Marine Biology (1994) 120:161-169
9 Springer-Verlag 1994
C. G. Lowe 9R. N. Bray 9 D. R. Nelson
Feeding and associated electrical behavior
of the Pacific electric ray Torpedo californica in the field
Received: 26 January 1994 / Accepted: 27 January 1994
Abstract The predatory behavior of 74 Pacific electric
rays (Torpedo californica), studied between August and
December during 1988 through 1991 in situ off the Palos
Verdes Peninsula, southern California, consisted of two
feeding modes: an ambush from the substratum during the
day and a more vigorous attack from the water column at
night. Predatory motor patterns and electric organ discharges (EODs) were recorded on the video and audio
channels of a housed camcorder. Predatory motor patterns
included four phases: (1) jump (simultaneous with EOD
initiation), (2) pectoral-fin cupping, (3) orientation to prey,
and (4) ingestion. The initial electrical activity of the rays
was a train of 46 to 414 5-ms monophasic EODs that lasted
0.45 to 7.06 s; the maximum number of EODs produced
during an attack was >1200. Maximum output, measured
on only one ray, was 45 V. Fifty-five rays were presented
one of four types of prey stimuli: live fish (LF), freshlyspeared fish (FSF), frozen fish (FF), or a simulated bioelectric field (SBF). The percent frequency of attacks for
the LF, FSF, and FF treatments ranged from 70 to >90%,
but was <30% for the SBF. The interval between prey presentation and attack was =30 s for the LF, FSF, and FF and
over five times longer for the SBF; intervals averaged
<4 s for the three rays tested at night. Attacks by rays on
energized electrodes provide the first evidence that electric
rays use electroreceptors to detect their prey. However, the
lack of clear differences among the four prey treatments in
five characteristics of the initial pulse train suggests that a
suite of sensory stimuli cooperate in triggering an attack
and regulating the electrical output during the attack.
Communicated by M. Strathmann, Friday Harbor
C. G. Lowe1 9R. N. Bray2 ([]) 9D. R. Nelson
Department of Biological Sciences,
California State University, Long Beach,
California 90840-3702,
USA
Present addresses:
1 University of Hawaii at Manoa, Department of Zoology, Honolulu, Hawaii 96822, USA
2 Biology Program, California State University, San Marcos, California 92096, USA
Introduction
Electric rays (family Torpedinidae) are one of only two
groups of strongly electric fishes found in the marine environment (Bennett 1971). Studies to date indicate that rays
of the genus Torpedo are piscivorous and produce electric
discharges while attacking prey (e.g. Bray and Hixon
1978). Attacks from the substratum in aquarium observations typically start with a "jump" over the prey and a simultaneous train of EODs (Belbenoit 1970, 1986, Belbenoit and Bauer 1972). The predatory behavior varies considerably, presumably due to differences in the chain of
events during an attack, stimuli emitted by prey, and age
of the ray (Belbenoit 1986). An added complication of laboratory observations, however, is that stress incurred during capture and maintenance and the artificial nature of the
laboratory environment may affect the behavior and
electrical activity of the rays (e.g. Bennett et al. 1961;
Pfeiffer 1961).
The only field observations on the predatory behavior
of electric rays indicate that they actively seek prey at night
(Bray and Hixon 1978). Diver surveys over a rocky reef in
southern California indicated that Pacific electric rays
(Torpedo californica) were far more common swimming
above the reef at night than during the day. Rays aggressively attacked and consumed speared fish presented to
them, and Bray and Hixon concluded that the rays were actively hunting for reef fish exposed but quiescent at night.
A tracking study of Pacific electric rays using ultrasonic
telemetry provides additional evidence that Pacific electric
rays swim about mainly at night (Bray, Lowe, and Nelson
in preparation).
The purpose of this study was to quantify electrical activity during predatory attacks of previously undisturbed
Pacific electric rays in the field. Field measurements of the
electrical activity of electric rays have not been reported
and we were interested in whether measurements made
from laboratory studies were conservative. Additionally,
since electric rays may feed mainly at night or in turbid
water (Pfeiffer 1961; Bray and Hixon 1978), we were inter-
162
e s t e d in h o w t h e y d e t e c t and e v a l u a t e t h e i r prey. W e varied the n a t u r e o f p r e y s t i m u l i b y p r e s e n t i n g r a y s w i t h either l i v e , f r e s h l y - s p e a r e d , or f r o z e n f i s h or a s i m u l a t e d bio e l e c t r i c field, and r e c o r d e d the s u b s e q u e n t m o t o r p a t t e r n s
and e l e c t r i c a l a c t i v i t y o f the rays.
