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First published online May 1, 2009
Journal of Experimental Biology 212, 1544-1552 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.025247
Electroreception in the euryhaline stingray, Dasyatis sabina
Florida Atlantic University, Biological Sciences, Boca Raton, FL 33431, USA
* Author for correspondence (e-mail: kajiura{at}fau.edu)
Accepted 25 February 2009
 |
Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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=2026
cm), brackish (15 p.p.t., =41 cm) and full strength
seawater (35 p.p.t., =19 cm). This study demonstrated that the
electrosensitivity of D. sabina is significantly reduced in FW. In
order to elicit a feeding response, stingrays tested in FW required an
electric field 200–300x greater than stingrays tested in brackish
and saltwater (median FW treatments=1.4 µV cm–1, median
brackish–saltwater treatments=6 nV cm–1), and the
maximum orientation distance was reduced by 35.2%, from 44.0 cm in the
brackish and saltwater treatments to 28.5 cm in FW. The St Johns River
stingrays did not demonstrate an enhanced electrosensitivity in FW, nor did
they exhibit reduced sensitivity when introduced to higher salinities.
Stingrays from both populations responded similarly to the prey-simulating
stimulus when tested at similar salinities, regardless of their native
environment. The reduction in electrosensitivity and detection range in FW is
attributed to both an environmental factor (electrical resistivity of the
water) and the physiological function of the ampullary canals. The plasticity
of this sensory system to function across such a wide environmental range
demonstrates its adaptive significance.
Key words: Dasyatidae, ampullae of Lorenzini, electrosensory, system, sensory plasticity
|
INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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All elasmobranch fishes (sharks, skates and rays) possess an extremely
sensitive electrosensory system that enables them to detect weak extrinsic
electric fields in their environment. This sensory capability has been
demonstrated to function in the detection and localization of weak bioelectric
fields of less than 0.5 nV cm–1 generated by prey
(Kalmijn, 1971
;
Tricas, 1982;
Haine et al., 2001;
Kajiura and Holland, 2002) and
conspecifics (Tricas et al.,
1995). It has also been shown to detect the relatively
low-frequency electric fields produced by predators
(Sisneros et al., 1998), and
is theorized to aid in geomagnetic orientation and navigation
(Kalmijn, 1974;
Paulin, 1995).
The elasmobranch electrosensory system consists of hundreds to thousands of
bulb-like electroreceptive organs known as the ampullae of Lorenzini. These
ampullae are grouped into three to five subdermal clusters that are
distributed over the head of galeoids and the head and body of batoids
(Chu and Wen, 1979;
Zakon, 1988). A single ampulla
consists of multiple alveolar sacs continuous with a narrow canal that
terminates in a pore on the skin surface
(Waltman, 1966). The canal
wall is comprised of cells that are bound by tight junctions that form a
higher impedance electrical barrier than the glycoprotein gel within the canal
(Murray and Potts, 1961;
Waltman, 1966;
Brown et al., 2002). The lumen
of the ampulla is lined by a single-layer epithelium that is comprised of
sensory and support cells (Waltman,
1966; Zakon, 1988;
New and Tricas, 2001).
The elasmobranch electrosensory system evolved in a highly conductive
seawater environment. However, there are several elasmobranch species that
have subsequently transitioned to a FW environment. The high impedance FW
environment presents a challenge to their electrosensory system. The obligate
FW South American stingrays (Potamotrygonidae) possess a much thicker skin
than their marine ancestors, which enables the animal to maintain an internal
ionic concentration that is greater than that of the surrounding FW
(New and Tricas, 2001). The
thicker skin also forms a high impedance barrier that results in a large
voltage differential across the skin
(Kalmijn, 1974;
Raschi and Mackanos, 1989;
New and Tricas, 2001). The
ampullae are significantly smaller (microampullae), are individually
distributed in the dermis rather than in subdermal clusters, and the canals
are much shorter (Raschi and Mackanos,
1989; New and Tricas,
2001). Thus, the subdermal location of the microampullae
facilitates detection of these transcutaneous voltage changes
(Kalmijn, 1974;
Zakon, 1988;
New and Tricas, 2001).
