Insights into young of the year white shark, Carcharodon carcharias, behavior in the Southern California Bight
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Environmental Biology of Fishes 70: 133–143, 2004.
© 2004 Kluwer Academic Publishers. Printed in the Netherlands.
Insights into young of the year white shark, Carcharodon carcharias,
behavior in the Southern California Bight
Heidi Dewar, Michael Domeier & Nicole Nasby-Lucas
Pfleger Institute of Environmental Research 901 B Pier View Way, Oceanside,
CA 92054, U.S.A. (e-mail: Heidi Dewar@alumni.ucsd.edu)
Received 9 May 2003 Accepted 2 September 2003
Key words: satellite telemetry, foraging, diving, thermoregulation
Synopsis
A young of the year female white shark, Carcharodon carcharias, was tagged with a pop-up satellite archival tag
off Southern California in early June of 2000. The tag was recovered after 28 days, and records of temperature,
depth and light intensity were extracted. Depth and temperature records indicate a number of interesting behaviors,
including a strong diurnal pattern. At night the shark remained in the top 50 m, often making shallow repetitive
vertical excursions. Most dives below the mixed layer were observed during the day, 91% of which occurred from
05:00 to 21:00 h, with depths extending to 240 m. Many of the dives exhibited secondary vertical movements that
were consistent with the shark swimming at the bottom (at depths from 9 to 165 m) where it was most likely
foraging. The white shark experienced dramatic and rapid changes in temperature, and demonstrated a considerable
tolerance for cold waters. Temperatures ranged from 9◦ C to 22◦ C, and although 89% of the total time was spent in
waters 16–22◦ C, on some days the small shark spent as much as 32% of the time in 12◦ C waters. The deep dives
into cold waters separate the white sharks from mako sharks, which share the California Bight nursery ground but
appear to remain primarily in the mixed layer and thermocline. Movement information (derived from light-based
geolocation, bottom depths and sea surface temperatures) indicated that the white shark spent the 28 days in the
Southern California Bight, possibly moving as far south as San Diego, California. While the abundance and diversity
of prey, warm water and separation from adults make this region an ideal nursery ground, the potential for interaction
with the local fisheries should be examined.
Introduction fidelity (Anderson & Goldman 1996, Cliff et al. 1996,
Ferreira & Ferreira 1996), foraging strategies (Tricas &
Our understanding of the biology of adult and ado- McCosker 1984, Klimley et al. 2001), thermal biology
lescent white sharks has advanced dramatically over (Carey et al. 1982, McCosker 1987, Goldman 1997)
the last 10–15 years (see Ellis & McCosker 1991, and general movement and activity patterns (Klimley
Klimley & Ainley 1996). Most studies have benefited et al. 1992, Strong et al. 1996, Goldman & Anderson
from the development of a suite of new tagging tech- 1999). While most efforts have focused on the near-
nologies (Arnold & Dewar 2001) as well as the affinity shore environment, satellite telemetry is beginning to
of white sharks for near-shore habitats, which pro- provide insights into offshore movements, reinforc-
vides an excellent opportunity for shore-based research ing the capacity for extensive migrations in adults
projects. Using a combination of photo identifica- (Boustany et al. 2002).