Materials and methods
Our study site was Abalone Cove at Palos Verdes Peninsula in southern California (33~
118~
The cove consists of a cobble beach, a subtidal rocky reef with attached giant kelp (Macrocystis pyrifera), and an offshore sand flat. We made most of our observations over the sand flat, beginning at the outer margin of the reef
at a depth of 8 to 12 m and extending to a depth of = 23 m. Rays (Torpedo californica) were in 10 to 15 m of water and usually buried in
the sand during the day and swimming in the water column at night.
Tests were conducted between August and December during 1988
through 1991. After testing, each ray was measured (total length) to
the nearest 10 cm using a calibrated pole, sexed, and tagged with a
color-coded spaghetti dart tag; the tagging ensured that each ray was
tested only once.
EOD waveform measurements
The waveforms of the electric organ discharge (EOD) produced by
the rays during predatory events were recorded with a Tektronics
model 214 storage oscilloscope in a watertight housing. We used two
types of recording electrodes for measuring EODs underwater: a
fixed dipole, with positive and negative poles spaced 20 cm apart,
to measure the voltage of the electric fields created by the ray's EODs;
and an adjustable caliper dipole, clamped directly on the dorsal and
ventral surfaces of the electric organ to measure the maximum voltage output of rays. Both electrodes were stainless steel rods, 2 mm
in diameter. The voltage drop through the electrodes was negligible
when in direct contact with a known voltage source in a seawater
tank. We conducted tests only on previously untested and undisturbed
rays found buried in the sand during the day. Male and female rays
between 60 and 110 cm were presented with live and freshly-speared
reef fish ranging from 15 to 20 cm (standard length, SL). Speared
fish, impaled on the positive electrode pole, were presented within
10 cm of the anterior margin of the ray's disk and were moved back
and forth in front of the ray until a response was elicited. Following
each response, waveform information (amplitude, polarity, EOD duration, and EOD shape) was transcribed underwater from the oscilloscope screen to a slate.
Table 1 Torpedo californica. Stimulus characteristics of the four
different prey treatments (P present; P§ present at increased
strength). Elevated electrical strength of FSF based on research by
Kalmijn (1972)
Prey treatment
EOD pulse-train measurements
We recorded the electrical and behavioral patterns produced by rays
with an underwater video camera (a housed Sony CCD-V3 8 mm
camcorder). The system was fitted with a monopole electrode connected through a voltage splitter to the audio channel, thus providing a simultaneous record of rays' movements (video) and EODs (audio) during a predatory attack. For each test, the monopole recording electrode was placed =10 to 20 cm above the dorsal surface of
an electric organ just before the prey stimuli were presented.
We used four different treatments representing various prey stimuli to study how rays detect their prey (Table 1). Previously undisturbed male and female rays were randomly presented either live
(LF), freshly-speared (FSF), or frozen then thawed (FF) fish, all
measuring 15 to 20 cm standard length and commonly found around
rocky reefs in southern California. These species (Rhacochilus vacca, Embiotoca jacksoni, Phanerodon furcatus: Embiotocidae; Halichoeres semicinctus, Oxyjulis californica: Labridae; Chromis punctipinnis: Pomacentridae; and Medialuna caIiforniensis: Kyphosidae)
were either caught by hook and line and lightly anesthetized with
MS-222 (LF treatment) or speared with a pole spear (FSF treatment);
the fish used during a particular trial depended on its immediate availability. For the LF treatments, each fish was tethered with 20-poundtest monofilament nylon line to a 1 m plastic rod, allowing us to move
the prey to within 10 cm of the anterior margin of the ray's disk. We
also examined the ray's response to a simulated bioelectric field
(SBF). The SBF generator, modified from a design used by Kalmijn
(1978), produced an 8 gA DC current across a 5 cm dipole. The apparatus had two sets of salt-bridged dipole electrodes (stainless steel,
1.5 mm diam), 50 cm apart, and a three-way switch. During a trial,
only one set of electrodes, randomly chosen, was energized. This enables us to control for the visual and mechanical stimuli also produced by a moving electrode.