Whereas the electrosensory systems of FW elasmobranchs have evolved to
function in a high impedance environment, the electroreceptors of euryhaline
elasmobranchs remain morphologically undifferentiated from exclusively marine
species (Whitehead, 2002).
Nonetheless, euryhaline species retain electroreceptive capabilities in FW, as
demonstrated in the bull shark (Carcharhinus leucas)
(Whitehead, 2002). How the
function of the elasmobranch electric sense is affected when euryhaline
species enter FW remains unknown.
The effect of decreasing salinity on the electrosensory system is of
particular interest because many euryhaline elasmobranchs are widely
distributed across a range of salinities. These include several species of
stingrays commonly found in FW tributaries and upstream of coastal areas,
including Dasyatis guttata, Dasyatis garouaensis, Dasyatis bennetti
and Dasyatis sephen (Thorson et
al., 1983; Thorson and Watson,
1975; Taniuchi,
1979). Larger elasmobranchs, such as the bull shark (C.
leucas) and the largetooth sawfish (Pristis perotteti) also
frequent FW systems but they continue to utilize the marine environment for
some critical life stages (Springer,
1963; Thorson et al.,
1966; Bass et al.,
1973; Thorson,
1974; Thorson,
1976; Jensen,
1976; Taniuchi,
1979; Snelson et al.,
1984).
The goal of this study was to determine the electroreceptive capabilities
of a euryhaline elasmobranch throughout the range of salinities and hence
conductivities that it would encounter in its natural environment. The
organism selected for this study was the Atlantic stingray (Dasyatis
sabina). This species is locally abundant throughout the primarily
brackish Indian River Lagoon (IRL) system in east Florida, USA, where it is
found over shallow open sand and silt bottoms, associated with sea grass beds
and spoil islands (Snelson and Williams,
1981; Snelson et al.,
1988). It has a broad diet of benthic fauna that primarily
consists of amphipods and mysids (Cook,
1994). The presence of a permanent FW population in the nearby St
Johns River (SJR), FL, USA, provided the opportunity to compare electrosensory
capabilities of populations of the same species that inhabit electrically
dissimilar environments. The SJR population completes its full life cycle in
FW, with no significant differences in size of maturity and reproductive
success compared with marine populations in the nearby IRL and the northeast
Gulf of Mexico (Johnson and Snelson,
1996). To our knowledge, D. sabina is the only marine
elasmobranch that has established a permanently FW population. Johnson and
Snelson (Johnson and Snelson,
1996) hypothesized that the population may have undergone
adaptations to its FW environment, although there are no known morphological
differences between the SJR population and any other marine D. sabina
populations. A comparison of the two populations may provide insight into
possible evolutionary adaptations and plasticity of the electrosensory system
in this species. Therefore, the objectives of this study were to behaviorally
determine the electrosensitivity of the Atlantic stingray to prey-simulating
electric fields in marine (35 p.p.t.), brackish (15 p.p.t.) and FW (0 p.p.t.)
treatments, and to then compare the electrosensitivities of stingrays from the
IRL population with that of the SJR population to determine if permanent
exposure to FW has affected the electric sense in this species.
|
MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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; Snelson et al.,
1988) (D.W.M., personal observation).
|
Stingray collection and maintenance
Stingrays were collected using equipment that avoided any damage to the
electroreceptors (i.e. hook wounds near the mouth). In the IRL, stingrays were
collected between August 2005 and January 2007 using a 183.5 m center-bag
seine. In Lake Harney, stingrays were collected between June 2006 and August
2006 by electrofishing from an airboat. Upon capture, each stingray was sexed,
measured and placed in a live well. Only sexually mature stingrays (>22 cm
disc width) were retained for this study to account for previously described
ontogenetic changes in response properties of the Atlantic stingray's
electrosense (Snelson et al.,
1988; Sisneros and Tricas,
2002).