tion, conventional tagging, visual observations, satel- These collective research efforts have provided a
lite technologies and acoustic telemetry, researchers rough outline of the biology of white sharks, especially
have amassed a substantial global database on white off the west coast of North America. In the waters off
shark biology. Studies have examined long-term site California and Mexico, white shark abundance varies134
seasonally and geographically, although over a large California on May 28, 2000, and then taken to the
portion of the coast they are encountered year round Southern California Marine Institute facility in Long
(Klimley 1985, Long et al. 1996). Marine mammals Beach Harbor. Here the animal was maintained in a
form a relatively large portion of the adult shark’s 6 m covered tank for 4 days where it remained alert
diet (Tricas & McCosker 1984, Klimley 1985), and and in good condition. Prior to its release on June 2,
adult white sharks are commonly associated with pin- 2000 the shark was moved from the tank using a sling,
niped rookeries along the California coast, particularly measured and then placed in a small holding tank on a
at Año Nuevo and the South Farallon Islands. In the fishing vessel. While still in the vessel’s holding tank,
summer it is thought that the females move from these the PAT (PAT-2000, Wildlife Computers, Redmond
feeding areas to nursery grounds to give birth (Klimley WA, U.S.A.) was inserted at the base of the dorsal fin
1985, Francis 1996). Pupping is thought to occur dur- using a large plastic dart. The shark was then released
ing the summer and fall in the California Bight, south of just off shore of Long Beach, California in 24 m of
Point Conception. In this region, both pregnant females water. Although the satellite tag was set to release after
and young of the year (YOY) white sharks have been 6 months, it was recovered 28 days later by a second
incidentally caught by a number of fishing gear types, fisherman near the point of release, at Huntington Flats,
primarily gill nets (Klimley 1985). The incidental take on June 30, 2000. The fisherman reported that only
of young sharks both here and in other areas has pro- the tag was entangled in the net and that there was no
vided the opportunity to examine stomach contents and evidence of the small shark.
it is apparent that, when compared to adult white sharks, The PAT is a relatively new tool used to examine the
the juveniles have a substantially different diet. While large-scale movements and behaviors of pelagic fish
the adults feed largely on marine mammals (Tricas & (Lutcavage et al. 2000, Block et al. 2001, Boustany et al.
McCosker 1984, Casey & Pratt 1985, Klimley 1985), 2002). These devices are secured to the fish and collect
juveniles have been found to feed primarily on inver- data on temperature (+0.05◦ C), depth (±0.5 m) and
tebrates, demersal teleosts and elasmobranchs. Squid light intensity (measured as irradiance at 550 nm) every
and epipelagic fish are also consumed but to a lesser 2 min. At a predetermined time, the tag releases from
extent. This shift in diet is matched by an ontogenetic the fish, floats to the surface and uploads summarized
change in dentition (Tricas & McCosker 1984, Hubbell data to the Argos satellites. If the tag is recovered either
1996). prior to or after its predetermined release time, the full
Although the combined global effort in the study data set (unsummarized) can be extracted.
of white sharks is rapidly elucidating adult and ado-
lescent biology, almost nothing is known about the Geolocation
juveniles. Current understanding of YOY biology is
based largely on the incidental take of juveniles and Values for latitude and longitude are estimated using
pregnant females, and stomach content analyses from a light intensity measurements and the apparent time of
relatively small number of individuals (Klimley 1985, dawn and dusk as indicated by the exponential change
Francis 1996, Uchida et al. 1996). Given the consid- in light levels recorded over these periods (Hill 1994,
erable shift in diet and the differences in geographic Klimley et al. 1994, Hill & Braun 2001). By calcu-
location, inferences about juveniles based on adult lating the midpoints between dawn and dusk, local
behavior are questionable. With the global concern noon and midnight can be determined and longitude
about white shark conservation (Heneman & Glazer calculated using standard astronomical equations. Day
1996, Murphy 1996), it is critical that additional infor- length (the time interval between dawn and dusk)
mation is obtained on this poorly understood life his- changes along the earth’s meridians in a predictable
tory stage. We report here the results from one pop-up manner and thus estimates of day length can be used
archival satellite tag (PAT) recovered after 28 days on to calculate latitude assuming the date is known. It is
a YOY white shark in the Southern California Bight. estimated that for this model of Wildlife Computers
PAT tags when archival records are recovered, latitude
and longitude can be determined within 0.78–3.5◦ and
Materials and methods 0.15–0.25◦ , respectively (Musyl et al. 2001). Latitude
estimates can however, be improved by comparing sea
A juvenile female white shark, 1.4 m fork length (FL), surface temperature (SST) measured by the tag with
was captured in a bottom set net off of Long Beach, SST determined from Advanced Very High Resolution135
Radiometry (AVHRR) imagery along a line of longi- based on the recapture and release points, apparent
tude with constraints employed on maximum move- benthic swimming behavior, maximum dive depths and
ments between days (Block et al. 2001, Gunn & Block the SST-augmented, light-based geolocation estimates.
