Skip to main content
SpringerLink
Log in

The yellow stingray (Urobatis jamaicensis) can discriminate the geomagnetic cues necessary for a bicoordinate magnetic map

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Elasmobranch fishes (sharks, skates, and rays) are hypothesized to use environmental cues, such as the geomagnetic field (GMF), to navigate across the ocean. However, testing the sensory and navigation abilities of large highly migratory fishes in the field is challenging. This laboratory study tested whether the yellow stingray, Urobatis jamaicensis, could detect and distinguish between the GMF cues used by other magnetically sensitive species to actively determine their location. Stingrays were divided into two cohorts for initial behavioral conditioning: one was trained to associate a change in GMF intensity with an aversive stimulus, whereas the other was trained using a change in GMF inclination angle. Individuals from each cohort remained naïve to the GMF conditioning stimulus used to condition the other cohort. The combined group learned the initial association within a mean (± SE) of 184.0 ± 34.8 trials. Next, stingrays from each cohort were randomly exposed to their original GMF conditioning stimulus and the novel GMF stimulus. The original magnetic stimulus continued to be reinforced, whereas the novel stimulus was not. The group demonstrated a significantly different response to the original (reinforced) and novel (non-reinforced) stimuli, which indicates that stingrays could distinguish between the intensity and inclination angle of a magnetic field. This experiment is the first to show that a batoid (skate or ray) can detect and distinguish between changes in GMF intensity and inclination angle, and supports the idea that elasmobranchs might use GMF cues to form a magnetically based cognitive map and derive a sense of location.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

The datasets created during and/or analyzed during the current study are available from the corresponding author upon reasonable request.

References

  • Able KP (1991) Common themes and variations in animal orientation systems. Am Zool 31:157–167

    Google Scholar 

  • Able K (2001) The concepts and terminology of bird navigation. J Avian Biol 32:174–183

    Google Scholar 

  • Adrianov GN, Brown HR, Ilyinsky OB (1974) Responses of central neurons to electrical and magnetic stimuli of the ampullae of Lorenzini in the Black Sea skate. J Comp Physiol 93:287–299

    Google Scholar 

  • Akoev GN, Ilyinsky OB, Zadan PM (1976) Responses of electroreceptors (ampullae of Lorenzini) of skates to electric and magnetic fields. J Comp Physiol 106:127–136

    Google Scholar 

  • Anderson JM, Clegg TM, Véras LVMV, Holland KH (2017) Insight into shark magnetic field perception from empirical observations. Sci Rep 7:1042. https://doi.org/10.1038/s41598-017-11459-8

    Article  CAS  Google Scholar 

  • Beason RC, Semm P (1987) Magnetic responses of the trigeminal nerve system of the bobolink (Dolichonyx oryzivorus). Neurosci Lett 80:229–234

    CAS  PubMed  Google Scholar 

  • Bedore CB, Harris LL, Kajiura SM (2014) Behavioral responses of batoid elasmobranchs to prey-simulating electric fields are correlated to peripheral sensory morphology and ecology. Zoology 117:95–103

    PubMed  Google Scholar 

  • Berdahl A, Westley PAH, Levin SA, Couzin ID, Quinn TP (2016) A collective navigation hypothesis for homeward migration in anadromous salmonids. Fish Fish 17:525–542

    Google Scholar 

  • Bingman VP, Cheng K (2005) Mechanisms of animal global navigation: comparative perspectives and enduring challenges. Ethol Ecol Evol 17:295–318

    Google Scholar 

  • Boström JE, Åkesson S, Alerstam T (2012) Where on earth can animals use a geomagnetic bi-coordinate map for navigation? Ecography 35:1039–1047

    Google Scholar 

  • Brown HR, Ilyinsky OB (1978) The ampullae of Lorenzini in the magnetic field. J Comp Physiol 126:333–341

    Google Scholar 

  • Brown HR, Ilyinsky OB, Muraveiko VM, Corshkov ES, Fonarev GA (1979) Evidence that geomagnetic variations can be detected by lorenzinian ampullae. Nature 277:649–650

    CAS  PubMed  Google Scholar 

  • Chapman DD, Feldheim KA, Papastamatiou YP, Hueter RE (2015) There and back again: a review of residency and return migrations in sharks, with implications for population structure and management. Annu Rev Mar Sci 7:547–570

