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The yellow stingray (Urobatis jamaicensis) can use magnetic field polarity to orient in space and solve a maze

DOI:10.1007/s00227-019-3643-9
Authors:
Kyle Newton at Oregon State University
Kyle Newton
Stephen M Kajiura at Florida Atlantic University
Stephen M Kajiura
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Abstract and Figures

Elasmobranch fishes (sharks, skates, and rays) have been hypothesized to use the geomagnetic field (GMF) to maintain a sense of direction as they navigate throughout their environment. However, it is difficult to test the sensory ecology and spatial orientation ability of large highly migratory fishes in the field. Therefore, we performed behavioral conditioning experiments on a small magnetically sensitive species, the yellow stingray (Urobatis jamaicensis), in the laboratory. We trained individuals to use the polarity, or the north–south direction, of the GMF as a cue to orient in space and navigate a T-maze for a food reward. Subjects were split into two groups that learned to associate the direction of magnetic north or south as the indicator of the reward location. Stingrays reached the learning criterion within a mean (± SE) of 158.6 ± 28.4 trials. Subjects were then reverse trained to use the previously unrewarded magnetic stimulus of the opposite polarity as the new cue for the reward location. Overall, the stingrays reached the reversal criterion in significantly fewer trials (120 ± 13.8) compared to the initial procedure. These data show that the yellow stingray can learn to associate changes in GMF polarity with a reward, relearn a behavioral task when the reward contingency is modified, and learn a reversal procedure faster than the initial association. These data support the idea that the yellow stingray, and perhaps other elasmobranchs, might use GMF polarity as a cue to orient and maintain a heading during navigation.
a–b Schematic diagram of the T-maze setup from an overheard view. The geomagnetic field is indicated by the red arrow, whereas gray lines and arrows indicate the isolines of the magnetic field applied by the green solenoid coils located at the maze intersection. Prior to the start of a trial (a) the stingray was behind a gate in the start arm and the magnetic stimulus was switched off. The trial began (b) as the magnetic stimulus was switched on, the gate was lifted, and the stingray swam into the intersection and choose to turn right. In this example, the stingray was trained to use magnetic north (N) as the indicator for the correct arm and it received a food reward after passing the magnetic coils (thick green lines)
a–b Schematic diagram of the T-maze setup from an overheard view. The geomagnetic field is indicated by the red arrow, whereas gray lines and arrows indicate the isolines of the magnetic field applied by the green solenoid coils located at the maze intersection. Prior to the start of a trial (a) the stingray was behind a gate in the start arm and the magnetic stimulus was switched off. The trial began (b) as the magnetic stimulus was switched on, the gate was lifted, and the stingray swam into the intersection and choose to turn right. In this example, the stingray was trained to use magnetic north (N) as the indicator for the correct arm and it received a food reward after passing the magnetic coils (thick green lines)
… 
The yellow stingray can be trained to use magnetic polarity as a positive stimulus to solve a T-maze task, then it can relearn the task when the reward contingency is reversed. Stingrays trained during the initial conditioning paradigm (n = 7) showed a significant increase in the mean (± SE) number of correct responses from the first two sessions to the final two sessions (p ≤ 0.01). Likewise, stingrays that underwent the serial reversal paradigm (n = 5) showed a significant increase in the mean (± SE) number of responses from the first two sessions to the final two sessions (p ≤ 0.05). Symbols indicate individual stingrays
The yellow stingray can be trained to use magnetic polarity as a positive stimulus to solve a T-maze task, then it can relearn the task when the reward contingency is reversed. Stingrays trained during the initial conditioning paradigm (n = 7) showed a significant increase in the mean (± SE) number of correct responses from the first two sessions to the final two sessions (p ≤ 0.01). Likewise, stingrays that underwent the serial reversal paradigm (n = 5) showed a significant increase in the mean (± SE) number of responses from the first two sessions to the final two sessions (p ≤ 0.05). Symbols indicate individual stingrays
… 