2001). Location estimates are further improved by The Huntington Flats fishing area, where the white
comparing maximum deep dives or bottom depths (see shark encountered the net both times, is located from
below) to regional bathymetric maps. three miles off Long Beach to the shelf break. On 12 of
the recorded days, the animal displayed dive patterns
Vertical movements suggesting that it dove to and along the seafloor, dis-
playing minimal secondary vertical movement while
From depth and temperature data recorded by the tag, at depth. During these dives, the bottom depths ranged
information on habitat preferences, behavioral patterns from 9 to 165 m (see below), and placed the shark over
and the thermal characteristics of the water column the continental shelf or slope, within 2–22 km of shore.
can be obtained. To examine vertical movements, dives Based on the available information, it appears that
longer than 4 min, where temperature changed by more the shark remained in the Southern California Bight
than 5◦ C (this eliminated minor vertical movements), (in the area delineated by the solid line) for the 28-day
were characterized by their depth (Ddepth ), temperature deployment, moving as far south as San Diego for
at depth (Dtemp ), duration (Dduration ), time of day, the sur- 3 days, from June 12 through June 14. For the remain-
face interval between dives (Sinterval ) and the integral of der of the days, the available data indicated that the
the change in temperature over the dive (Tintegral ). The shark was between Long Beach and Camp Pendleton.
integral was used to estimate the magnitude of the dive Also, shown is the 240-m contour, which is the deepest
from a thermal perspective and is essentially, the tem- dive depth observed. Unfortunately, the errors in geolo-
perature change multiplied by the length of exposure. cation estimates, even with the use of SST, preclude the
This was calculated by first subtracting the ambient generation of an actual track over this spatial scale.
temperature at depth from SST for each 2-min sam-
pling interval, providing a profile of the temperature Depth and temperature
difference with time throughout each dive. To obtain
the area (integral) within the temperature profile, the The vertical movements were examined for diurnal pat-
area for each 2-min sampling interval was calculated by terns, habitat preference and other behaviors. The first
first multiplying each temperature difference by 2 min, 8 h after the release were excluded from the analy-
these values were then summed over the duration of the sis to allow for a recovery period following tagging
dive (Equation (1)). (Arnold & Dewar 2001). Based on the temperature
profiles, the depth of the mixed layer varied through-
Tintegral = (SST − Dtemp ◦ C)2 min (1) out June, ranging from 10 to 20 m. (A thermal lag
in the thermistor makes a more precise definition
The Tintegral will be greater for longer dives or those of the thermal profile difficult.) Figure 2a shows a
into cooler waters. Thus, higher Tintegral values reflect comparison of the day and night depth distributions.
a greater level of thermal stress. Each dive was also (Daylight hours include the period of dawn and dusk
examined to establish whether the vertical movement where light is detected.) At night depths were con-
at depth was consistent with the shark swimming at strained to within the top 50 m with 96% of the time
or near the bottom (e.g. secondary vertical movements spent above 20 m, 39% of which was at the sur-
while at depth were minimal). All data were analyzed face (depth = 0–1 m). During the day, depth ranged
for normalcy and the average ±SD reported unless from 0 to 240 m and although 89% of the time was
otherwise indicated. above 20 m, a greater percentage of time (62%) was
spent at the surface with less time in the remaining
portion of the mixed layer. The shark spent sig-
Results nificantly more time in deep water during the day
than at night (2-sample Kolmogorov–Smirnov Test,
Geolocation p = 0.008).