    Google Scholar 

  • Clark E (1959) Instrumental conditioning of lemon sharks. Science 130:217–218

    CAS  PubMed  Google Scholar 

  • Collet TS, Graham P (2004) Animal navigation: path integration, visual landmarks and cognitive maps. Curr Biol 14:R475–R477

    Google Scholar 

  • Crooks N, Waring CP (2013) A study into the sexual dimorphisms of the Ampullae of Lorenzini in the lesser-spotted catshark, Scyliorhinus canicula (Linnaeus, 1758). Environ Biol Fish 96:585–590

    Google Scholar 

  • Endres CS, Putman NF, Ernst DA, Kurth JA, Lohmann CF, Lohmann KJ (2016) Mulit-modal homing in sea turtles: modeling dual use of geomagnetic and chemical cues in island-finding. Front Behav Neurosci 10:19. https://doi.org/10.3389/fnbeh.2016.00019

    Article  PubMed  PubMed Central  Google Scholar 

  • Fahy DP, Spieler RE, Hamlett WC (2007) Preliminary observations on the reproductive cycle and uterine fecundity of the yellow stingray, Urobatis jamaicensis (Elasmobranchii: Myliobatiformes: Urolophidae) in Southeast Florida, USA. Raffles Bull Zool Suppl 14:131–139

    Google Scholar 

  • Fischer JH, Freake MJ, Phillips JB (2001) Evidence for the use of magnetic map information by an amphibian. Anim Behav 62:1–10

    Google Scholar 

  • Flowers KI, Ajemian MJ, Bassos-Hull K, Feldheim KA, Hueter RE, Papastamatiou YP, Chapman DD (2016) A review of batoid philopatry, with implications for future research and population management. Mar Ecol Prog Ser 562:251–261

    Google Scholar 

  • Fuss T, Bleckmann H, Schluessel V (2014) Visual discrimination abilities in the grey bamboo shark, Chiloscyllium griseum. Zoology 117:104–111

    PubMed  Google Scholar 

  • Fuss T, Russnak V, Stehr K, Schluessel V (2017) World in motion: perception and discrimination of movement in juvenile grey bamboo sharks (Chiloscyllium griseum). Anim Behav Cogn 4(3):223–241. https://doi.org/10.26451/abc.04.03.03.2017

    Article  Google Scholar 

  • Gardiner JM, Whitney NM, Hueter RE (2015) Smells like home: the role of olfactory cues in the homing behavior of blacktip sharks, Carcharhinus limbatus. Integr Comp Biol 55(3):495–506

    PubMed  Google Scholar 

  • Gould JL (1998) Sensory bases of navigation. Curr Biol 8(20):R731–R738

    CAS  PubMed  Google Scholar 

  • Gould JL (2004) Animal navigation. Curr Biol 14(6):R221–R224

    CAS  PubMed  Google Scholar 

  • Gould JL (2011) Animal navigation: longitude at last. Curr Biol 21(6):R225–R227

    CAS  PubMed  Google Scholar 

  • Griffin DR (1952) Bird navigation. Biol Rev Camb Philos Soc 27:359–400

    Google Scholar 

  • Hueter RE, Heupel MR, Heist EJ, Keeney DB (2005) Evidence of philopatry in sharks and implications for the management of shark fisheries. J Northwest Atl Fish Sci 35:239–247

    Google Scholar 

  • Kalmijn AJ (1974) The detection of electric fields from inanimate and animate sources other than electric organs. In: Fessard A (ed) Handbook of sensory physiology III/3: electroreceptors and other specialized receptors in lower vertebrates. Springer, Berlin, pp 147–200

    Google Scholar 

  • Kalmijn AJ (1978) Experimental evidence of geomagnetic orientation in elasmobranch fishes. In: Schmidt-Koening K, Keaton WT (eds) Animal migration, navigation, and homing. Springer, Berlin, pp 347–353

    Google Scholar 

  • Kalmijn AJ (1982) Electric and magnetic field detection in elasmobranch fishes. Science 218:916–918