Stingrays caught in the IRL at salinities less than 7 p.p.t. were assigned
to the FW IR0 treatment (0 p.p.t., =2026 cm), those captured at
salinities between 7.1 and 24.9 p.p.t. were assigned to the brackish-water
IR15 treatment (15 p.p.t., =41 cm) and stingrays captured in
salinities greater than 25 p.p.t. were assigned to the saltwater IR35
treatment (35 p.p.t., =19 cm). A major drought in 2006 resulted
in higher salinities throughout the IRL, which precluded collection of
stingrays for the IR0 FW treatment. As a result, seven brackish water
stingrays were acclimated to FW by decreasing salinity levels by 2 p.p.t.
every 24 h, and were then assigned to the IR0 treatment. Because the SJR was
always fresh, all SJR stingrays were assigned to the FW SJ0 treatment.
All stingrays were maintained in identical 122x244x50 cm fiberglass holding tanks at either the Florida Atlantic University (FAU) Marine Science facility or the Boca Raton campus, FL, USA. The IR35 stingrays were held at the FAU Marine Science facility in marine flow-through aquaria at 23.0–26.8°C. The IR0, IR15 and SJ0 stingrays were held at the FAU Boca Raton campus in closed-circuit flow tanks at 21.3–22.0°C. All rays were fed to satiation once daily on a diet of thawed grass shrimp.
Experimental apparatus
The experimental tank was identical to the holding tank and connected to
the same water flow and filtration system. An opaque 122x213 cm acrylic
plate lay on the bottom of the experimental tank. An identical plate was also
placed in the bottom of the holding tank to replicate the environment of the
experimental tank. Four electric dipoles were equally spaced 40 cm apart from
one another in four quadrants of a 1x1 m square near one end of the
acrylic plate (Fig. 2). Each
dipole consisted of a pair of holes drilled into the plate. The gap distance
between the centers of the dipole openings were 1 cm, which simulated a small
prey item. Under each opening, a water-filled polyethylene tube was mounted
flush to the underside of the acrylic plate to act as a salt bridge. The
polyethylene tubing was 50 cm in length and connected to gold-plated stainless
steel pins terminating from a shielded 18 AWG SO underwater cable (Teledyne
Impulse, San Diego, CA, USA). Each dipole's pair of cables was connected to an
electric stimulator based on Kajiura and Holland's
(Kajiura and Holland, 2002)
design that would produce a prey-simulating dipole electric field. The
electric field produced by the dipole was maintained at a constant intensity
by continuous adjustment of the applied current from 6.9 to 8.3 µA. Current
was randomly delivered to one of the four electric dipoles and was monitored
with a multimeter to be within 0.1 µA of the target intensity. A digital
video camera mounted on a tripod was positioned 1 m above the surface of the
water over the center of the electrode array to record each trial.
|
=2026 cm), 15 p.p.t. (=41 cm) or 35 p.p.t.
(=19 cm) and had been feeding for a minimum of seven days. Prior
to commencement of experimental trials, stingrays were fasted for a minimum of
48 h. One stingray was moved from the holding tank to the experimental tank
and allowed to acclimate for a minimum of 10 min. The stingray was aroused to
feed by placing one piece of thawed shrimp in the experimental tank to elicit
a prey-searching behavior, determined by increased swimming velocity and
turning frequency. Once the stingray ingested the shrimp and began to search
for more food, video recording commenced and the stimulator was switched on to
deliver current to one of the four dipoles. The electric field was maintained
until the stingray was observed to bite at the active dipole, resulting in a
positive response, at which time the stimulator was immediately switched off.
