Response of juvenile scalloped hammerhead sharks to electric stimuli

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ARTICLE IN PRESSS.M. Kajiura, T.P. Fitzgerald / Zoology 112 (2009) 241–250 247(Griffiths, 1989; Kalmijn, 1982a). The variables include:r is the resistivity of the seawater (O cm), I is the appliedelectric current (A), d is the electrode separation distance(i.e. distance between positive and negative poles of thedipole) (cm), r is the radius (i.e. distance from the centerof the dipole to the position in space for which thepotential is being calculated) (cm) and y is the anglefrom the position in space to the center of the dipolewith respect to the dipole axis. This equation describesthe voltage in half space, with the electrodes mounted tothe base of an insulating plate such that the conductingmedium is a hemisphere above the electrodes (Kalmijn,1982a). From this equation, it is apparent that thevoltage (V) varies as an inverse square of distance (r).The voltage also varies as a function of angle withrespect to the dipole axis, being maximal in the plane ofthe dipole axis (01) and decreasing as a cosine functionto a theoretical null in the perpendicular plane (901).The empirically measured values closely matched thecalculated ideal values for both components (Fig. 3).Although it was the voltage that was directlymeasured in these experiments, it is thought thatelasmobranch electroreceptors act as voltage gradientdetectors (Kalmijn, 1971, 1974, 1978, 1988). The voltagegradient, or electric field (E), is the spatial derivative ofthe voltage and hence has the units V m 1 . For an idealdipole, the voltage gradient varies not as an inversesquare, but as an inverse cube with distance. A cosineangular dependency is retained granting the greatestelectric field intensity in the plane parallel to the dipoleaxis with a minimal field strength in the perpendicularplane (Griffiths, 1989; Denny, 1993). For each experimentaltrial, the appropriate values of distance (r) andangle (y) were used to determine the electric fieldintensity at the point where the shark initiated itsorientation to the dipole. The close concordancebetween the measured and calculated values confirmsthat the response thresholds calculated for the sharksbased upon distance (r) and angle (y) accuratelyrepresent the actual field intensities encountered by thesharks. There is also behavioral evidence to support thatthe electric field intensity is greatest in the plane parallelto the dipole axis. Both scalloped hammerhead andsandbar sharks initiate orientations from a greaterdistance at small axis angles and need to be closer tothe dipole to demonstrate a response when they are inthe orthogonal plane (Kajiura and Holland, 2002).The equation used to model the electric field intensityassumes that the orientation distance exceeds that of theelectrode separation distance (r4d) (Kalmijn, 1982a;Denny, 1993; Benedek and Villars, 2000). This assumptionhas been accepted in other studies of elasmobranchelectroreception (Kalmijn, 1982a; Johnson et al., 1984;Kajiura and Holland, 2002; Kajiura, 2003) and issufficient for the resolution obtained in this study. Thatis, since the head of the shark is large with respect to thedipole separation distance, and it is covered withthousands of electroreceptor pores (Kajiura, 2001),there is no single point along the head that can betaken as the detection point. Therefore, the calculatedfield intensity should be used as an approximation andnot a definitive measure of threshold sensitivity. Thevalue of this technique lies in its ability to comparerelative field intensities rather than determiningthe absolute sensory capabilities which would bebest addressed by using neurophysiological techniques(Tricas and New, 1998).This study chose the point along the side of the headthat was closest to the center of the dipole as the pointused to calculate the electric field intensity. This isparticularly important for sphyrnid sharks in which thedistance from the lateral margin to the center of thehead can be large. Therefore, if the measurement hadbeen taken to the center of the head it would increase theorientation distance by several cm yielding a greatersensitivity value. Ideally, measurements should be takento the actual location of the electroreceptor ampullaewithin the head. However, in S. lewini, most electroreceptorson the lateral margins of the head converge inthe large infraorbital cluster which extends along muchof the width of the cephalofoil (Chu and Wen, 1979).This precludes measuring to a single point within thecluster which is why the more conservative estimate ofthe periphery of the head was chosen.Behavioral responseThe fact that the sharks bit at the dipoles attests to theadequacy of the stimulus to represent prey. The sharksinitiated orientations from distances in excess of 40 cmand demonstrated their ability to precisely locate thedipole source by biting only when directly over thecenter of the dipole. The non-active (control) electrodeswere never bitten even though they were visuallyidentical to the activated electrodes. In addition, thefood odor that diffused throughout the pen served onlyto arouse the sharks and did not present a point stimulusfor orientation. Indeed, the sharks never bit at the odorsource on the acrylic plate.Two parameters, electrode separation distance andapplied current strength, were independently manipulatedto test for differences in orientation distance todifferent stimulus conditions. The 1, 3 and 5 cm dipolessimulated small, medium and large prey items for thissize of shark and the electric current strengths, from 5.0to 50.0 mA, were used to generate prey-simulating, weakelectric fields similar to the 50–500 mV fields measuredaround crustaceans and teleosts (Kalmijn, 1974).A given electric field intensity will occur at a greaterdistance from the center of the dipole when theseparation distance between the poles is increased, thus
