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

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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.
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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). ...
... 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 example, in the laboratory, yellow stingrays (Urobatis jamaicensis) can learn behavioral responses based on reward contingencies, indicating the ability to associate a stimulus with a reward and to discriminate among stimuli as to which yield rewards and which do not. They were also able to relearn the task upon modification of the reward structure, and do so at a faster rate than the initial learning curve (Newton and Kajiura, 2020). In the wild, blacktip sharks (Carcharhinus limbatus) integrate input from multiple sensory channels (smell, electroreception, vision, etc.) to navigate over both small-and large-scale distances (Gardiner et al., 2015). ...
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... In addition, elasmobranchs are able to perceive magnetic field (e.g. Kalmijn, 1982;Meyer et al., 2005;Newton & Kajiura, 2020) and one study reported that a shark utilized its perception of magnetic field for navigation (Keller et al., 2021). ...
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... The use of the geomagnetic field as a navigation aid in chondrichthyans was presumed previously (Kalmijn, 1974;Klimley, 1993;Paulin, 1995). strengthened the assumption that there is an active use of the geomagnetic field of the earth in these species (Keller et al., 2021;Newton & Kajiura, 2020). It is not yet fully clarified whether the detection of variation in magnetic fields is conducted via the ampullae of Lorenzini or/and through another (unknown) structure (Anderson et al., 2017;Kalmijn, 1984;Walker et al., 2003). ...
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Thesis
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... For example, the European eel (Anguilla anguilla) displayed orientation shifts in response to very subtle variations in the ambient field (e.g., a 2.4 μT intensity increase and a 2 inclination decrease) (Naisbett-Jones et al., 2017). In addition to this orientation sense based on polarity (Kalmijn, 1978;Newton & Kajiura, 2020a), recent findings demonstrate that elasmobranchs possess a magnetic map sense Newton & Kajiura, 2020b). Current knowledge suggests that marine species may be responsive to extremely subtle magnetic field variations that are associated with power cables and occur within a limited spatial scale away from the cable sheath (Hutchison et al., 2021). ...
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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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