The stimulator was reactivated when the stingray was at least 80 cm away from
the next randomly selected dipole, which represented twice the distance of the
maximum observed response. This procedure was repeated until a positive
response was observed at each dipole or until the stingray no longer showed
interest (defined by either no longer biting at the active dipole or by not
exhibiting a prey-searching behavior), ending the trial. The stingray was then
fed to satiation and returned to its holding tank. Stingrays that did not
exhibit a prey-searching behavior or motivation to feed were subjected to a
second trial under the same experimental conditions.
The IRL stingrays were tested only at the same salinity in which they were captured (i.e. 0, 15, 35 p.p.t.). The SJR stingrays were tested first in FW (0 p.p.t.) then slowly acclimated to 15 p.p.t., increasing the tank salinity by 2 p.p.t. every 24 h. Once acclimated to brackish water and feeding normally for a minimum of one week, trials were conducted and the results constituted the SJ15 treatment. The stingrays were then acclimated to 35 p.p.t. following the same protocol and tested again in saltwater (SJ35 treatment).
Data analysis
Video clips of successful responses were extracted from the source tapes
and edited using the software Final Cut Pro (Apple, Cupertino, CA, USA). All
video clips were renumbered prior to analysis to conceal the treatment and
test salinity, thereby enabling the analysis to be conducted in a single-blind
fashion to prevent bias. From the resultant video clips the frame in which the
stingray initiated an orientation to the dipole was extracted. The point at
which the orientation was initiated was determined by observing one or a
combination of three behaviors: a freeze response, where the stingray rapidly
ceased to undulate its pectoral fins, a flaring out of the pelvic fins to slow
its forward motion or a sudden change in swimming trajectory
(Kajiura and Holland, 2002).
The response frame was contrast adjusted and deinterlaced using the software
Adobe Photoshop (Adobe Systems, Mountain View, CA, USA) to make the stingray's
spiracle more visible. From this frame, the stingray's distance from the
center of the dipole to the point at which the orientation was initiated
(orientation distance) and the angle of the orientation point with respect to
the dipole axis (orientation angle) were quantified using the software ImageJ
(NIH, Bethesda, MD, USA). Orientation distance was measured from the center of
the dipole to the posterior margin of the closest spiracle, which closely
approximates the position of the hyoid ampullary cluster (see supplementary
movie). The responses for each stingray were reviewed by a second analyst in a
single-blind fashion to verify the initiation point for the orientation to the
dipole. The results of both analysts were in agreement within one frame of the
orientation point for all responses.
The orientation distance and angle were incorporated into the ideal dipole
field equation (Griffiths,
1989) to determine the electric field at the point where the
stingray first oriented towards the simulated prey
(Kalmijn, 1982). The ideal
dipole equation states:
 | (1) |
is
the resistivity of the water (the experimental factor, cm), I
is the applied current (6.9–8.3 µA), d is the gap distance
between the centers of the dipole openings (1 cm), r is the measured
orientation distance (cm) and 
is the measured orientation angle with
respect to the dipole axis (deg.). The orientation angle is included in the
equation to account for the cosine dependency of the electric field
(Kalmijn, 1982).
The weakest electric field that elicited a positive response for each
stingray was defined as its best response and used for statistical analysis. A
natural log transformation was applied to the derived electric field values to
meet the assumptions of normality and homoscedasticity
(Ramsey and Schafer, 2002). A
one-way analysis of covariance (ANCOVA) was employed to test for differences
in the minimum detected electric field among the treatments, with disc width
included as the covariate (Dowdy and
Wearden, 1991). All statistical analyses were conducted using SAS
version 8.02 (Cary, NC, USA).
To better illustrate the functional detection range of the stingrays in the
different environments, a two-dimensional detection area around the dipole was
graphically depicted. The detection range was plotted on a 90 deg. polar plot
by calculating r, derived from median E, at all angles from
0–90 deg. () for each environment. This graphical representation
of the detection area around the dipole exemplifies the cosine dependency of
the electric field. This approach was also used to calculate the maximum
detection range using the single weakest electric field for each
environment.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). The SJR stingrays were successfully acclimated from 0 p.p.t. to 15 p.p.t. but experienced high mortality (60%) immediately after the second acclimation period from 15 to 35 p.p.t. Logistical constraints precluded collecting additional stingrays from Lake Harney, resulting in the exclusion of the SJ35 treatment from the analysis.