The audio portion of each test was printed out on a Gould Mark
220 high-speed oscillographic chart recorder and then digitized with
a digitizing tablet for measurement of time intervals between individual EODs. From these intervals, we determined total train length
and total number of EODs within the train. We limited some analyses to the initial part of the total sequence of EODs because of the
likelihood of experimenter-induced artifacts during subsequent
EODs. The end of the initial pulse train was defined as the first 80 ms
gap between consecutive EODs. We computed instantaneous pulse
rates as the reciprocal of the time interval between adjacent EODs;
from these data, we then computed the average and maximum instantaneous pulse rate within the initial train. Since diving logistics
resulted in small sample sizes and unbalanced design, which could
result in inaccurate probability (p)-values, we compared the
p-values of parametric analyses with those computed from comparable randomization tests using 10 000 reshufflings (Sokal and
Rohlf 198I, Crowley 1992); the two p-values always agreed within
0.01.
Results
Response
Visual Mechanical
Electrical Chemical
voluntary a twitch
Live fish (LF)
P
Freshly-speared
fish (FSF)
P
Frozen fish (FF) P
Simulated bioelectric field
(SBF)
P
P
P
P
P
P+
P+
P
a Swimming movements of body and fins
A total o f 74 Torpedo californica w e r e t e s t e d b e t w e e n A u g u s t and D e c e m b e r d u r i n g 1988 t h r o u g h 1991. F e m a l e
rays were significantly longer than males (females: s =
88_+12 c m (+1 S D ) ; m a l e s : 2 = 7 9 + 6 c m ; S t u d e n t ' s t-test
t = - 3 . 3 4 , d f = 7 2 , p = 0 . 0 0 3 ) , but w e r e less c o m m o n (19
f e m a l e s , 55 m a l e s ; G - t e s t G = 18.28, df= 1, p < 0 . 0 0 1 ) .
EOD waveform characteristics
E O D w a v e f o r m s w e r e r e c o r d e d f r o m 11 o f the 13 rays that
w e r e p r e s e n t e d f r e s h l y - s p e a r e d p r e y (the o t h e r t w o r a y s
163
did not attack). Individual EODs consisted of a DC pulse
with a rapid rise to peak and slow decay to baseline; the
dorsal surface of the electric organ was always positive and
the ventral surface negative. Pulse durations ranged from
4 to 5 ms (Y = 5 +0.5 ms). The amplitude of the waveforms
varied greatly, ranging from 0.02 to 0.50 V cm -1 (~ = 0.17
_+0.18 V cm -1 , n = 11). There was little correlation between
EOD amplitude and total lengths of rays ( r = - 0 . 1 0 , p =
0.768). The large variation in amplitude measurements is
at least in part due to our difficulty in placing the dipole
electrodes at a consistent distance and orientation from the
rays.
Only one ray was tested for m a x i m u m electric organ
output using the caliper electrodes. The m a x i m u m voltage,
measured by clamping the caliper electrodes on the dorsal
and ventral surfaces of the ray's electric organ, was 45 V,
with a waveform similar to those observed in the other tests.
Predatory motor patterns
Daytime predatory motor patterns of rays showed stereotyped chains of behaviors similar to those described by Belbenoit ( 1981). Of the 10 ray s presented live tethered prey,
8 were initially buried in sand (e.g. Fig. 1 A, C) and two
were swimming (e.g. Fig. 1 B, G). Predatory behaviors
started with a jump over the prey (Fig. 1 D) (simultaneous
with initiation of the EODs), followed by pectoral-fin cupping around the prey (Fig. 1 E, H), orientation of the ray
so that it could grasp the fish head first (Fig. 1 F, I - J ) , and
final ingestion of the prey whole. All 10 rays presented
with live fish initiated their attacks with a jump over the
prey (Fig. 2); however, 4 of the rays missed or apparently
lost sensory contact with the prey after the initial jump (Fig.
2 e, f, g, j). Pectoral-fin cupping and orientation behavior
immediately followed a jump in 9 of the 10 cases, with durations depending on the time required for manipulation of
the prey for ingestion. Two of the ten rays apparently had
difficulties in handling prey because of interference with
the tether; they stopped their attacks and swam away without ingesting the fish (Fig. 2 a, h).