The yellow stingray can solve a serial reversal task in fewer trials compared to the initial conditioning paradigm. The mean (± SE) number of sessions to criterion for stingrays (n = 5) that learned to use magnetic field polarity to solve a T-maze task during reversal training was significantly fewer compared to the initial conditioning experiments (p ≤ 0.05). Symbols indicate individual stingrays
The yellow stingray can solve a serial reversal task in fewer trials compared to the initial conditioning paradigm. The mean (± SE) number of sessions to criterion for stingrays (n = 5) that learned to use magnetic field polarity to solve a T-maze task during reversal training was significantly fewer compared to the initial conditioning experiments (p ≤ 0.05). Symbols indicate individual stingrays
… 
a–g Learning acquisition curves for yellow stingrays conditioned to use magnetic field polarity (positive stimulus) as a cue to solve a T-maze task for a food reward. Red lines indicate female stingrays and blue lines are males. Squares indicate that the positive stimulus is magnetic north and circles are magnetic south. Solid lines and symbols indicate the first series of training sessions for a positive stimulus, whereas empty symbols and dotted lines indicate reversal training to the opposite positive stimulus. Sessions of ten trials occurred daily and the number of correct choices for a session is plotted. Individual stingrays (n = 7) reached the learning criterion for initial training by: a 120 trials**, b 100 trials*, c 250 trials*, d 180 trials*, e 170 trials* f 250 trials**, and g 50 trials*. Stingrays were reverse trained (n = 5) and reached the learning criterion by: c 150 trials*, d 120 trials*, e 100 trials***, f 150 trials**, and g 80 trials**. (* = p ≤ 0.05; ** = p ≤ 0.01; *** = p ≤ 0.005)
a–g Learning acquisition curves for yellow stingrays conditioned to use magnetic field polarity (positive stimulus) as a cue to solve a T-maze task for a food reward. Red lines indicate female stingrays and blue lines are males. Squares indicate that the positive stimulus is magnetic north and circles are magnetic south. Solid lines and symbols indicate the first series of training sessions for a positive stimulus, whereas empty symbols and dotted lines indicate reversal training to the opposite positive stimulus. Sessions of ten trials occurred daily and the number of correct choices for a session is plotted. Individual stingrays (n = 7) reached the learning criterion for initial training by: a 120 trials**, b 100 trials*, c 250 trials*, d 180 trials*, e 170 trials* f 250 trials**, and g 50 trials*. Stingrays were reverse trained (n = 5) and reached the learning criterion by: c 150 trials*, d 120 trials*, e 100 trials***, f 150 trials**, and g 80 trials**. (* = p ≤ 0.05; ** = p ≤ 0.01; *** = p ≤ 0.005)
… 
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Marine Biology (2020) 167:36
https://doi.org/10.1007/s00227-019-3643-9
ORIGINAL PAPER
The yellow stingray (Urobatis jamaicensis) can use magnetic eld
polarity toorient inspace andsolve amaze
KyleC.Newton1,2 · StephenM.Kajiura1
Received: 20 August 2019 / Accepted: 30 December 2019 / Published online: 6 February 2020
© Springer-Verlag GmbH Germany, part of Springer Nature 2020
Abstract
Elasmobranch fishes (sharks, skates, and rays) have been hypothesized to use the geomagnetic field (GMF) to maintain a
sense of direction as they navigate throughout their environment. However, it is difficult to test the sensory ecology and
spatial orientation ability of large highly migratory fishes in the field. Therefore, we performed behavioral conditioning
experiments on a small magnetically sensitive species, the yellow stingray (Urobatis jamaicensis), in the laboratory. We
trained individuals to use the polarity, or the north–south direction, of the GMF as a cue to orient in space and navigate a
T-maze for a food reward. Subjects were split into two groups that learned to associate the direction of magnetic north or
south as the indicator of the reward location. Stingrays reached the learning criterion within a mean (± SE) of 158.6 ± 28.4
trials. Subjects were then reverse trained to use the previously unrewarded magnetic stimulus of the opposite polarity as the
new cue for the reward location. Overall, the stingrays reached the reversal criterion in significantly fewer trials(120 ± 13.8)
compared to the initial procedure. These data show that the yellow stingray can learn to associate changes in GMF polarity
with a reward, relearn a behavioral task when the reward contingency is modified, and learn a reversal procedure faster than
the initial association. These data support the idea that the yellow stingray, and perhaps other elasmobranchs, might use
GMF polarity as a cue to orient and maintain a heading during navigation.
