Description of the mechanoreceptive lateral line and electroreceptive ampullary systems in the freshwater whipray, Himantura dalyensis
Teagan A. Marzullo A D , Barbara E. Wueringer A , Lyle Squire Jnr B and Shaun P. Collin A C
+ Author Affiliations
- Author Affiliations
A Sensory Neurobiology Group, School of Biomedical Sciences, The University of Queensland, Brisbane, Qld 4072, Australia.
B Cairns Marine, Stratford, Qld 4870, Australia.
C School of Animal Biology and the UWA Oceans Institute, The University of Western Australia, Crawley, WA 6009, Australia.
D Corresponding author. Email: teagan.marzullo@uqconnect.edu.au
Marine and Freshwater Research 62(6) 771-779 https://doi.org/10.1071/MF10156
Submitted: 18 June 2010 Accepted: 17 January 2011 Published: 24 June 2011
Journal Compilation © CSIRO Publishing 2011 Open Access CC BY-NC-ND
Abstract
Mechanoreceptive and electroreceptive anatomical specialisations in freshwater elasmobranch fishes are largely unknown. The freshwater whipray, Himantura dalyensis, is one of a few Australian elasmobranch species that occur in low salinity (oligohaline) environments. The distribution and morphology of the mechanoreceptive lateral line and the electroreceptive ampullae of Lorenzini were investigated by dissection and compared with previous studies on related species. The distribution of the pit organs resembles that of a marine ray, Dasyatis sabina, although their orientation differs. The lateral line canals of H. dalyensis are distributed similarly compared with two marine relatives, H. gerrardi and D. sabina. However, convolutions of the ventral canals and proliferations of the infraorbital canal are more extensive in H. dalyensis than H. gerrardi. The intricate nature of the ventral, non-pored canals suggests a mechanotactile function, as previously demonstrated in D. sabina. The ampullary system of H. dalyensis is not typical of an obligate freshwater elasmobranch (i.e. H. signifer), and its morphology and pore distribution resembles those of marine dasyatids. These results suggest that H. dalyensis is euryhaline, with sensory systems adapted similarly to those described in marine and estuarine species.
Additional keywords: ampullae of Lorenzini, Himantura polylepis, mechanosensory lateral line, pit organs.
References
Andres, K. H., and von Düring, M. (1988). Comparative anatomy of vertebrate electroreceptors. Progress in Brain Research 74, 113–131.| Comparative anatomy of vertebrate electroreceptors.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1M%2Fkt1ylsQ%3D%3D&md5=14e5484c396378b150d48c5ba8db647eCAS | 3055044PubMed |
Ashley, L. M., and Chiasson, R. B. (1988). ‘Laboratory Anatomy of the Shark.’ (Brown and Benchmark: New York, NY.)
Bleeker, P. (1852). Bijdrage tot de kennis der Plagiostomen van den Indischen Archipel. Bataviaasch Genootschap der Kunsten en Wetenschappen 24, 1–92.
Bodznick, D., and Montgomery, J. C. (2005). The physiology of low frequency electrosensory systems. In ‘Electroreception’. (Eds T. H. Bullock, C. D. Hopkins, A. N. Popper and R. R. Fay.) pp. 132–153. (Springer: New York, NY.)
Chu, Y. T., and Wen, M. C. (1979). ‘A Study of the Lateral – Line Canal System and that of the Lorenzini Ampullae and Tubules of Elasmobranchiate Fishes of China: Monograph of Fishes of China.’ (Academic Press: Shanghai.)
Coombs, S. (1994). Nearfield detection of dipole sources by the goldfish (Carassius auratus) and the mottled sculpin (Cottus bairdi). The Journal of Experimental Biology 190, 109–129.
| 1:STN:280:DyaK2M%2FltlKgsw%3D%3D&md5=3eb06481455588f189f3262ddbad7de3CAS | 7964388PubMed |
Dijkgraaf, S. (1963). Functioning and significance of lateral-line organs. Biological Reviews of the Cambridge Philosophical Society 38, 51–105.
| Functioning and significance of lateral-line organs.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF383hvFynuw%3D%3D&md5=749fa1dc4e7d6b2a084c3b66fd34f96eCAS | 14027866PubMed |
Herbert, B., and Peeters, J. (1995). ‘Freshwater Fishes of Far North Queensland.’ (Department of Primary Industries: Brisbane.)
