Electroreception in the obligate freshwater stingray, Potamotrygon motoro
Lindsay L. Harris A , Christine N. Bedore B and Stephen M. Kajiura A CA Department of Biological Sciences, Florida Atlantic University, 777 Glades Road, Boca Raton, FL 33431, USA.
B Biology Department, Duke University, Durham, NC 27708, USA.
C Corresponding author. Email: kajiura@fau.edu
Marine and Freshwater Research 66(11) 1027-1036 https://doi.org/10.1071/MF14354
Submitted: 9 November 2014 Accepted: 17 January 2015 Published: 9 April 2015
Abstract
Elasmobranch fishes use electroreception to detect electric fields in the environment, particularly minute bioelectric fields of potential prey. A single family of obligate freshwater stingrays, Potamotrygonidae, endemic to the Amazon River, demonstrates morphological adaptations of their electrosensory system due to characteristics of a high impedance freshwater environment. Little work has investigated whether the reduced morphology translates to reduced sensitivity because of the electrical properties of freshwater, or because of a marine-tuned sensory system attempting to function in freshwater. The objective of the present study was to measure electric potential from prey of Potamotrygon motoro and replicate the measurements in a behavioural assay to quantify P. motoro electrosensitivity. Median orientation distance to prey-simulating electric fields was 2.73 cm, and the median voltage gradient detected was 0.20 mV cm–1. This sensitivity is greatly reduced compared with marine batoids. A euryhaline species with marine-type ampullary morphology was previously tested in freshwater and demonstrated reduced sensitivity compared with when it was tested in seawater (0.2 μV cm–1 v. 0.6 nV cm–1). When the data were adjusted with a modified ideal dipole equation, sensitivity was comparable to P. motoro. This suggests that the conductivity of the medium, more so than ampullary morphology, dictates the sensitivity of elasmobranch electroreception.
Additional keywords: batoid, bioelectric fields, conductivity, passive electrosense.
References
Almeida, M. P., Lins, P. M. O., Charvet-Almeida, P., and Barthem, R. B. (2010). Diet of the freshwater stingray Potamotrygon motoro (Chondrichthyes: Potamotrygonidae) on Marajó Island (Pará, Brazil). Brazilian Journal of Biology 70, 155–162.| Diet of the freshwater stingray Potamotrygon motoro (Chondrichthyes: Potamotrygonidae) on Marajó Island (Pará, Brazil).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3c7osF2lug%3D%3D&md5=a2cc443ad8d900bc166fc586b00a10b0CAS |
Ballantyne, J. S., and Robinson, J. W. (2010). Freshwater elasmobranchs: a review of their physiology and biochemistry. Journal of Comparative Physiology. B. Biochemical, Systemic, and Environmental Physiology 180, 475–493.
| Freshwater elasmobranchs: a review of their physiology and biochemistry.Crossref | GoogleScholarGoogle Scholar |
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 | GoogleScholarGoogle Scholar | 23629880PubMed |
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 | GoogleScholarGoogle Scholar | 24290363PubMed |
Foskett, J. K., Bern, H. A., Machen, T. E., and Conner, M. (1983). Chloride cells and the hormonal regulation of teleost fish osmoregulation. The Journal of Experimental Biology 106, 255–281.
| 1:CAS:528:DyaL2cXhsFCitrw%3D&md5=b9494ffc1a212f99cce0e960d4e571f8CAS | 6361207PubMed |
Garrone-Neto, D., and Sazima, I. (2009). Stirring, charging, and picking: hunting tactics of potamotrygonid rays in the upper Paraná River. Neotropical Ichthyology 7, 113–116.
| Stirring, charging, and picking: hunting tactics of potamotrygonid rays in the upper Paraná River.Crossref | GoogleScholarGoogle Scholar |
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 | GoogleScholarGoogle Scholar |
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 | GoogleScholarGoogle Scholar | 19749096PubMed |
Kajiura, S. M. (2003). Electroreception in neonatal bonnethead sharks, Sphyrna tiburo. Marine Biology 143, 603–611.
Kajiura, S. M., and Fitzgerald, T. P. (2009). Response of juvenile scalloped hammerhead sharks to electric stimuli. Zoology (Jena, Germany) 112, 241–250.
| Response of juvenile scalloped hammerhead sharks to electric stimuli.Crossref | GoogleScholarGoogle Scholar |
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 |
Kalmijn, A. J. (1972). Bioelectric fields in sea water and the function of the ampullae of Lorenzini in elasmobranch fishes. In ‘SIO Oceanography’. (Ed. SIO Reference 72–83.) pp. 1–21. (Scripps Institution of Oceanography, University of California: 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, Vol. 3’. (Ed. A. Fessard.) pp. 147–200. (Springer-Verlag: New York.)
