. M., Gibbs, S. E., and Harcourt, R. G. (2007). Quantitative diet assessment of wobbegong sharks (genus Orectolobus) in New South Wales, Australia. ICES Journal of Marine Science: Journal du Conseil 64, 1272–1281. open url image1

Jones, A. A., Hall, N. G., and Potter, I. C. (2010). Species compositions of elasmobranchs caught by three different commercial fishing methods off southwestern Australia, and biological data for four abundant bycatch species. Fishery Bulletin 108, 365–381. open url image1

Jordan, L. K., Kajiura, S. M., and Gordon, M. S. (2009). Functional consequences of structural differences in stingray sensory systems. Part II: electrosensory system. The Journal of Experimental Biology 212, 3044–3050.
Functional consequences of structural differences in stingray sensory systems. Part II: electrosensory system.CrossRef | 19749096PubMed | open url image1

Kajiura, S. M., and Holland, K. N. (2002). Electroreception in juvenile scalloped hammerhead and sandbar sharks. The Journal of Experimental Biology 205, 3609.
| 12409487PubMed | open url image1

Kajiura, S. M., Cornett, A. D., and Yopak, K. E. (2010). Sensory adaptations to the environment: electroreceptors as a case study. In ‘Sharks and their Relatives: Physiological Adaptations, Behavior, Ecology, Conservation, and Management’. (Eds J. C. Carrier, M. R. Heithaus and J. A. Musick.) pp. 393–433. (CRC Press: London.)

Kalmijn, A. J. (1966). Electro-perception in sharks and rays. Nature 212, 1232–1233.
Electro-perception in sharks and rays.CrossRef | open url image1

Kalmijn, A. J. (1974). The detection of electric fields from inanimate and animate sources other than electric organs. In ‘Handbook of Sensory Physiology’. (Ed. A. Fessard.) pp. 147–200. (Springer Verlag: Berlin.)

Kalmijn, A. J. (1978). Electric and magnetic sensory world of sharks, skates, and rays. In ‘Sensory Biology of Sharks, Skates, and Rays’. (Eds E. S. Hodgson and R. F. Mathewson.) pp. 507–528. (Office of Naval Research: Arlington, VA.)

Kempster, R. M., and Collin, S. P. (2011a). Electrosensory pore distribution and feeding in the megamouth shark Megachasma pelagios (Lamniformes: Megachasmidae). Aquatic Biology 11, 225–228.
Electrosensory pore distribution and feeding in the megamouth shark Megachasma pelagios (Lamniformes: Megachasmidae).CrossRef | open url image1

Kempster, R. M., and Collin, S. P. (2011b). Electrosensory pore distribution and feeding in the basking shark Cetorhinus maximus (Lamniformes: Cetorhinidae). Aquatic Biology 12, 33–36.
Electrosensory pore distribution and feeding in the basking shark Cetorhinus maximus (Lamniformes: Cetorhinidae).CrossRef | open url image1

Kempster, R. M., McCarthy, I. D., and Collin, S. P. (2012). Phylogenetic and ecological factors influencing the number and distribution of electroreceptors in elasmobranchs. Journal of Fish Biology 80, 2055–2088.
Phylogenetic and ecological factors influencing the number and distribution of electroreceptors in elasmobranchs.CrossRef | 1:STN:280:DC%2BC38rksVyisg%3D%3D&md5=8d63b5361a796919157dd77e28425798CAS | 22497416PubMed | open url image1

Kempster, R. M., Hart, N. S., and Collin, S. P. (2013a). Survival of the Stillest: Predator Avoidance in Shark Embryos. PLoS ONE 8, e52551.
Survival of the Stillest: Predator Avoidance in Shark Embryos.CrossRef | 1:CAS:528:DC%2BC3sXht1SmtbY%3D&md5=a8a2ba8c0b25d4173dd337134fd2bb94CAS | 23326342PubMed | open url image1

Kempster, R. M., Garza-Gisholt, E., Egeberg, C. A., Hart, N. S., O’Shea, O. R., and Collin, S. P. (2013b). 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, Behavior and Evolution 81, 1–10. open url image1

Last, P. R., and Stevens, J. D. (2009) ‘Sharks and Rays of Australia.’ Second edn. (CSIRO Publishing: Melbourne.)

Marzullo, T. A., Wueringer, B. E., Squire, L., and Collin, S. P. (2011). Description of the mechanoreceptive lateral line and electroreceptive ampullary systems in the freshwater whipray, Himantura dalyensis. Marine and Freshwater Research 62, 771–779.
Description of the mechanoreceptive lateral line and electroreceptive ampullary systems in the freshwater whipray, Himantura dalyensis.CrossRef | 1:CAS:528:DC%2BC3MXnvFanurs%3D&md5=66f4474a3263cf8bf07d2e797a60003eCAS | open url image1

Motta, P. J., and Wilga, C. D. (2001). Advances in the study of feeding behaviors, mechanisms, and mechanics of sharks. Environmental Biology of Fishes 60, 131–156.
Advances in the study of feeding behaviors, mechanisms, and mechanics of sharks.CrossRef | open url image1