Introduction
Orientation is an integral part of animal navigation where
an organism aligns itself with respect to an external cue
(Berthold 2001; Gould 1998) to maintain a desired head-
ing. However, calculating a heading requires thatthe animal
know its current position relative to that of its goal so that it
can determine the correct direction in which to travel (Gould
1998; 2004). The animal can then use an appropriate envi-
ronmental cue, such as visual landmarks, localized sounds
or odor gradients, the position of the sun, or the direc-
tion of thegeomagnetic field (GMF) as an external point
of reference to maintain the correct orientation. Animals
can use different types of cues to form distinct cognitive
compasses and employ them as needed when environmen-
tal stimuli cease to propagate and become unreliable (Able
1991; Gould 1998). The physical nature of a cue and how it
behaves in a medium, such as seawater, will determine how
effective that cue is for navigating over a given spatiotem-
poral scale. Cues that originate from localized sources tend
to diminish rapidly with space and time, which makes them
effective beacons or landmarks (Shettleworth and Sutton
2005; Cheng 2012) for relatively short distance navigation.
Conversely, global cues such as celestial rotation or GMF
polarity fluctuate very little over small spatiotemporal scales
and are well suited for navigational tasks that can last several
months and span thousands of kilometers.
The GMF has polarity, or a north–south directional com-
ponent, because on the surface of the Earthit is emitted from
the magnetic north pole located in the southern hemisphere
and terminates atthe magnetic south pole in the northern
hemisphere. The GMF at any geographic location can be
described by a vector with an overall intensity of 20–70 µT
and an inclination angle (measured relative to the surface of
the Earth) that ranges from + 90° to − 90°. These quantities
Responsible Editor: J. Carlson.
Reviewed by undisclosed experts.
* Kyle C. Newton
kyle.newton@wustl.edu
1 Department ofBiological Science, Florida Atlantic
University, 777 Glades Road, BocaRaton, FL33431, USA
2 Present Address: Department ofOtolaryngology, Washington
University School ofMedicine, 660 South Euclid Avenue,
Campus Box8115, St.Louis, MO63110, USA
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... Fields for Navigation Chondrichthyans have been hypothesized to use the geomagnetic feld (GMF) as a cue to navigate across oceans that are largely devoid of prominent features or useful landmarks (Kalmijn 1974;Klimley 1993;Paulin 1995). Behavioral conditioning experiments have shown that the urolophid stingrays can discriminate between the north and south poles of a magnetic feld (Kalmijn 1978;Newton and Kajiura 2020a) and use GMF polarity to solve a spatial navigation task (Newton and Kajiura 2020a), which suggests that stingrays might have magnetic polarity-based compass, or sense of direction. The Yellow Stingray can discriminate between changes in GMF intensity and inclination angle (Newton and Kajiura 2020b), and juvenile Bonnetheads can use these GMF cues to consistently reorient themselves toward their home range in experimentally altered magnetic felds (Keller et al. 2021). ...
... Fields for Navigation Chondrichthyans have been hypothesized to use the geomagnetic feld (GMF) as a cue to navigate across oceans that are largely devoid of prominent features or useful landmarks (Kalmijn 1974;Klimley 1993;Paulin 1995). Behavioral conditioning experiments have shown that the urolophid stingrays can discriminate between the north and south poles of a magnetic feld (Kalmijn 1978;Newton and Kajiura 2020a) and use GMF polarity to solve a spatial navigation task (Newton and Kajiura 2020a), which suggests that stingrays might have magnetic polarity-based compass, or sense of direction. The Yellow Stingray can discriminate between changes in GMF intensity and inclination angle (Newton and Kajiura 2020b), and juvenile Bonnetheads can use these GMF cues to consistently reorient themselves toward their home range in experimentally altered magnetic felds (Keller et al. 2021). ...
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... Each of these locomotory modes poses different challenges for researchers attempting to monitor orientation behavior. As a result, a number of different experimental arenas have been designed, ranging from simple circular arenas (Putman et al. 2014c) to more elaborate arenas and mazes (Nishi et al. 2018;Newton and Kajiura 2020a). The need to develop an arena that matches the behavior of each species of fish-and sometimes each life-history stage-stands in sharp contrast to magnetic orientation studies with birds, most of which rely on a standard experimental arena that takes advantage of the migratory restlessness characteristic of many songbirds (Emlen and Emlen 1966;Wiltschko and Wiltschko 1995). ...