    CAS  PubMed  Google Scholar 

  • Keller BA (2020) The spatiotemporal ecology of the bonnethead shark, Sphyrna tiburo: migration, parturition and magnetic-based navigation. PhD Dissertation, Florida State University, College of Arts and Sciences, Tallahassee, FL, USA

  • Kelly JC, Nelson DR (1975) Hearing thresholds of the horn shark, Heterodontus francisci. J Acoust Soc Am 58:905

    CAS  PubMed  Google Scholar 

  • Kempster RM, Garza-Gisholt E, Egeberg CA, Hart NS, O’Shea OR, Collin SP (2013) Sexual dimorphism of the electrosensory system: a quantitative analysis of nerve axons in the dorsal anterior lateral line nerve of the blue-spotted fantail ray (Taeniura lymma). Brain Behav Evol 8:226–235

    Google Scholar 

  • Kirschvink JL, Walker MW, Diebel CE (2001) Magnetite-based magnetoreception. Curr Opin Neurobiol 11:462–467

    CAS  PubMed  Google Scholar 

  • Klimley AP (1993) Highly directional swimming by scalloped hammerhead sharks, Sphyrna lewini, and subsurface irradiance, temperature, bathymetry, and geomagnetic-field. Mar Biol 117:1–22

    Google Scholar 

  • Kramer G (1953) Wird die Sonnenhöhe bei der Heimfinde orientierung ververtet? J Ornithol 94:201–219

    Google Scholar 

  • Kramer G (1957) Experiments in bird orientation and their interpretation. Ibis 99:196–227

    Google Scholar 

  • Lohmann KJ (1991) Magnetic orientation by hatchling loggerhead sea turtles (Caretta caretta). J Exp Biol 155:37–49

    CAS  PubMed  Google Scholar 

  • Lohmann KJ, Lohmann CMF (1994) Detection of magnetic inclination angle by sea turtles: a possible mechanism for determining latitude. J Exp Biol 194:23–32

    CAS  PubMed  Google Scholar 

  • Lohmann KJ, Lohmann CMF (1996) Detection of magnetic field intensity by sea turtles. Nature 380:59–61

    CAS  Google Scholar 

  • Lohmann KJ, Lohmann CMF (2006) Sea turtles, lobsters, and oceanic maps. Mar Freshw Behav Physiol 39:49–64

    Google Scholar 

  • Lohmann KJ, Lohmann CMF, Putman NF (2007) Magnetic maps in animals. J Exp Biol 210:3697–3705

    PubMed  Google Scholar 

  • Merritt R, Purcell C, Stroink G (1983) Uniform magnetic field produced by three, four and five square coils. Rev Sci Instrum 54:879–882

    Google Scholar 

  • Meyer CG, Holland KN, Papastamatiou YP (2005) Sharks can detect changes in the geomagnetic field. J R Soc Interface 2:129–130

    PubMed  Google Scholar 

  • Montgomery JC (1984) Frequency response characteristics of primary and secondary neurons in the electrosensory neurons in the electrosensory system of the thornback ray. Comp Biochem Physiol 79A:189–195

    Google Scholar 

  • Naisbett-Jones LC, Putman NF, Stephenson JF, Ladak S, Young KA (2017) A magnetic map leads juvenile European eels to the Gulf Stream. Curr Biol. https://doi.org/10.1016/j.cub.2017.03.015

    Article  PubMed  Google Scholar 

  • Nelson DR (1967) Hearing thresholds, frequency discrimination and acoustic orientation in the lemon shark, Negaprion brevirostris (Poey). Bull Mar Sci 17(3):741–767

    Google Scholar 

  • Newton KC, Kajiura SM (2017) Magnetic field discrimination, learning and memory in the yellow stingray, Urobatis jamaicensis. Anim Cogn 20(4):603–614

    PubMed  Google Scholar 

  • Newton KC, Kajiura SM (2020) The yellow stingray, Urobatis jamaicensis, can use magnetic field polarity to orient in space and solve a maze. Mar Biol 167:36. https://doi.org/10.1007/s00227-019-3643-9

    Article  Google Scholar 

  • Nosal AP, Chao Y, Farrara JD, Chai F, Hastings PA (2016) Olfaction contributes to pelagic navigation in a coastal shark. PLoS ONE 11(1):e0143758. https://doi.org/10.1371/journal.pone.0143758