Murray, R. W. (1960). Electrical sensitivity of the ampullae of Lorenzini. Nature 187, 957.
Electrical sensitivity of the ampullae of Lorenzini.CrossRef | 1:STN:280:DyaF3c%2Fks1KmtQ%3D%3D&md5=717e2fd6624d71d55817ad0e1d52a44eCAS | 13727039PubMed | open url image1

New, J. G. (1997). The evolution of vertebrate electrosensory systems. Brain, Behavior and Evolution 50, 244–252.
The evolution of vertebrate electrosensory systems.CrossRef | 1:STN:280:DyaK2svlsF2qtA%3D%3D&md5=5bd54ee5dbe0bc83d7072bee8428eb19CAS | 9310199PubMed | open url image1

Parker, G. H., and Van Heusen, A. P. (1917). The reception of mechanical stimuli by the skin, lateral-line organs and ears in fishes, especially in Amiurus. The American Journal of Physiology 44, 463–489. open url image1

Paulin, M. G. (1995). Electroreception and the compass sense of sharks. Journal of Theoretical Biology 174, 325–339.
Electroreception and the compass sense of sharks.CrossRef | open url image1

Pittenger, G. G. (1984). Movements, distribution, feeding, and growth of the Pacific angel shark, Squatina californica, at Catalina Island, California. M.Sc., University of California.

Raschi, W. (1986). A morphological analysis of the ampullae of Lorenzini in selected skates (Pisces, Rajoidei). Journal of Morphology 189, 225–247. open url image1

Rivera-Vicente, A. C., Sewell, J., and Tricas, T. C. (2011). Electrosensitive Spatial Vectors in Elasmobranch Fishes: Implications for Source Localization. PLoS ONE 6, e16008.
Electrosensitive Spatial Vectors in Elasmobranch Fishes: Implications for Source Localization.CrossRef | 1:CAS:528:DC%2BC3MXhtFWnsL8%3D&md5=b1d3398c35d4aedb71569e49940c9082CAS | 21249147PubMed | open url image1

Scheich, H., Langner, G., Tidemann, C., Coles, R. B., and Guppy, A. (1986). Electroreception and electrolocation in platypus. Nature 319, 401–402.
Electroreception and electrolocation in platypus.CrossRef | 1:STN:280:DyaL287hvVKksQ%3D%3D&md5=bfbc059bfc01aa0a0c1abd63d16cb046CAS | 3945317PubMed | open url image1

Sisneros, J. A., Tricas, T. C., and Luer, C. A. (1998). Response properties and biological function of the skate electrosensory system during ontogeny. Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology 183, 87–99.
Response properties and biological function of the skate electrosensory system during ontogeny.CrossRef | 1:STN:280:DyaK1czls1Gisg%3D%3D&md5=797a87879878f116f550043732b1af4fCAS | open url image1

Theiss, S., Collin, S., and Hart, N. (2010). Interspecific visual adaptations among wobbegong sharks (Orectolobidae). Brain, Behavior and Evolution 76, 248–260.
Interspecific visual adaptations among wobbegong sharks (Orectolobidae).CrossRef | 21051877PubMed | open url image1

Theiss, S., Hart, N. S., and Collin, S. P. (2011). Morphology and distribution of the ampullary electroreceptors in wobbegong sharks: implications for feeding behaviour. Marine Biology 158, 723–735.
Morphology and distribution of the ampullary electroreceptors in wobbegong sharks: implications for feeding behaviour.CrossRef | open url image1

Tricas, T. C. (2001). The neuroecology of the elasmobranch electrosensory world: why peripheral morphology shapes behavior. Environmental Biology of Fishes 60, 77–92.
The neuroecology of the elasmobranch electrosensory world: why peripheral morphology shapes behavior.CrossRef | open url image1

Tricas, T. C., Michael, S. W., and Sisneros, J. A. (1995). Electrosensory optimization to conspecific phasic signals for mating. Neuroscience Letters 202, 129–132.
Electrosensory optimization to conspecific phasic signals for mating.CrossRef | 1:CAS:528:DyaK28Xls1KltA%3D%3D&md5=3953b5895aee3887cae3d6da02d7894dCAS | 8787848PubMed | open url image1

Winther-Janson, M., Wueringer, B. E., and Seymour, J. E. (2012). Electroreceptive and mechanoreceptive anatomical specialisations in the epaulette shark (Hemiscyllium ocellatum). PLoS ONE 7, e49857.
Electroreceptive and mechanoreceptive anatomical specialisations in the epaulette shark (Hemiscyllium ocellatum).CrossRef | 1:CAS:528:DC%2BC38XhvVKqsbbO&md5=56ac7aa39e4b57d7ba7cbbbb0d28ae2bCAS | 23226226PubMed | open url image1

Wueringer, B. E., and Tibbetts, I. R. (2008). Comparison of the lateral line and ampullary systems of two species of shovelnose ray. Reviews in Fish Biology and Fisheries 18, 47–64.
Comparison of the lateral line and ampullary systems of two species of shovelnose ray.CrossRef | open url image1



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