In one instance, we inadvertently presented two prey to
one ray (Fig. 2j). The closer fish, a halfmoon (Kyphosidae: Medialuna californiensis), was still subdued because
of the anesthetic while the farther fish, a black perch (Embiotocidae: Embiotocajacksoni), was alert and swimming
from the ray's left to right side. The ray jumped toward the
black perch, turning to its right as the fish passed. At the
beginning of the jump, the ray produced a burst of EODs
that immobilized the black perch (Fig. 2j: Ja); however,
the ray over-jumped the fish and ceased the attack. The ray
jumped 20 s later toward the halfmoon (J2), just missing
it. The ray jumped again 03) and landed on the immobilized black perch, ingesting it 01) after 30 s of pectoral-fin
cupping. The ray then attacked the subdued halfmoon with
a slow jump (J4). The fish was accidentally pulled away
because the tether line became tangled. The ray then produced the most intense EOD burst observed, followed the
fish into the water column, and ingested it (I2). The ray al-
Fig. 1 Torpedo californica. Positions and motor patterns of Pacific electric rays before and during daytime predatory attacks. A Ray
buried in sand with its head to right. B ray swimming within 1 m of
bottom; white-tipped rod in diver's left hand is electrode connected
with a wire to audio channel of the camcorder, black-tipped rod in
right hand was used to position a tethered fish (beneath ray's disk,
out of sight). C - F predatory sequence of 80 cm male ray, initially
buried in sand, attacking a 17 cm standard length (SL) blacksmith
(Chromispunctipinnis; Pomacentridae); C prior to attack, ray's head
was directly facing camera and prey swam in from the ray's left;
D - E jump with a simultaneous turn to ray's left using thrust from
tail fin; F orientation to prey and ingestion; timings after initiation
of attack were D = 0.3 s, E = 0.5 s, F = 0.8 s. G - J predatory sequence
of 70 cm male ray, initially swimming 2 to 5 cm above bottom, attacking a 21 cm SL black perch (Embiotoca jacksoni; Embiotocidae); H late jump and early envelopment stages; I - J envelopment
and orientation; timings after initiation of attack were H=l.8 s,
I=2.6 s, J=3.4 s (from 8 mm video frames)
164
Fig. 2 Torpedocalifornica.
Pulse profiles and associated
motor patterns of ten Pacific
electric rays presented live fish
on a tether; rays are ordered by
increasing time length of predatory attack. Symbols above
pulse profiles represent time
course of motor events, where
J(1-4) = a jump over the prey,
M = ray missed prey during
jump, horizontal bar = duration
of pectoral-fin cupping and
orientation, and I(t - 2) = point of
ingestion (EODs electric organ
discharges)
If
I
200 -
J
z"
-~M(
J2
100
I
200
100
I
,0
C
\
I
200
i JJ
~100
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30
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..[
4O
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50 s 60
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10 20 30 z.O 50 s 60
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J2
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ways directed its jump toward the most active fish. It took
the ray =2 min to attack and consume both fishes.
In all trials, the initial EOD occurred at the beginning
of the jump and the discharge train usually continued into
the pectoral-fin cupping phase (e.g. Fig. 2). Of the 35 rays
that attacked prey, 22 continued to discharge at a slower
and more variable rate during the orientation and ingestion
phases than during the jump phase; 13 stopped the attack
40
Time
8O
tL
s 120
during various portions of the first three phases and either
swam away immediately or stopped searching for the fish
after several minutes. The frequency of EODs at the start
of the trains was typically 150 to 200 EODs s-1 and d e creased over time (Fig. 2).
We observed the same predatory attack phases during
the three night tests except that the rays were either swimming or drifting in the water column 1 to 2 m above the
165
substratum. Rays lunged forward at prey with a motor pattern similar to a jump and then cupped their pectoral fins
around the prey. At this point, rays would either pin the
fish to the bottom or go into a spiral or forward-rolling maneuver, depending on the ray's distance above the substratum; these behaviors led to orientation and ingestion of the
prey. Additional details of predatory behavior of electric
rays at night are described in Bray and Hixon (1978).
100
\
E
8
We compared the time interval between prey presentation
and attack for the 36 rays that attacked prey stimuli (LF:
10, FSF: 15, FF: 7, SBF: 4). There was a significant difference in latency time among the four prey treatments
(one-way ANOVA; F=15.30; df--3,32; p<0.001). Although rays responded to the three fish treatments at approximately the same mean latency, rays took five times
longer to respond to the SBF treatment (Fig. 3 b).