248ARTICLE IN PRESSS.M. Kajiura, T.P. Fitzgerald / Zoology 112 (2009) 241–2505µA1cm5µA5cm5µA1cm50µA1cm5.4cm5.4cm1.0µV12.0cm1.0µV16.9cm1.0µV1.0µVFig. 6. Diagrammatic representation of how electric fieldintensity varies with changes in dipole separation and appliedcurrent strength. Any given voltage (V) will occur at a greaterdistance from the center of the dipole when (A) dipoleseparation is increased and current strength is constant; orwhen (B) current strength is increased and dipole separation isconstant. In (A), the applied electric current is held constant at5 mA for dipole separations of 1 and 5 cm creating DC dipolemoments of 5 and 25 mA cm, respectively. A voltage of 1.0 mVis produced at 5.4 cm from the center of a dipole with a 1 cmseparation distance. That same voltage (1.0 mV) occurs at adistance of 12.0 cm from the center of a dipole with a 5 cmseparation distance. Therefore, increasing the electrode separationfrom 1 to 5 cm would more than double the possibledetection distance in this example. In (B), the dipole separationis held constant at 1 cm for applied current strengths of 5 mAand 50 mA. A voltage of 1.0 mV is produced at 5.4 cm from thecenter of a dipole that has an applied current strength of 5 mA.That same voltage (1.0 mV) occurs at a distance of 16.9 cmfrom the center of a dipole that has an applied current strengthof 50 mA. Therefore, increasing the current strength from 5.0 to50.0 mA would provide a three-fold increase in possibledetection distance. Both of these examples assume a seawaterresistivity of 18.0 O cm, and an orientation angle of 01.creating a greater DC dipole moment (Fig. 6A).Therefore, it was predicted that for a given electric fieldintensity (E) the sharks would orient to a dipole from agreater distance (r) when the separation between thepoles (d) was increased: ((Ep(d/r)). Thus the sharks willencounter a given electric field intensity at a greaterdistance from the center of the dipole when the electrodeseparation is increased (Fig. 6A). The prediction ofincreased orientation distance with increased dipole sizewas supported by the data. The sharks oriented from asignificantly greater distance when exposed to a 5 cmdipole compared to a 1 cm dipole (Fig. 4).Although the sharks oriented from a significantlygreater distance when the electrode separation distancewas increased, if the electrode separation distanceexceeds the size of a natural prey item the sharks mightnot interpret the larger electric field as prey (Fitzgerald,2002). Therefore, the behavior of the sharks may beinfluenced by their perception of the stimulus and theymight not respond as predicted if the parameters areextrapolated beyond certain limits. For instance, if theelectrode separation is exceedingly large, the sharksmight not bite at the dipole but might actually berepelled. Because this study examined only preysimulatingstimuli, this hypothesis invites further investigation.A given electric field intensity will also occur at agreater distance from the center of the dipole when theapplied current strength is increased (Fig. 6B). Therefore,if sharks respond by orienting to the dipole whenthey detect some threshold electric field intensity (E), itwas predicted that the sharks would orient from agreater distance (r) when exposed to dipoles of aconstant size but with greater applied current strengths(I): (Ep(I/r)). The prediction of increased orientationdistance at greater applied current strength was alsosupported by the data (Fig. 5).The range of electric currents used in these experimentswas chosen based upon literature values that hadsuccessfully elicited feeding behavior by various elasmobranchspecies (Kalmijn, 1971, 1978, 1982a; Johnsonet al., 1984; Kajiura and Holland, 2002; Kajiura, 2003).The applied currents were constrained within a rangeknown to be stimulatory to the sharks, therefore it is notsurprising that the sharks responded as predicted byinitiating feeding orientations at successively greaterdistances with increased applied current. However, thecorrelation of orientation distance with applied currentmust be qualified by recalling that the nature of theresponse is dependent upon the shark perceiving thestimulus as prey. If the stimulus is not perceived as prey,the shark may detect the electric field but not bite at it.Alternatively, a shark that detects and orients to anelectric field at a distance may abandon that orientationonce the stimulus strength no longer resembles that of aprey item. Although the sharks would theoreticallyrespond from a greater distance at higher currentstrengths, their behavior might differ from that predictedby simply scaling the model.Threshold sensitivityIt was predicted that the sharks would demonstratethe best response to stimuli that most closely matchedtheir natural prey items. Although a variety of preyitems of different sizes are found in the stomach ofjuvenile hammerhead sharks in Kaneohe Bay, the mostcommon prey items are benthic shrimp (Family:Alpheidae) and gobies (Family: Gobiidae) (Clarke,1971; Bush, 2003). Both of these prey items are mostclosely approximated in size by the 1 and 3 cm dipoles.
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Response of juvenile scalloped hammerhead sharks to electric stimuli

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