... Fish quickly learned to discriminate between the two magnetic field conditions, although the exact parameter(s) of the field detected by the fish could not be determined. A similar approach was later used in studies with several additional species (e.g., Walker et al. 1997;Newton and Kajiura 2020a), demonstrating that magnetic conditioning is viable in diverse fishes. A somewhat different technique involving cardiac conditioning has provided evidence that rainbow trout can detect not only changes in magnetic field direction, but also large shifts in magnetic field inclination and intensity (Hellinger and Hoffmann 2009). ...
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... For comparison, a study examining the detection of magnetic anomalies in pigeons in a conditioned choice experiment used 145 µT above background levels (Mora et al. 2004). In a follow up study by Newton and Kajiura (2020a), yellow stingrays were trained to use the polarity of the geomagnetic field (i.e. the north-south direction) as an orientation cue to find food in a T-maze. All stingrays reached the learning criterion and were then reverse trained to associate the previously unrewarded magnetic stimulus (i.e. ...
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... Inspiring studies: Salmon migration over the Trans Bay Cable (Wyman et al. 2018); eel migration over cables (Westerberg et al. 2008, ongoing BOEM study); elasmobranch detection of changes in the geomagnetic angle of inclination in lab studies (Newton et al. 2020); modelled and measured EMFs and mesocosm studies on crustaceans and elasmobranchs (Hutchison et al. 2020c); recent review on the topic (Hutchison et al. 2020b). This topic was also recently identified as a research need for sea turtles (Gitschlag et al. 2021). ...
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Using the expression of the immediate early gene (IEG) egr-1 as a neuronal activity marker, brain regions potentially involved in learning and long-term memory functions in the grey bamboo shark were assessed with respect to selected visual discrimination abilities. Immunocytochemistry revealed a significant up-regulation of egr-1 expression levels in a small region of the telencephalon of all trained sharks (i.e., ‘early’ and ‘late learners’, ‘recallers’) when compared to three control groups (i.e., ‘controls’, ‘undisturbed swimmers’, ‘constant movers’). There was also a well-defined difference in egr-1 expression patterns between the three control groups. Additionally, some staining was observed in diencephalic and mesencephalic sections; however, staining here was weak and occurred only irregularly within and between groups. Therefore, it could have either resulted from unintentional cognitive or non-cognitive inducements (i.e., relating to the mental processes of perception, learning, memory, and judgment, as contrasted with emotional and volitional processes) rather than being a training effect. Present findings emphasize a relationship between the training conditions and the corresponding egr-1 expression levels found in the telencephalon of Chiloscyllium griseum. Results suggest important similarities in the neuronal plasticity and activity-dependent IEG expression of the elasmobranch brain with other vertebrate groups. The presence of the egr-1 gene seems to be evolutionarily conserved and may therefore be particularly useful for identifying functional neural responses within this group.
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Zebrafish and medaka offer insights into the neurobehavioral correlates of vertebrate magnetoreception
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Full-text available
  • Feb 2018
An impediment to a mechanistic understanding of how some species sense the geomagnetic field ("magnetoreception") is the lack of vertebrate genetic models that exhibit well-characterized magnetoreceptive behavior and are amenable to whole-brain analysis. We investigated the genetic model organisms zebrafish and medaka, whose young stages are transparent and optically accessible. In an unfamiliar environment, adult fish orient according to the directional change of a magnetic field even in darkness. To enable experiments also in juveniles, we applied slowly oscillating magnetic fields, aimed at generating conflicting sensory inputs during exploratory behavior. Medaka (but not zebrafish) increase their locomotor activity in this assay. Complementary brain activity mapping reveals neuronal activation in the lateral hindbrain during magnetic stimulation. These comparative data support magnetoreception in teleosts, provide evidence for a light-independent mechanism, and demonstrate the usefulness of zebrafish and medaka as genetic vertebrate models for studying the biophysical and neuronal mechanisms underlying magnetoreception.