Since previous observations by Bray and Hixon (1978)
suggested that rays actively seek prey at night, we predicted that latency time would be lower at night. Only three
Ingestions
L
50
o
2oo
c
o
W IO0
Frequency of attacks and ingestions
Latency of attack
~
13_
Comparison among prey stimuli
We presented one of the four prey treatments to 55 rays
that ranged in total length from 60 to 100 cm (Y=79.9+
7.9 cm). The number of rays receiving the LF, FSF, FF, and
SBF stimuli was 11, 19, 10, and 15, respectively. The total lengths of rays among the four stimuli groups were similar (one-way ANOVA); F - 1 . 0 3 , df=3,49; p=0.388).
Thirty-six of the rays attacked the stimuli within 4 rain of
presentation; the remaining 19 did not attack and eventually swam away. Water temperatures during the experiments ranged from 13 to 18 ~ (Y = 15.4+ 1.9C ~ and differed significantly among the four prey treatments (oneway ANOVA; F = 4.47, df= 3,22; p = 0.014). Water temperatures were lower during the FSF presentations (Y=
13.3 ~ than the three other treatments [SBF: 15.6, LF:
15.9, FF: 16.3 ~ Tukey's honest-significant difference
(HSD) test, p < 0.05].
The frequency of attacks differed significantly among
the four prey stimuli (G-test, G = 15.03, df=3, p=0.002;
Fig. 3 a). The attack percentage for the SBF treatment was
<30% while those for the other treatments ranged from 70
(FF) to 91% (LF); when the SBF treatment was removed
from the analysis, the differences in attack frequency
among the three remaining treatments were not significant
(G= 1.56, df= 2, p = 0.459). Of the rays that attacked, the
frequency of ingestions also differed significantly among
the three fish stimuli (omitting SBF; G-- 10.4, df=2, p=
0.006; Fig. 3 a). Ingestion percentage was lowest for FF
(14%) and was identical for LF and FSF (80%). All three
rays presented fish prey at night responded with a predatory attack; of these, two rays ingested the fish.
~Attacks
oi
6
~q
0
G
&oo
0
W
d 200
Z
o
%
,9,
120
80
4O
'r
If
300
200
O
LU
loo
LF,
FSF
FF
Treatments
SBF
Fig. 3 Torpedocalifornica. Summary of predatory attacks and associated electrical activities of rays receiving 1 of 4 prey stimuli (LF
live fish; FSF = freshly-speared fish; FF frozen fish, SBF simulated bioelectric field), a Percentage of attacks out of all rays presented treatments (openbars) and percentage of ingestions out of all rays
that attacked (hatched bars); b latency between stimulus presentation and jump; c - f are for initial pulse train only: c duration,
d number of EODs, e average pulse rate, f maximum instantaneous
pulse rate. Bars represent means + 1 SD
rays were tested at night with the monopole electrode (one
with live fish and two with freshly-speared fish), so we
pooled daytime LF and FSF treatments to allow for a
d a y - night comparison of latency times. The rays did respond more quickly at night (2 = 3.6 + 1.2 s, n = 3) than during the day (Y =28.9+28.4 s, n = 25); these differences in
latency were statistically significant [Student's t-test, t=
2.52, df= 26, p (one-tailed) = 0.009].
166
Pulse-train characteristics
We obtained usable pulse-train data on 26 rays (LF: 10
rays, FSF: 6, FF: 6, SBF: 4). Total lengths of these rays
ranged from 70 to 100 cm (Y=81.2+7.1 cm) and did not
differ significantly among the four treatments (one-way
ANOVA; F = 1.66; df= 3,22; p = 0.204).
The total number of EODs produced during predatory
attacks ranged from 46 to 1234 (y = 282.6 +231.3 EODs)
and occurred over intervals ranging from 0.45 to 128.2 s.
Some of this variation was due to experimenter influence.
For example, we observed that the duration of the entire
pulse train could be lengthened if the diver continued to
move the tethered fish during an attack. The initial pulse
train, however, was unaffected by these artifacts. As a result, we restricted our comparison among treatments to the
characteristics of the initial pulse trains during an attack.
The length of the initial pulse trains ranged from 0.45
to 7.06 s and averaged 3.46 + 1.86 s. Although initial pulse
trains for FSF were nearly twice as long as those for LF,
FF, and SBF, the differences were not significant, possibly
because of the large within-group variation (Fig. 3 c, Table 2).