Electric field detection threshold
Of the 51 stingrays tested, seven were excluded from the analysis due to
lack of motivation to feed during trials. All observed responses entailed
either a straight trajectory into the active dipole followed by a freeze and
pelvic fin flare-out or a single turn in swimming trajectory. The size and
electrosensitivity of the remaining experimental rays is summarized for each
treatment in Table 1. Each
stingray's best response (i.e. lowest electric field) is shown in
Fig. 3. Best responses in all
treatments showed the orientation distance from the dipole decreased as the
stingray approached from a higher angle to the dipole axis
(Fig. 4). The strength of the
electric field differed significantly among the five treatments (ANCOVA;
F5,39=70.79, P<0.0001,
R2=0.90), and the disc width covariate did not
significantly affect the model (P=0.09). A Tukey–Kramer
post hoc test revealed that neither the two FW treatments (IR0
vs SJ0, P=0.99), nor the saltwater vs the brackish
treatments (IR15 vs IR35, P=0.60; IR15 vs SJ15,
P=0.19; IR35 vs SJ15, P=0.84) differed
statistically. However, the median electric field in both FW treatments was
significantly greater than each of the brackish–saltwater (BSW)
treatments (P=<0.0001). The median electric fields in the two FW
treatments (IR0=1.2 µVcm–1, SJ0=1.5
µVcm–1) were greater than the median electric fields for
the saltwater (IR35=0.005 µVcm–1) and two brackish water
treatments (SJ15=0.003 µVcm–1, IR15=0.01
µVcm–1). The weakest electric field detected was 0.0006
µVcm–1 by an IR35 stingray whereas the weakest electric
field in either FW treatment was 0.2 µVcm–1 by an IR0
stingray. These results justified pooling the treatments into two groups: a FW
and a BSW treatment group.
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Prey detection range
Detection ranges were derived for the two pooled environmental groups,
rather than for all five treatments. The point at which the stingray initiated
its orientation to the dipole was plotted using polar coordinates for each
successful response (Fig. 5A).
The median electric fields for the BSW (0.006 µVcm–1) and
FW (1.4 µVcm–1) groups were derived from the best
responses for each stingray in their respective treatment. In the plane of the
dipole axis (0 deg.), the derived median detection distance was 25.03 cm in
BSW and 15.33 cm in FW (Fig.
5B). The maximum detection distance in the plane of the dipole
axis (0 deg.) was also calculated using the minimum electric field value for
each group (BSW=0.6 nV cm–1, FW=0.2
µVcm–1). The derived maximum detection distance was 44.03
cm in BSW and 28.52 cm in FW (Fig.
5B). These values slightly exceeded the maximum observed detection
distance of 38.8 cm at 46.5 deg. in BSW and 24.47 cm at 41.1 deg. in FW.
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|
DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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The Atlantic stingray D. sabina is able to detect and orient towards a prey-simulating, weak electric field across a wide range of salinities, including FW. Interestingly, despite the electric field strength being much greater in FW, the sensitivity of the electrosensory system appears to be reduced. This is evidenced by the detection range and electrosensitivity of the stingrays in both FW treatments being significantly less than those tested in the BSW treatments. The derived median and maximum orientation distances of stingrays tested in FW were reduced by 38.8% and 35.2%, respectively, compared with the combined BSW treatments. Differences in electrosensitivity were even more pronounced, as the stingrays tested in FW required a stimulus intensity of 200–300x greater to elicit a behavioral response. Furthermore, this difference was retained regardless of whether the stingrays were captured from the permanent FW population or the marine estuary. This reduced sensitivity is akin to prey items producing a signal that is 200x `louder' in FW but the stingrays are unable to detect it.