A summary of temperature measurements over the
Figure 1 shows the geographic region in which the record indicated the following. Although the majority
white shark was located over the 28-day deployment of the time (89%) was spent in waters 16–22◦ C136
50m contour
100m contour
240m contour Long Beach
500m contour
Release point Huntington Beach
Huntington Flats
Camp Pendleton
San
Diego
Figure 1. Map of Southern California outlining the estimated area where the white shark remained over the 28-day deployment. The black
dotted line indicates the 3-mile line, which marks the eastern boundary of the fishing grounds at Huntington flats. The 240 m contour, the
deepest depth the shark attained, is also indicated.
(Figure 2b), on some days the shark spent as much the thermocline to an average depth of 71 m (±7 m).
as 32% of the time in 12◦ C waters (see below). The She remained at depth for 26–76 min and had surface
lowest temperatures encountered by the shark, down intervals ranging from 52 to 122 min. During the day-
to 9◦ C, were associated with vertical excursions. On light hours on this day, the shark spent 32% of its time
average, the minimum temperature encountered on a between 50 and 75 m in 12◦ C water and 65% of its time
given day was lower than SST by 8.6◦ C (±3.0, rang- at the surface at between 20◦ C and 21◦ C.
ing from 2.4◦ C to 13.4◦ C). SST varied by only 3.8◦ C A similar pattern of only shallow excursions at night
(18.2–22◦ C; average = 20 ± 1). Examination of SST and deep dives during the day was observed during 20
in relation to daily AVHRR imagery indicated that the of the 28 days. Most of the remaining 8 days occurred
white shark was detected primarily in the warmer water at the beginning of the record; for 5 days immediately
masses found closer to shore. following its release, the shark remained above 30 m
While the behaviors and vertical distributions in the mixed layer. For the 20 days where deep dives
observed during the night were relatively consistent were documented, a closer examination of the tem-
over the 28-day record, there was a considerable poral occurrence of these dives confirms the diurnal
degree of variation observed among behaviors during pattern observed in Figure 3b. Of the 82 dives docu-
the daylight hours as evidenced in Figure 3a,b. On mented, only seven (8.5%) occurred at night and six of
June 8 (Figure 3a) during both the day and night hours, the seven were on two nights (June 19 and 21, 2000)
the shark remained in the mixed layer making regular shortly after the full moon (June 17, 2000). The tim-
vertical movements between the surface and ∼25 m. ing of dives (Figure 4) is bi-modally distributed with
On 20 June (Figure 3b) a very different pattern was peaks from 05:00 to 07:00 h and 13:00 to 19:00 h when
observed. Although the shark generally remained in the 21% and 41% of the dives were made, respectively.
top 25 m at night, during the day she was either at the When comparing 1-h blocks, the largest percentage of
surface (depth = 0–1 m) or made rapid dives below dives occurred before the sun reached the horizon from137
0.20
a) 70
Percent of total dives
Night 0.18
60 sunrise sunset
Day 0.15
50
Percent time
0.13 repr esenta tive light
40 level
0.10
30 0.08
20 0.05
10 0.03
0 0.00
0
0
0
0
0
0
0
0
0
0
0
0
:0
:0
:0
:0
:0
:0
:0
:0
:0
:0
:0
:0
m
m
m
m
0m
m
11
13
15
17
19
21
23
-1
-3
-5
-7
-9
10
00
00
00
00
00
2
20
50
0
0-
0-
0-
0-
0-
0-
0-
25
10
to
:0
:0
:0
:0
:0
:0
:0
0:
2:
4:
6:
8:
to
to
to
10
12
14
16
18
20
22
0
to
to
2
10
20
0
50
10
Time intervals
Surface Mixed layer Below mixed layer
Figure 4. Percentage of dives at different hourly intervals over
a 24-h day. Only dives longer than 4 min where temperature
b) 60
changed by at least 5◦ C are included. Also indicated is a
50 representative light curve for a 24-h period.