The total number of EODs within the initial train ranged
from 45 to 414, averaging 163.8+ 105.2 EODs. The FSF
received more EODs per pulse train than the other treat-
Table 2 Torpedo californica. Results of one-way ANOVAs comparing five characteristics of initial pulse trains among LF, FSF, FF,
and SBF prey stimuli. The dfin all five tests were 3,22 (EODs electric
organ discharges)
Property of initial pulse train
F
p
Length
Number of EODs
Average instantaneous pulse rate
Decline in frequency of EODs
Maximum instantaneous pulse rate a
1.34
1.01
2.94
0.42
3.12
0.286
0.406
0.056
0.744
0.047
a Data were log-transformed to meet assumptions of homogeneity
of variances
Table 3 Torpedocalifornica. Partialcorrelations between five characteristics of initial pulse trains during predatory attacks by 26 rays
presented 1 of 4 prey treatments
Train length
No. of EODs
0.95 **
Average instantaneous
pulse rate -0.59"*
Decline in
frequency of
EODs
0.77 **
Maximum instantaneous
pulse rate
0.43 *
No. of
EODs
Average
Decline in
instantaneous frequency
pulse rate
of EODs
-0.45"
ments, but the differences were not significant (Fig. 3 d,
Table 2).
The average instantaneous pulse rate within the initial
pulse trains ranged from 60.8 to 122.4 EODs s -1, averaging 90.2+ 16.7 EODs s-1 among the four treatments. The
LF elicited the highest mean pulse rate and the FSF received the lowest (Fig. 3 e); the differences in pulse rates
among treatments were marginally significant (Table 2).
All four treatments showed a general decline in frequency of EODs throughout the course of the initial trains
(e.g. Fig. 2 for LF only). The least-squares slopes of the
regression between pulse rate and elapsed time were all
negative and did not differ significantly among the four
treatments (Table 2).
The maximum instantaneous pulse rate ranged from 129
to 308 EODs s-1 and averaged 178.4+_42.7 EODs s -1. The
LF and FF mean maximum pulse rates were similar and
substantially higher than the FSF and SBF treatments (Fig.
3 f). The differences in maximum pulse rates among treatments were marginally significant (Table 2); however, an
a posteriori test was unable to identify similar groups
(Tukey's HSD, p > 0.05).
Within the LF treatments, there was a significant positive regression between average instantaneous pulse rate
and water temperature (average instantaneous pulse rate --4.9 + 6.61 9 temperature; r 2 = 0.62; p = 0.007). Additionally, maximum instantaneous pulse rates were higher at
higher water temperatures (maximum instantaneous pulse
rate = 20.2 + 11.1 9 temperature; r 2 = 0.30; p = 0.10), and the
relationship probably would have been statistically significant with a larger sample size. Among all four treatments
taken together, however, there was no relationship between
any of the four pulse characteristics and either water temperature or total length of the rays (ANOVAs, p-values for
overall slopes of temperature and size covariates > 0.05).
The five characteristics of the initial pulse train (train
length, number of EODs, average and maximum instantaneous pulse rates, and decline of the pulse rate over time)
were intercorrelated. Partial correlation analysis indicated
that the train length was positively correlated with number
of EODs, decline in frequency of EODs, and maximum instantaneous pulse rate, but was negatively correlated with
average instantaneous pulse rate (Table 3). The number of
EODs was positively correlated with decline in frequency
of EODs, and was negatively correlated with average instantaneous pulse rate. Finally, average instantaneous
pulse rate was negatively correlated with the decline in frequency of EODs (Table 3). When all five characteristics
were compared simultaneously among the four treatments,
the overall differences among treatments were nearly significant (MANOVA; Wilk's lambda=0.33; F = 1 . 6 9 ;
df= 15,50; p = 0.084).
0.78 ** -0.73 **
Discussion
0.34
0.00
* Significant at p <_0.05; ** significant at p < 0.01
0.20
This study is the first to record the electrical activity of
electric rays in the field. Our aim was to study the electri-
167
cal activity and behavior of undisturbed rays as they attacked fish prey. Since the behavior of rays in captivity
may not reflect natural behavior, it is important to compare our results with those obtained in laboratory studies.
At the outset, we make two qualifications. First, we studied Torpedo californica, the only common species of
electric ray off southern California, while most previous
research has been conducted on species of Torpedo found
in the North Atlantic or in the Mediterranean Sea. Thus,
any dissimilarities may result from differences among species rather than between methods. Second, we wanted to
assess the natural variation in predatory behavior among
different rays. Since we never studied previously-tagged
individuals, all of our measurements were statistically independent. Thus, we feel the large variation we observed
in behavior and electrical activity is accurate and reflects
individual differences in the motivation to feed due to recency of feeding and other ecological and physiological
factors. Previous laboratory work on electric rays (e.g. Belbenoit 1981, 1986) described in detail the behavior of certain individual rays and did not provide overall summary
statistics. This, coupled with repeated observations on the
same individuals, makes it difficult to compare our variation with that observed in the laboratory.