When compared with the IRL stingrays, the FW SJR stingrays did not
demonstrate a significantly enhanced electrosensitivity in FW, nor did they
exhibit a significantly reduced electrosensitivity in brackish water. In fact,
the electrosensitivities did not differ between the two populations in either
FW or brackish water. The response of the FW SJR stingrays that were
acclimated to brackish water, as well as the IRL stingrays caught in brackish
water that were acclimated to FW, were similar to the responses of other
stingrays from both populations that were tested at those salinities without
acclimation. This demonstrates the plasticity of the electrosensory system, as
individuals from one environment transferred to another were able to function
similarly to individuals native to that environment. To minimize the stress of
the acclimation process, prevent osmotic shock and maintain normal feeding
behavior, the stingrays were slowly acclimated to the test salinity (±2
p.p.t. day–1) and then held at the test salinity for a
minimum of one week. Previous studies subjected stingrays collected from the
SJR to faster rates of acclimation up to 32 p.p.t. but the effects of the
rapid acclimation on feeding behavior are unknown because the stingrays were
food-deprived throughout the one-month trial
(Piermarini and Evans,
1998).
The electrosensitivities determined for the BSW stingrays are consistent
with previous studies that tested other elasmobranch species in marine
environments with a similar experimental apparatus. Small smooth dogfish
(Mustelus canis) initiated responses to prey-simulating electrical
stimuli of <2 nV cm–1 from >35.6 cm
(Kalmijn, 1982). Juvenile
scalloped hammerhead sharks (Sphyrna lewini) and sandbar sharks
(Carcharhinus plumbeus) demonstrated minimum electrosensitivities of
0.4 nV cm–1 and 0.5 nV cm–1 and maximum
detection distances of 30.6 cm and 31.6 cm, respectively
(Kajiura and Holland, 2002).
Neonatal bonnethead sharks (Sphyrna tiburo) responded to electric
fields of <1 nV cm–1 from a maximum detection distance of
22 cm (Kajiura, 2003). Direct
comparison of the results of FW stingrays with the results of other FW
elasmobranchs is limited due to a lack of quantified physiological or
behavioral sensitivities of the electrosensory system in previous studies.
Szabo et al. (Szabo et al.,
1972) reported that the obligate FW stingray Potamotrygon
circularis exhibited a minimum behavioral threshold of 120
µVcm–1 whereas Szamier and Bennett
(Szamier and Bennett, 1980)
reported the threshold sensitivity of Potamotrygon to be 1 mV.
Whitehead (Whitehead, 2002)
reported that bull sharks initiated all responses from >15 cm but did not
report a maximum detection distance or behavioral threshold sensitivity.
Although the sensitivity of the FW stingrays in this study is greater than
these other species, it is still several orders of magnitude lower than any
other marine elasmobranch.
|
cm
and FW resistivity of 2026 cm). Each equipotential represents an order
of magnitude difference in both seawater and FW treatments. The model clearly
illustrates that the voltage decreases much more dramatically with distance
from the source in seawater compared with FW. For the maximum demonstrated
detection distance (
40 cm) the electric field decreases by five orders of
magnitude in seawater compared with only three orders of magnitude for that
same distance in FW (Fig. 6A).
The electric field strength drops much more quickly with distance in seawater
(Fig. 6B). In essence, the
electric field is being grounded in seawater whereas the electric field
maintains its strength over a greater linear distance in the resistive FW
environment, resulting in a much smaller voltage change with distance. So
although the absolute voltage is greater in FW, the slope is much smaller.
Therefore the relevant stimulus to the electrosensory system may be the
relative change in voltage, rather than a minimum threshold.
The modeled dipole illustrated in Fig.
6 demonstrates that the electric field is directly proportional to
resistivity (Kalmijn, 1982).