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Insight into shark magnetic field perception from empirical observations
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Full-text available
  • Sep 2017
Elasmobranch fishes are among a broad range of taxa believed to gain positional information and navigate using the earth’s magnetic field, yet in sharks, much remains uncertain regarding the sensory receptors and pathways involved, or the exact nature of perceived stimuli. Captive sandbar sharks, Carcharhinus plumbeus were conditioned to respond to presentation of a magnetic stimulus by seeking out a target in anticipation of reward (food). Sharks in the study demonstrated strong responses to magnetic stimuli, making significantly more approaches to the target (p = < 0.01) during stimulus activation (S+) than before or after activation (S−). Sharks exposed to reversible magnetosensory impairment were less capable of discriminating changes to the local magnetic field, with no difference seen in approaches to the target under the S+ and S− conditions (p = 0.375). We provide quantified detection and discrimination thresholds of magnetic stimuli presented, and quantify associated transient electrical artefacts. We show that the likelihood of such artefacts serving as the stimulus for observed behavioural responses was low. These impairment experiments support hypotheses that magnetic field perception in sharks is not solely performed via the electrosensory system, and that putative magnetoreceptor structures may be located in the naso-olfactory capsules of sharks.
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A Magnetic Map Leads Juvenile European Eels to the Gulf Stream
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Migration allows animals to track the environmental conditions that maximize growth, survival, and reproduction [1–3]. Improved understanding of the mechanisms underlying migrations allows for improved management of species and ecosystems [1–4]. For centuries, the catadromous European eel (Anguilla anguilla) has provided one of Europe’s most important fisheries and has sparked considerable scientific inquiry, most recently owing to the dramatic collapse of juvenile recruitment [5]. Larval eels are transported by ocean currents associated with the Gulf Stream System from Sargasso Sea breeding grounds to coastal and freshwater habitats from North Africa to Scandinavia [6, 7]. After a decade or more, maturing adults migrate back to the Sargasso Sea, spawn, and die [8]. However, the migratory mechanisms that bring juvenile eels to Europe and return adults to the Sargasso Sea remain equivocal [9, 10]. Here, we used a ‘‘magnetic displacement’’ experiment [11, 12] to show that the orientation of juvenile eels varies in response to subtle differences in magnetic field intensity and inclination angle along their marine migration route. Simulations using an ocean circulation model revealed that even weakly swimming in the experimentally observed directions at the locations corresponding to the magnetic displacements would increase entrainment of juvenile eels into the Gulf Stream System. These findings provide new insight into the migration ecology and recruitment dynamics of eels and suggest that an adaptive magnetic map, tuned to large-scale features of ocean circulation, facilitates the vast oceanic migrations of the Anguilla genus [7, 13, 14].
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Magnetic field discrimination, learning, and memory in the yellow stingray (Urobatis jamaicensis)
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Elasmobranch fishes (sharks, skates, and rays) have been hypothesized to use the geomagnetic field as a cue for orienting and navigating across a wide range of spatial scales. Magnetoreception has been demonstrated in many invertebrate and vertebrate taxa, including elasmobranchs, but this sensory modality and the cognitive abilities of cartilaginous fishes are poorly studied. Wild caught yellow stingrays, Urobatis jamaicensis (N = 8), underwent conditioning to associate a magnetic stimulus with a food reward in order to elicit foraging behaviors. Behavioral conditioning consisted of burying magnets and non-magnetic controls at random locations within a test arena and feeding stingrays as they passed over the hidden magnets. The location of the magnets and controls was changed for each trial, and all confounding sensory cues were eliminated. The stingrays learned to discriminate the magnetic stimuli within a mean of 12.6 ± 0.7 SE training sessions of four trials per session. Memory probes were conducted at intervals between 90 and 180 days post-learning criterion, and six of eight stingrays completed the probes with a ≥75% success rate and minimum latency to complete the task. These results show the fastest rate of learning and longest memory window for any batoid (skate or ray) to date. This study demonstrates that yellow stingrays, and possibly other elasmobranchs, can use a magnetic stimulus as a geographic marker for the location of resources and is an important step toward understanding whether these fishes use geomagnetic cues during spatial navigation tasks in the natural environment.