Overall, our field measurements of electrical activity
agree quite closely with laboratory results. The individual
EODs we recorded were monophasic DC pulses averaging
--5 ms in duration, similar to previous findings (Bennett et
al. 1961; Bennett 1971; Belbenoit and Bauer 1972; Michaelson et al. 1979). Our maximum amplitude measurement of 45 V on a single Torpedo californica in the field
was similar to laboratory recordings for adult T. nobiliana
(50 to 60 V: Bennett et al. 1961) and T. marmorata (30 to
50 V: Zimmermann and Whittaker 1974; Mellinger et al.
1978, Belbenoit 1979). Coates and Cox (1942) reported
that the peak voltage produced by T. occidentalis was 220
V; however, Bennett et al. (1961) argued that this measurement was in error.
The lack of a relationship between the amplitude of the
EODs and size of the rays is consistent with previous research on other species of Torpedo. The voltage of EODs
increases rapidly in embryos and neonates of Torpedo spp.
and reaches a plateau at an age of several months. This age
corresponds to a length in T. marmorata of = 13 cm (Mellinger et al. 1978, Belbenoit 1979) and a weight in T. ocellata o f = 15 g (Michaelson et al. 1979). Our specimens
ranged in total length from 60 to 110 cm and in weight
from =4 to 26 kg, well beyond the size (and age) at which
the amplitude of EODs of T. californica probably stabilizes.
The temporal characteristics of the pulse train, although
variable, were also similar to those reported for other species. The general decrease in instantaneous frequency of
EODs during the pulse train (Fig. 2) is similar to that observed in all other species of Torpedo studied. The highest
instantaneous pulse rate we recorded was 308 EODs s-1.
Maximum rates in other Torpedo species range from 100
EODs s -1 in T. nobiliana (Bennett et al. 1961) to over 400
EODs s -1 in T. marmorata (Belbenoit and Bauer 1972). We
found that T. californica produced up to 414 EODs during
the initial pulse train. The maximum number recorded during predatory attacks in other species was 394 for T. marmorata (Belbenoit and Bauer 1972) and 340 for T. ocellata (Belbenoit and Moller 1971). We note, however, that
T. californica can produce many more EODs, especially
when fish prey are not ingested after the initial attack or
when rays attack a second prey; we recorded a maximum
of 1234 EODs produced when a ray attacked two fish (Fig.
2j).
Water temperature influences the pulse-train characteristics. The positive relationship between average instantaneous pulse rate and water temperature within the LF treatments corresponded to a Qa0 of 1.75 between 14 and
24 ~ this is slightly below the Qlo of 2 reported by Auger and Fessard (1928). Similarly, the positive trend
between maximum pulse rate and water temperature also
has been observed in Torpedo marmorata (Belbenoit 1979,
1986). Radii-Weiss and Kova6evi6 (1970) reported that in
vitro preparations of electric organ tissue of T. marmorata
and T. ocellata displayed decreased amplitudes and increased latencies after stimulation at temperatures below
15 and 10~ respectively. The authors speculated that
these rays may not use their electric organs during the autumn and winter when water temperatures are low.
The motor patterns of Pacific electric rays were very
similar to the "jumping predation" of Torpedo marmorata
described by Belbenoit and Bauer (1972) and Belbenoit
(1981, 1986). During our daytime tests, rays ambushed
prey by quickly jumping over the top of them from the
sand. During nighttime tests~ rays actively searched for
prey and lunged at prey from in front or below them with
vigorous thrusts of their tail. The rays started discharging
just when they began the "jump" phase, similar to T. marmorata (Belbenoit 1981, 1986).
The experiment with four prey treatments was designed
to assess the importance of various stimuli between initiation of an attack and ingestion (Table 1). The three treatments involving fish (live, freshly-speared, or frozen) all
triggered a high percentage of attacks. The lack of a clear
difference in latency and any of the pulse-train characteristics among these three treatments (Fig. 3 b - f ) , however,
does not enable us to eliminate visual, mechanical, electrical or chemical stimuli in prey detection by electric rays
(Table 1). Belbenoit (1981) observed that Torpedo marmorata attacked fast-moving inanimate objects as well as
fish and concluded that mechanical stimuli were necessary.