In this study, the difference in mean resistivity between the saltwater
(=19 cm) and FW (=2026 cm) treatments was
approximately 100x, which should result in a proportional 100x
difference in electric field sensitivity. However, median electrosensitivity
was more than 200x greater in the BSW treatments (6.0 nV
cm–1) than in the FW (1.4 µVcm–1)
treatments. The disparity indicates that the reduced sensitivity in FW is not
solely due to the electrical properties of the water but is due in part to
biological differences when detecting electric fields in FW vs BSW
environments.
Unlike the obligate FW Potamotrygonid stingrays, which have undergone
dramatic morphological changes to their electrosensory system, the euryhaline
elasmobranchs retain a marine electrosensory morphology characterized by long
subdermal canals. The long canals have been convincingly argued to act like an
antenna and provide the ampullae with the voltage difference along the length
of the canals, at least in a marine environment
(Brown et al., 2005). This is
based upon a calculation of the path resistance along the length of a canal,
which is much higher than the resistance between epidermal pores on the
surface of the body. Using the same parameters and equations as Brown et al.
(Brown et al., 2005), the canal
resistance was calculated to be 160x greater than the pore-to-pore
resistance in seawater; the same value they achieved. However, in FW with a
resistivity of 2000 cm–1, the canal resistance is
only slightly greater (1.6x) than the pore-to-pore resistance. This may
effectively reduce the typical antenna-like role and allow the canals to
function as a cable and conduct the pore voltage to the ampullae. However,
this calculation is predicated upon the glycoprotein gel in the canals
possessing the same resistivity in both FW and seawater environments –
an assumption that remains to be tested. If this assumption is correct, the
reduced ability of the ampullary system to function in FW could account for
the observed reduction in sensitivity. The cable-like function of the canals
in FW reduces the contrast in signals detected by the hundreds of
electroreceptors across the sensory array
(Kalmijn, 1974;
Brown, 2002). Furthermore, the
high external resistivity of FW results in a transcutaneous voltage
difference, which effectively diminishes the demonstrated advantage of the
varied ampullary canal geometry (Kalmijn,
1974; Camperi et al.,
2007).
The reduction in sensitivity of the Atlantic stingray's electrosensory
system in FW does not necessarily equate to a decrease in function. All FW
stingrays were able to detect, localize and successfully bite at the
prey-simulating stimulus, some from distances in excess of 15 cm. The FW
population of Atlantic stingrays in the SJR completes their entire life cycle
in FW (Johnson and Snelson,
1996), which represents the strongest evidence that the
electrosensory system continues to function effectively in FW.
Despite their permanent exposure to FW over the past 100,000 years
(Cook, 1939), the SJR stingrays
did not demonstrate an enhanced electrosensitivity in FW, nor did they exhibit
reduced sensitivity when reintroduced to higher salinities. Stingrays from
both populations responded similarly to the prey-simulating stimulus when
tested in similar salinities, regardless of from where they were collected in
the wild. The plasticity of this sensory system to function in such diverse
environments demonstrates its adaptive significance.
|
Acknowledgments |
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|
Footnotes |
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|
References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Brown, B. R. (2002). Modeling an electrosensory
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Brown, B. R., Hutchinson, J. C., Hughes, M. E., Murray, R. W. and Kellogg, D. R. (2002). Electrical characterization of gel collected from shark electrosensors. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 65,061903 .[Medline]
Brown, B. R., Hughes, M. E. and Russo, C. (2005). Infrastructure in the electric sense: admittance data from shark hydrogels. J. Comp. Physiol. A 191,115 -123.[CrossRef][Medline]
Camperi, M., Tricas, T. C. and Brown, B. R. (2007). From morphology to neural information: the electric sense of the skate. PLoS Comput. Biol. 3, 1-14.[CrossRef]
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= all
response points for BSW group; 
= best response points for each
stingray in the BSW group; 
= all response points for FW group; • =
best response points for each stingray in the FW group). (B) The derived
detection range as the median detection distance (dashed line) and the maximum
detection distance (dotted line). See text for further details.