Jordan, L. K. (2008). Comparative morphology of stingray lateral line canal and electrosensory systems. Journal of Morphology 269, 1325–1339.
| Comparative morphology of stingray lateral line canal and electrosensory systems.Crossref | GoogleScholarGoogle Scholar | 18655157PubMed |
Kajiura, S. M. (2003). Electroreception in neonatal bonnethead sharks, Sphyrna tiburo. Marine Biology 143, 603–611.
| Electroreception in neonatal bonnethead sharks, Sphyrna tiburo.Crossref | GoogleScholarGoogle Scholar |
Kalmijn, A. J. (1971). Electric sense of sharks and rays. The Journal of Experimental Biology 55, 371–383.
| 1:STN:280:DyaE38%2FislGrug%3D%3D&md5=0500a54cee429a86ffada2d24e974d61CAS | 5114029PubMed |
Kalmijn, A. J. (1974). The detection of electric fields from inanimate and animate sources other than electric organs. In ‘Electroreceptors and Other Specialized Receptors in Lower Vertebrates’. (Eds T. H. Bullock, A. Fessard and R. H. Hartline.) pp. 147–200. (Springer-Verlag: Berlin.)
Last, P. R., and Manjaji-Matsumoto, B. M. (2008). Himantura dalyensis sp. nov., a new estuarine whipray (Myliobatoidei: Dasyatidae) from northern Australia. In ‘Descriptions of New Australian Chondrichthyans’. (Eds P. R. Last, W. T. White and J. J. Pogonoski.) pp. 283–291. (CSIRO Marine and Atmospheric Research: Canberra.)
Last, P. R., and Stevens, J. D. (2009). ‘Sharks and Rays of Australia.’ 2nd edn. (CSIRO Publishing: Melbourne.)
Last, P. R., White, W. T., and Pogonoski, J. J. (2008). ‘Descriptions of New Australia Chondrichthyans.’ (CSIRO Marine and Atmospheric Research: Hobart.)
Martin, L. K., and Cailliet, G. M. (1988). Aspects of the reproduction of the bat ray, Myliobatis californica, in Central California. Copeia 3, 754–762.
| Aspects of the reproduction of the bat ray, Myliobatis californica, in Central California.Crossref | GoogleScholarGoogle Scholar |
Maruska, K. P. (2001). Morphology of the mechanosensory lateral line system in elasmobranch fishes: ecological and behavioral considerations. Environmental Biology of Fishes 60, 47–75.
| Morphology of the mechanosensory lateral line system in elasmobranch fishes: ecological and behavioral considerations.Crossref | GoogleScholarGoogle Scholar |
Maruska, K. P., and Tricas, T. C. (1998). Morphology of the mechanosensory lateral line system in the Atlantic stingray, Dasyatis sabina: the mechanotactile hypothesis. Journal of Morphology 238, 1–22.
| Morphology of the mechanosensory lateral line system in the Atlantic stingray, Dasyatis sabina: the mechanotactile hypothesis.Crossref | GoogleScholarGoogle Scholar |
Maruska, K. R., and Tricas, T. C. (2004). Test of the mechanotactile hypothesis: neuromast morphology and response dynamics of mechanosensory lateral line primary afferents in the stingray. The Journal of Experimental Biology 207, 3463–3476.
| Test of the mechanotactile hypothesis: neuromast morphology and response dynamics of mechanosensory lateral line primary afferents in the stingray.Crossref | GoogleScholarGoogle Scholar | 15339942PubMed |
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 | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1MzhvVahtw%3D%3D&md5=23dbb435a93562112e622108f70d17ecCAS | 19411548PubMed |
Merrick, J. R., and Schmida, G. E. (1984). ‘Australian Freshwater Fishes: Biology and Management.’ (J. R. Merrick: Sydney.)
