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

Electrosensory-driven feeding behaviours of the Port Jackson shark (Heterodontus portusjacksoni) and western shovelnose ray (Aptychotrema vincentiana)

R. M. Kempster A B , C. A. Egeberg A , N. S. Hart A and S. P. Collin A

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

B Corresponding author. Email: ryankempster@supportoursharks.com

Marine and Freshwater Research 67(2) 187-194 http://dx.doi.org/10.1071/MF14245
Submitted: 18 August 2014  Accepted: 16 January 2015   Published: 22 May 2015

Abstract

Elasmobranch fishes (sharks, skates and rays) possess a highly sensitive electrosensory system that enables them to detect weak electric fields, such as those produced by potential prey organisms. Despite several comparative anatomical studies, the functional significance of interspecific variation in electrosensory system morphology remains poorly understood. In the present study, we directly tested the electrosensitivity of two benthic elasmobranchs that share a similar habitat and feed on similarly sized prey items (Port Jackson sharks, Heterodontus portusjacksoni, and western shovelnose rays, Aptychotrema vincentiana), but differ significantly in their electrosensory system morphology. Aptychotrema vincentiana possesses almost five times the number of electrosensory pores of H. portusjacksoni (~1190 and ~239 respectively), yet both species are able to initiate feeding responses to electric-field gradients below 1 nV cm–1, similar to other elasmobranch species tested. However, A. vincentiana showed a greater ability to resolve the specific location of electrosensory stimuli, because H. portusjacksoni would more often overshoot the target and have to turn around to locate it. These results suggested that differences in abundance and distribution of electrosensory pores have little to no effect on the absolute electrical sensitivity in elasmobranchs, and instead, may reflect species-specific differences in the spatial resolution and directionality of electroreception.

Additional keywords: ampullae of Lorenzini, benthic, elasmobranch, electroreception, resolution, sensitivity, sensory biology.


References

Bedore, C. N., and Kajiura, S. M. (2013). Bioelectric fields of marine organisms: voltage and frequency contributions to detectability by electroreceptive predators. Physiological and Biochemical Zoology 86, 298–311.
Bioelectric fields of marine organisms: voltage and frequency contributions to detectability by electroreceptive predators.CrossRef | 23629880PubMed | open url image1

Bedore, C. N., Harris, L. L., and Kajiura, S. M. (2014). Behavioral responses of batoid elasmobranchs to prey-simulating electric fields are correlated to peripheral sensory morphology and ecology. Zoology 117, 95–103.
Behavioral responses of batoid elasmobranchs to prey-simulating electric fields are correlated to peripheral sensory morphology and ecology.CrossRef | 24290363PubMed | 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 116, 270–276.
A comparison of the electrosensory morphology of a euryhaline and a marine stingray.CrossRef | 23988133PubMed | open url image1

Egeberg, C. A., Kempster, R. M., Theiss, S. M., Hart, N. S., and Collin, S. P. (2014). 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. Marine and Freshwater Research 65, 1003–1008.
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.CrossRef | open url image1

Gardiner, J. M., Atema, J., Hueter, R. E., and Motta, P. J. (2014). Multisensory integration and behavioral plasticity in sharks from different ecological niches. PLOS ONE 9, e93036.
Multisensory integration and behavioral plasticity in sharks from different ecological niches.CrossRef | 24695492PubMed | open url image1

Haine, O. S., Ridd, P. V., and Rowe, R. J. (2001). Range of electrosensory detection of prey by Carcharhinus melanopterus and Himantura granulata. Marine and Freshwater Research 52, 291–296.
Range of electrosensory detection of prey by Carcharhinus melanopterus and Himantura granulata.CrossRef | 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. (2001). Head morphology and electrosensory pore distribution of carcharhinid and sphyrnid sharks. Environmental Biology of Fishes 61, 125–133.
Head morphology and electrosensory pore distribution of carcharhinid and sphyrnid sharks.CrossRef | open url image1

Kajiura, S. M. (2003). Electroreception in neonatal bonnethead sharks, Sphyrna tiburo. Marine Biology 143, 603–611.
Electroreception in neonatal bonnethead sharks, Sphyrna tiburo.CrossRef | open url image1

Kajiura, S. M., and Fitzgerald, T. P. (2009). Response of juvenile scalloped hammerhead sharks to electric stimuli. Zoology 112, 241–250.
Response of juvenile scalloped hammerhead sharks to electric stimuli.CrossRef | 19097876PubMed | 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, 3609–3621.
| 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. JC Carrier, MR Heithaus and JA 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. (1971). The electric sense of sharks and rays. The Journal of Experimental Biology 55, 371–383.
| 1:STN:280:DyaE38%2FislGrug%3D%3D&md5=15700a5acc2c05992bd6a8b6ebedb21dCAS | 5114029PubMed | open url image1

Kalmijn, A. J. (1972). ‘Bioelectric Fields in Sea Water and the Function of the Ampullae of Lorenzini in Elasmobranch Fishes. SIO Reference.’ (Scripps Institution of Oceanography, UC: San Diego, CA.)