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O’Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Oxford University Press/Clarendon Press, Oxford

    Google Scholar 

  • Paulin MG (1995) Electrorecpetion and the compass sense of sharks. J Theor Biol 174:325–339

    Google Scholar 

  • Peters RC, Evers HP (1985) Frequency selectivity in the ampullary system of an elasmobranch fish (Scyliorhinus canicula). J Exp Biol 118:99–109

    Google Scholar 

  • Phillips JB, Freake MJ, Fischer JH, Borland SC (2002) Behavioral titration of a magnetic map coordinate. J Comp Physiol A 188:157–160

    Google Scholar 

  • Piercy AN, Snelson FF, Grubbs RD (2006) Urobatis jamaicensis. IUCN Red List of Threatened Species. Version 2016-1. http://www.iucnredlist.org/details/60109/0. Accessed 30 Mar 2017

  • Putman NF, Endres CS, Lohmann CMF, Lohmann KJ (2011) Longitude perception and bicoordinate magnetic maps in sea turtles. Curr Biol 21:463–466

    CAS  PubMed  Google Scholar 

  • Putman NF, Lohman KJ, Putman EJ, Quinn TP, Klimley AP, Noakes DLG (2013) Evidence for geomagnetic imprinting as a homing mechanism in pacific salmon. Curr Biol 23(4):312–316

    CAS  PubMed  Google Scholar 

  • Putman NF, Scanlon MM, Billman EJ, O’Neil JP, Couture RB, Quinn TP, Lohmann KJ, Noakes DLG (2014) An inherited magnetic map guides ocean navigation in juvenile pacific salmon. Curr Biol 24(4):446–450

    CAS  PubMed  Google Scholar 

  • Putman NF, Williams CR, Gallagher EP, Dittman AH (2020) A sense of place: pink salmon use a magnetic map for orientation. J Exp Biol 223:jeb218735

    PubMed  Google Scholar 

  • Rodda GH (1984) The orientation and navigation of juvenile alligators: evidence of magnetic sensitivity. J Comp Physiol 154:649–658

    Google Scholar 

  • Scanlan MM, Putman NF, Pollock AM, Noakes DL (2018) Magnetic map in nonanadromous Atlantic salmon. PNAS 115:10995–10999

    CAS  PubMed  Google Scholar 

  • Schluessel V, Bleckmann H (2005) Spatial memory and orientation strategies in the elasmobranch Potamotrygon motoro. J Comp Physiol A 191:695–706

    Google Scholar 

  • Schluessel V, Fricke G, Bleckmann H (2012) Visual discrimination and object categorization in the cichlid Pseudotropheus sp. Anim Cogn 15:525–537

    CAS  PubMed  Google Scholar 

  • Schluessel V, Beil O, Weber T, Bleckmann H (2014) Symmetry perception in bamboo sharks (Chiloscyllium griseum) and Malawi cichlids (Pseudotropheus sp.). Anim Cogn 17(5):1187–1205

    CAS  PubMed  Google Scholar 

  • Schluessel V, Kortekamp N, Cortes JA, Klein A, Bleckmann H (2015) Perception and discrimination of movement and biological motion patterns in fish. Anim Cogn 18(5):1077–1091. https://doi.org/10.1007/s10071-015-0876-y

    Article  CAS  PubMed  Google Scholar 

  • Schluessel V, Hiller J, Krueger M (2018) Discrimination of movement and visual transfer abilities in cichlids (Pseudotropheus zebra). Behav Ecol Sociobiol 72:61. https://doi.org/10.1007/s00265-018-2476-8

    Article  Google Scholar 

  • Schwarze S, Bleckmann H, Schluessel V (2013) Avoidance conditioning in bamboo sharks (Chiloscyllium griseum and C. punctatum): behavioral and neuroanatomical aspects. J Comp Physiol A 199(10):843–856

    Google Scholar 

  • Semm P, Beason RC (1990) Responses to small magnetic variations by the trigeminal system of the bobolink. Brain Res Bull 25:735–740