Murray, R. W. (1974). The ampullae of Lorenzini. In ‘Electroreceptors and Other Specialized Receptors in Lower Vertebrates’. (Eds T. H. Bullock, A. Fessard and R. H. Hartline.) pp. 125–146. (Springer-Verlag: Berlin.)
Nickel, E., and Fuchs, S. (1974). Organization and ultrastructure of mechanoreceptors (Savi vesicles) in the elasmobranch Torpedo. Journal of Neurocytology 3, 161–177.
| Organization and ultrastructure of mechanoreceptors (Savi vesicles) in the elasmobranch Torpedo.Crossref | GoogleScholarGoogle Scholar |
Peach, M. B. (2001). The dorso-lateral pit organs of the Port Jackson shark contribute sensory information for rheotaxis. Journal of Fish Biology 59, 696–704.
| The dorso-lateral pit organs of the Port Jackson shark contribute sensory information for rheotaxis.Crossref | GoogleScholarGoogle Scholar |
Peach, M. B. (2003). Inter- and intraspecific variation in the distribution and number of pit organs (free neuromasts) of sharks and rays. Journal of Morphology 256, 89–102.
| Inter- and intraspecific variation in the distribution and number of pit organs (free neuromasts) of sharks and rays.Crossref | GoogleScholarGoogle Scholar | 12616576PubMed |
Puzdrowski, R. L., and Leonard, R. B. (1993). The octavolateral systems in the stingray, Dasyatis sabina. 1. Primary projections of the octaval and lateral line nerves. The Journal of Comparative Neurology 332, 21–37.
| The octavolateral systems in the stingray, Dasyatis sabina. 1. Primary projections of the octaval and lateral line nerves.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3s3psVSltg%3D%3D&md5=745d3977b795fb47073b05f3c45fb37aCAS | 8514920PubMed |
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 | GoogleScholarGoogle Scholar |
Raschi, W., Keithan, E. D., and Rhee, W. C. H. (1997). Anatomy of the ampullary electroreceptor in the freshwater stingray, Himantura signifer. Copeia 1, 101–107.
| Anatomy of the ampullary electroreceptor in the freshwater stingray, Himantura signifer.Crossref | GoogleScholarGoogle Scholar |
Szabo, T., Enger, P. S., Kalmijn, A. J., and Bullock, T. H. (1972). Microampullary organs and a submandibular sense organ in a fresh water ray, Potamotrygon. Journal of Comparative Physiology 79, 15–27.
| Microampullary organs and a submandibular sense organ in a fresh water ray, Potamotrygon.Crossref | GoogleScholarGoogle Scholar |
Tam, W. L., Wong, W. P., Loong, A. M., Hiong, K. C., Chew, S. F., et al. (2003). The osmotic response of the Asian freshwater stingray (Himantura signifer) to increased salinity: a comparison with marine (Taeniura lymma) and Amazonian freshwater (Potamotrygon motoro) stingrays. The Journal of Experimental Biology 206, 2931–2940.
| The osmotic response of the Asian freshwater stingray (Himantura signifer) to increased salinity: a comparison with marine (Taeniura lymma) and Amazonian freshwater (Potamotrygon motoro) stingrays.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnslKnsbc%3D&md5=3e156207c55f5b292e2d0771424399c5CAS | 12878662PubMed |
Tester, A. L., and Nelson, G. J. (1967). Free neuromasts (pit organs) in sharks. In ‘Sharks, Skates and Rays’. (Eds P. W. Gilbert, R. F. Matthewson and D. P. Rall.) pp. 503–531. (Johns Hopkins Press: Baltimore, MD.)
Thorburn, D. C., Morgan, D. L., Rowland, A. J., and Gill, H. (2004). Elasmobranchs of the Fitzroy River, Western Australia. Report to the Natural Heritage Trust, Department of Agriculture, Fisheries and Forestry, Canberra.
Whitehead, D. L. (2002). Ampullary organs and electroreception in freshwater Carcharhinus leucas. Journal of Physiology, Paris 96, 391–395.
| Ampullary organs and electroreception in freshwater Carcharhinus leucas.Crossref | GoogleScholarGoogle Scholar | 14692487PubMed |
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 | GoogleScholarGoogle Scholar |