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: Washington, DC.)

Kalmijn, A. J. (1982). Electric and magnetic field detection in elasmobranch fishes. Science 218, 916–918.
Electric and magnetic field detection in elasmobranch fishes.CrossRef | 1:STN:280:DyaL3s%2FktFeitw%3D%3D&md5=8b7f4d134018bb967a0b1cad7509fec2CAS | 7134985PubMed | open url image1

Kempster, R. M. (2014). The role of electroreception in elasmobranchs. Ph.D. Thesis, The University of Western Australia, Perth, WA.

Kempster, R. M., and Collin, S. P. (2011a). 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., and Collin, S. P. (2011b). 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., 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=dd19fd0fda3eaf0b3d41e13485a64579CAS | 22497416PubMed | open url image1

Kempster, R. M., Garza-Gisholt, E., Egeberg, C. A., Hart, N. S., O’Shea, O. R., and Collin, S. P. (2013a). 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

Kempster, R. M., Hart, N. S., and Collin, S. P. (2013b). 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=f24244ddd8f9342c87ee42aeafede4f1CAS | 23326342PubMed | open url image1

Maxwell, J. C. (1865). A dynamical theory of the electromagnetic field. Philosophical Transactions of the Royal Society of London 155, 459–512.
A dynamical theory of the electromagnetic field.CrossRef | open url image1

McComb, D. M., and Kajiura, S. M. (2008). Visual fields of four batoid fishes: a comparative study. The Journal of Experimental Biology 211, 482–490.
Visual fields of four batoid fishes: a comparative study.CrossRef | 18245624PubMed | open url image1

McGowan, D. W., and Kajiura, S. M. (2009). Electroreception in the euryhaline stingray, Dasyatis sabina. The Journal of Experimental Biology 212, 1544–1552.
Electroreception in the euryhaline stingray, Dasyatis sabina.CrossRef | 1:STN:280:DC%2BD1MzhvVahtw%3D%3D&md5=c9eaabb5478d3fe339e4b44226acfce7CAS | 19411548PubMed | open url image1

O’Shea, O. R., Thums, M., van Keulen, M., Kempster, R. M., and Meekan, M. G. (2013). Dietary partitioning by five sympatric species of stingray (Dasyatidae) on coral reefs. Journal of Fish Biology 82, 1805–1820.
Dietary partitioning by five sympatric species of stingray (Dasyatidae) on coral reefs.CrossRef | 1:STN:280:DC%2BC3snptlGqtw%3D%3D&md5=a1a51f19c5f19f77f246b5c557f14ae7CAS | 23731138PubMed | open url image1

Raschi, W. (1984). Anatomical observations on the ampullae of Lorenzini from selected skates and galeoid sharks of the western North Atlantic. Ph.D. Thesis, College of William and Mary, Williamsburg, VA, USA.

Raschi, W. (1986). A morphological analysis of the ampullae of Lorenzini in selected skates (Pisces, Rajoidei). Journal of Morphology 189, 225–247.
A morphological analysis of the ampullae of Lorenzini in selected skates (Pisces, Rajoidei).CrossRef | 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=d8d5bd7e0adc25dddf5bab6242e19767CAS | 21249147PubMed | 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=d0a97aa713eea59233bac77b934b6307CAS | open url image1

Sommerville, E., Platell, M. E., White, W. T., Jones, A. A., and Potter, I. C. (2011). Partitioning of food resources by four abundant, co-occurring elasmobranch species: relationships between diet and both body size and season. Marine and Freshwater Research 62, 54–65.
Partitioning of food resources by four abundant, co-occurring elasmobranch species: relationships between diet and both body size and season.CrossRef | open url image1

Tricas, T. C. (1982). Bioelectric-mediated predation by swell sharks, Cephaloscyllium ventriosum. Copeia , 948–952.
Bioelectric-mediated predation by swell sharks, Cephaloscyllium ventriosum.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=2f7ec5a2323e4d6d144f374eeaa11baaCAS | 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=d7b65004f3a028a43a943b8dc5344954CAS | 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

Wueringer, B. E., Squire, L., Kajiura, S. M., Tibbetts, I. R., Hart, N. S., and Collin, S. P. (2012). Electric field detection in sawfish and shovelnose rays. PLoS One 7, e41605.
Electric field detection in sawfish and shovelnose rays.CrossRef | 1:CAS:528:DC%2BC38XhtFanu7nI&md5=0d1ce02b57954e8288a1b3fc04ad8f93CAS | 22848543PubMed | open url image1



Rent Article Export Citation Cited By (2)