Our observation on the ray that attacked two fish (Fig. 2j)
supports this hypothesis: although a subdued fish was
closer, the ray turned and initially attacked a rapidly-swimming fish twice as far away. The SBF provoked far fewer
attacks (Fig. 3 a). The major stimuli associated with the
SBF trials were the electrical field and the slow and steady
movements and visual cue when the apparatus was positioned in front of the ray. Belbenoit (1986) showed that
T. marmorata attacks plastic poles (without electrodes)
moved near the anterior margin of their disk, presumably
due to the mechanical and possibly visual stimuli. It is unlikely that the attacks in our experiments with the SBF were
168
due solely to such stimuli, however, because rays never attacked the paired, unenergized dipole; the probability of
all four attacks occurring on the energized d ~ o l e (vs the
unenergized dipole) by chance alone is 0 . 5 ~ o r 0.0625.
Thus, the SBF treatment provides the first direct evidence
that electric rays include electrical cues in their detection
and/or assessment of prey. Note, however, that the SBF apparatus consisted of a dipole DC field of fixed amplitude
and geometry and lacked modulation that is characteristic
of live fish (Kalmijn 1978). This, and the lack of "natural"
mechanical, visual, or chemical stimuli, may explain the
low proportion of attacks (Fig. 3 a) and long latency (Fig.
3 b) with the SBF apparatus.
Our finding that LF and FSF treatments resulted in high
percentages of ingestion compared to the FF (Fig. 3 a) indicates that electric rays rely on additional feedback from
their prey after the initial attack. The major differences in
stimuli between FF and the other two fish treatments were
the lack of an appreciable bioelectric field and the absence
of muscle twitches induced by the EODs (Table 1); vision
during this stage cannot play an important role because the
prey is beneath the disk, out of view of the dorsally-located
eyes.
Belbenoit (1981) concluded that mechanical reception,
which probably involves tactile stimulation of the free
nerve endings in the skin and acoustic stimulation of the
lateral line, appears to provide information on the location
of the prey underneath the disk. Our observations support
this hypothesis. Rays consistently enveloped prey in their
disk during daytime attacks from the sand and nighttime
attacks in midwater. In addition to concentrating the
electric field over the prey, this envelopment orients mechanoreceptors around the prey, probably providing three-dimensional mechanical information on the prey's activity
and location. This mechanoreception may be augmented
by electroreception via the single row of ampullary pores
that encircles the outer edge of each electric organ. The response of prey to EODs further contributes to the mechanical stimuli. Fish are often tetanized and quiver after the
initial attack (Bray and Hixon 1978 and present authors'
personal observations), which probably provides constant
mechanical stimuli. Additionally, rays often produced
EODs after the initial attack (Fig. 2). During the FSF treatments, we often felt the freshly-speared fish twitch through
our spear while it was trapped beneath the disk, probably
as a result of these sporadic EODs. The muscle twitches
induced by these sporadic EODs may enhance mechanical
location of prey beneath the disk.
Rays responded faster to LF and FSF presented at night
than during the day. Bray and Hixon (1978) noted that rays
were more active at night and probably foraging at that
time; therefore, it was not surprising that rays attacked
more readily at night. Slower daytime responses might be
attributable to the apparent resting state of the rays. Because of this low daytime-activity state, rays may require
additional time to become aware of potential prey.
More information is needed on how rays detect prey at
night. To date, including this study, most observations have
been made on rays resting on sand during the day. In this
ambushing mode, the ray and surrounding substrata are immobile when prey move nearby, and the prey is always at
the same level or above the ray. At night, on the other hand,
rays swim slowly or drift in pursuit of fish prey (Bray and
Hixon 1978), prey may or may not be mobile (depending
on their nocturnal behavior), and prey is often beneath the
moving ray, out of sight. These nocturnal differences in
predator and prey behavior create a different suite of stimuli than those during the day and can provide a challenging but rewarding area of future research.
Acknowledgements We thank D. and D. Neilson, R. Watkins, and
especially M. Ezcurra for their help in the field. We thank G. Lowe
for her review of this manuscript and her aid in the field. Financial
support was provided by the National Geographic Society, Committee of Research and Exploration through Grant # 3881-88, and the
Scholarly and Creative Activity Committee at California State University, Long Beach.
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