    CAS  PubMed  Google Scholar 

  • Siciliano AM, Kajiura SM, Long JH, Porter ME (2013) Are you positive? Electric dipole polarity discrimination in the yellow stingray (Urobatis jamaicensis). Biol Bull 225:85–91

    PubMed  Google Scholar 

  • Sisneros JA, Tricas TC (2000) Androgen-induced changes in response dynamics of primary ampullary electrosensory primary afferent neurons. J Neurosci 20(22):8586–8595

    CAS  PubMed  PubMed Central  Google Scholar 

  • Speed CW, Field IC, Meekan MG, Bradshaw CJA (2010) Complexities of coastal shark movements and their implications for management. Mar Ecol Prog Ser 408:275–293

    Google Scholar 

  • Tricas T, New JG (1998) Sensitivity and response dynamics of elasmobranch electrosensory primary afferent neurons to near threshold fields. J Comp Physiol A 182:89–101

    CAS  PubMed  Google Scholar 

  • Tricas TC, Michael SW, Sisneros JA (1995) Electrosensory optimization to conspecific phasic signals for mating. Neurosci Lett 202:129–132

    CAS  PubMed  Google Scholar 

  • Vaudo JJ, Lowe CG (2006) Movement patterns of the round stingray Urobatis halleri (Cooper) near a thermal outfall. J Fish Biol 68:1756–1766

    Google Scholar 

  • Walker MM, Diebel CE, Kirschvink JL (2003) Detection and use of the Earth’s magnetic field by aquatic vertebrates. In: Collin SP, Marshall NJ (eds) Sensory processing in aquatic environments. Springer, New York, pp 53–74

    Google Scholar 

  • Wiltschko W, Wiltschko R (2007) Conditioning to magnetic directions. NeuroReport 18:949–950

    PubMed  Google Scholar 

Download references

Acknowledgements

This research was supported by grants to KCN from the Florida Atlantic University (FAU) Graduate Grant, the Save Our Seas Foundation Small Grant, the Henry F. Mollet Research Award from the American Elasmobranch Society, the Gordon Gilbert Graduate Scholarship from the Friends of Gumbo Limbo Nature Center, and the PADI Foundation Grant. The authors thank S. Creager, A. Murakami, E. Cave, L. Celano, J. Noble, G. Gil, B. Bowers, K. Kramer, and S. Ramirez for help with stingray collection and husbandry, and R. Stackman and M. Salmon for assistance with experimental design and animal training protocols.

Author information

Author notes

  1. Kyle C. Newton

    Present address: Department of Otolaryngology, Washington University School of Medicine, 666 Euclid Ave, Campus Box 8115, Saint Louis, MO, 63110, USA

Authors and Affiliations

  1. Department of Biological Sciences, Florida Atlantic University, 777 Glades Road, Boca Raton, FL, 33431, USA

    Kyle C. Newton & Stephen M. Kajiura

Authors
  1. Kyle C. Newton
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stephen M. Kajiura
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kyle C. Newton.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Statement of animal welfare and ethics

All applicable international, national, and institutional guidelines for the care and use of animals were followed. All procedures performed in these studies involving animals were in accordance with the ethical standards of the Florida Atlantic University Institutional Animal Care and Use Committee under protocols A23-13 and A16-33. Animals were collected pursuant to Florida Fish and Wildlife Conservation Commission Special Activities License SAL 15-1413A-SR.

Significance

Previous work has shown that elasmobranchs (sharks, skates, and rays) can detect magnetic stimuli and might use the Earth’s magnetic field as a navigational cue. However, the specific nature of the geomagnetic cues that elasmobranchs can detect are largely unknown. This study used behavioral conditioning to demonstrate that the yellow stingray, Urobatis jamaicensis, can detect changes in the intensity and inclination angle to the geomagnetic field. These cues change predictably with latitude and are used by other magnetically sensitive species to determine their location during long distance navigation.

Additional information

Responsible Editor: J. Carlson.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Reviewed by P. Klimley and an undisclosed expert.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Newton, K.C., Kajiura, S.M. The yellow stingray (Urobatis jamaicensis) can discriminate the geomagnetic cues necessary for a bicoordinate magnetic map. Mar Biol 167, 151 (2020). https://doi.org/10.1007/s00227-020-03763-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-020-03763-1

Search

Navigation