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A review of batoid philopatry, with implications for future research and population management
Article
Full-text available
  • Dec 2016
Animal movements, in particular residency or return migrations (collectively defined as ‘philopatry’), can shape population structure and have implications for management. This review examines the evidence for philopatry in batoids, which are some of the least understood and most threatened vertebrates, and updates a prior review of the same in sharks. Evidence for philopatry in batoids was found in 46 studies, including 31 species that involve 11 species complexes. Batoid philopatry research has lagged behind shark philopatry research, with the annual publication rate of shark philopatry studies in the last 5 yr (17 yr-1) being more than twice that of batoids (7 yr-1). Philopatry research on both sharks and rays is taxonomically skewed: <50% of elasmobranch families are represented. Research is also skewed towards charismatic megafauna (white sharks, whale sharks, and manta rays), while the batoid philopatry literature is biased towards ‘Near Threatened’ species, even though approx. 47.5% of batoids are considered to be ‘Data Deficient’ by the IUCN. Limited evidence was found for residency in batoids, contrary to popular assumptions that they are sedentary, and there was limited evidence for sex-differentiated movements. Hypothesis-driven research, longer study durations, more taxon and life stage diverse studies, and consistent use of philopatry terminology are needed to advance the fields of batoid philopatry and conservation. Given strong evidence of philopatry in some species of batoids, management should proceed at the local scale until more studies are conducted.
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How to get out of a maze? Stingrays (Potamotrygon motoro) use directional over landmark information when provided with both in a spatial task
Article
Background: Previous studies have shown that stingrays can exploit a variety of spatial learning strategies, including directional, landmark, and place learning. In these studies, allocentric and global strategies were preferred over egocentric information and local strategies. Elasmobranchs represent the oldest extant vertebrate group. Considering their key phylogenetic position, we wished to address the evolution of spatial strategies as well as the significance of specific strategies over others. Aim: Investigate cue preferences in two types of maze experiments by assessing the significance of single landmarks and directional cues (both egocentric strategies) for orientation. Organism: Freshwater stingrays (Potamotrygon motoro). Methods: In two independent experiments, five juvenile stingrays were trained to find their way through a maze while being given both landmark and directional information.Transfer tests (in which conflicts between both kinds of information were created) showed which cues the rays used preferentially to reach their goal. Results: All rays successfully learned to master the mazes in both experiments, so all were capable of learning and the application of spatial memory. Rays placed more importance on directional information than on landmark cues. This applied to abstract cues (provided in the form of cards featuring symbols) as well as ‘natural’ landmark cues (in the form of plants). Once rays were trained to use directional information, it was not possible to reverse their preference and get them to use landmark information instead. Conclusion: Freshwater stingrays learn quickly and prefer directional information to single landmark cues.
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Influence of Magnetic Field on the Spatial Orientation in Zebrafish (Danio rerio) (Cyprinidae) and Roach (Rutilus rutilus) (Cyprinidae)
Article
  • May 2016
Preferred direction of motion under influence of geomagnetic field and its modifications was registered in zebrafish (Danio rerio) raised in laboratory culture and in roach (Rutilus rutilus) from the Rybinsk Reservoir. In the geomagnetic field, specimens of zebrafish prefer two opposite directions oriented towards the north and south, while they prefer towards east and west at 90° turning of the horizontal component of geomagnetic field. The specimens of roach in the geomagnetic field prefer only the direction oriented towards east–northeast. This direction coincides with the direction along the canal where roach was sampled to the main river channel part of the Rybinsk Reservoir. At 90° rotation of the horizontal component of geomagnetic field, the direction turns to the south–southeast. The reasons for selection of certain directions in the geomagnetic field are discussed.
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Experimental Evidence of Geomagnetic Orientation in Elasmobranch Fishes
Chapter
  • Jan 1978
Marine sharks, skates, and rays are endowed with an electric sense that enables them to detect voltage gradients as low as 0.01 μV/cm within the frequency range of direct current (DC) up to about 8 Hz. Their electroreceptor system comprises the ampullae of Lorenzini, which are delicate sensory structures in the snouts of these elasmobranch fishes. Sharks, skates, and rays use their electric sense in prédation, sharply cueing in on the DC and low-frequency bioelectric fields of their prey. Swimming through the earth’s magnetic field, they also induce electric fields that may provide them with the physical basis of an electromagnetic compass sense. Their ability to orient magnetically has in fact been demonstrated in recent training experiments.
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