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 | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3s%2FktFeitw%3D%3D&md5=8b7f4d134018bb967a0b1cad7509fec2CAS | 7134985PubMed |
Kalmijn, A. J. (1988). Detection of weak electric fields. In ‘Sensory Biology of Aquatic Animals’. (Eds J. Atema, R. R. Fay, A. N. Popper and W. N. Tavolga.) pp. 151–186. (Springer-Verlag: New York.)
Lovejoy, N. R., Albert, J. S., and Crampton, W. G. R. (2006). Miocene marine incursions and marine/freshwater transitions: evidence from Neotropical fishes. Journal of South American Earth Sciences 21, 5–13.
| Miocene marine incursions and marine/freshwater transitions: evidence from Neotropical fishes.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 |
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=c9eaabb5478d3fe339e4b44226acfce7CAS | 19411548PubMed |
Peters, R. C., and Bretschneider, F. (1972). Electric phemonena in the habitat of the catfish Ictalurus nebulosus. Journal of Comparative Physiology 81, 345–362.
| Electric phemonena in the habitat of the catfish Ictalurus nebulosus.Crossref | GoogleScholarGoogle Scholar |
Robertson, J. D. (1953). Further studies on ionic regulation in marine invertebrates. The Journal of Experimental Biology 30, 277–296.
| 1:CAS:528:DyaG2cXlsVSkug%3D%3D&md5=b9a342979c21f015af0e96173cc0cb27CAS |
Shibuya, A., Zuanon, J., de Araújo, M. L. G., and Tanaka, S. (2010). Morphology of lateral line canals in Neotropical freshwater stingrays (Chondrichthyes: Potamotrygonidae) from Negro River, Brazilian Amazon. Neotropical Ichthyology 8, 867–876.
| Morphology of lateral line canals in Neotropical freshwater stingrays (Chondrichthyes: Potamotrygonidae) from Negro River, Brazilian Amazon.Crossref | GoogleScholarGoogle Scholar |
Stein, B. E., and Meredith, M. A. (1993). ‘The Merging of the Senses.’ (Ed M. S. Gazzaniga.) (The MIT Press: Cambridge, MA.)
Szabo, T., Kalmijn, A. J., Enger, P. S., and Bullock, T. H. (1972). Microampullary organs and a submandibular sense organ in the fresh water ray, Potamotrygon. Journal of Comparative Physiology 79, 15–27.
| Microampullary organs and a submandibular sense organ in the fresh water ray, Potamotrygon.Crossref | GoogleScholarGoogle Scholar |
Szamier, R. B., and Bennett, M. L. V. (1980). Ampullary electroreceptors in the fresh water ray, Potamotrygon. Journal of Comparative Physiology. A. Neuroethology, Sensory, Neural, and Behavioral Physiology 138, 225–230.
| Ampullary electroreceptors in the fresh water ray, Potamotrygon.Crossref | GoogleScholarGoogle Scholar |
Taylor, N. G., Manger, P. R., Pettigrew, J. D., and Hall, L. S. (1992). Electromyogenic potentials of a variety of platypus prey items: an amplitude and frequency analysis. In ‘Platypus and Echindas’. (Ed. M. L. Augee.) pp. 216–224. (The Royal Zoological Society of NSW: Sydney.)
Tricas, T. C., and New, J. G. (1997). Sensitivity and response dynamics of elasmobranch electrosensory primary afferent neurons to near threshold fields. Journal of Comparative Physiology. A. Neuroethology, Sensory, Neural, and Behavioral Physiology 182, 89–101.
| Sensitivity and response dynamics of elasmobranch electrosensory primary afferent neurons to near threshold fields.Crossref | GoogleScholarGoogle Scholar |
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 | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xls1KltA%3D%3D&md5=2f7ec5a2323e4d6d144f374eeaa11baaCAS | 8787848PubMed |
Wood, C. M., Matsuo, A. Y. O., Gonzalez, R. J., Wilson, R. W., Patrick, M. L., and Val, A. L. (2002). Mechanisms of ion transport in Potamotrygon, a stenohaline freshwater elasmobranch native to the ion-poor blackwaters of the Rio Negro. The Journal of Experimental Biology 205, 3039–3054.
| 1:CAS:528:DC%2BD38XovVWhtbs%3D&md5=b687b5187f6b12356812544a0f2d4a03CAS | 12200407PubMed |
Wueringer, B. E., Squire, L. J., 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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFanu7nI&md5=0d1ce02b57954e8288a1b3fc04ad8f93CAS | 22848543PubMed |