Percent time
40
30
20
05:00 to 06:00 h. The most extreme dive to 240 m at 9◦ C
10 occurred at 05:19 h and was for 80 min.
0 For all dives Ddepth ranged from 18 to 240 m (median
48 m). Dtemp ranged from 9◦ C to 15◦ C (average 11.7 ±
12
14
16
18
20
22
10
to
1.5◦ C). Dduration ranged from 6 to 110 min (average 39±
to
to
to
to
to
to
10
12
14
16
18
20
8
Temperature bins (oC) 23 min). Sinterval ranged from 0 to 716 min (median 63).
The Tintegral ranged from 27 to 900 min ◦ C (average
Figure 2. The percentage of time spent at different (a) depths, 296±219). Although there is a large degree of variabil-
for both day and night, and (b) temperature for the entire 28-day ity in the data, regression analysis indicates a significant
record.
increase in Sinterval as a function of Tintegral (p < 0.05,
r2 = 0.15). More time in cold water was associated
a) 30 0
with longer surface intervals. Up to Tintegral values of
Temperature ( oC)
25
depth
20 444 min ◦ C, Sinterval ranged from 0 to 216 min, at higher
Depth (m)
20
40
values Sinterval increased, ranging from 26 to 310 min.
15
temperature
The shark was able to make dives into relatively cool
10 `
60
waters (10.8◦ C) for up to 58 min with little time at the
5 light 80 surface prior to subsequent dives.
0 100
Closer examination of Figure 3a,b illustrates two
0:00 4:00 8:00 12:00 16:00 20:00 0:00 additional behaviors of interest. First, in Figure 3a inset,
Time note the regular vertical excursions between the sur-
face and the bottom of the mixed layer. The rates of
b) 30 0 ascent and descent were calculated over portions of the
Temperature ( o C)
25 depth record when similar patterns were observed (only depth
50
changes greater than 10 m were examined). The mean
Depth (m)
20
15 100 rate of ascent (1.2 m min−1 ± 0.4) was significantly
10
slower than the mean rate of descent (2.5 m min−1 ±0.6)
temperature
light 150 (two sample t-test, p = 0.001). The second pattern is
5
seen in Figure 3b. Note that at depth there is very little
0 200
0:00 4:00 8:00 12:00 16:00 20:00 0:00
secondary vertical fluctuation. The profile is consistent
Time
with the shark swimming near a sloping bottom. Dives
of this nature occurred on 12 days and ranged from 8 to
Figure 3. Temperature, depth and light level data recorded every 110 min in duration (average 44 ± 26 min) over depth
2 min over a 24-h period for (a) 8 June and (b) 20 June. from 9 to 165 m (average 51 ± 28 m).138
Discussion to reduce transport costs (Weiss 1973), this proved
not to be the case. Theoretical analysis conducted by
The archival record obtained from the pop-up satellite Weiss indicates that for energy savings to be realized
tag represents the most detailed dataset available on the for negatively buoyant fish, the rate of ascent must
movements and behaviors of a juvenile white shark in be greater than descent and specific angles of incli-
the Southern California Bight, a key nursery ground nation are required. Although with no information on
for this species. This white shark was likely born in movement over ground it was not possible to quantify
the spring of 2000. The reported size at birth for white angles of ascent and descent, the relative rates of ascent
sharks is 1.2–1.5 m total length (TL) (Francis 1996). and descent for the small white shark are opposite
Using the conversion factors provided by Mollet and that required for energy savings. A similar pattern was
Cailliet (1996), the 1.4 m FL for the small female equals observed for blue sharks tracked acoustically by Carey
a 1.54 m TL. The record obtained provides important and Scharold (1990); the rates of descent were faster
information over a time period in the life-history of than for ascent. Carey and Scharold reported that the
white sharks when they are least understood and vul- angles of ascent and descent were also not consistent
nerable to predation and incidental take by fisheries. with burst-glide swimming. The fact that sharks tend
Additional studies are necessary to confirm results and to be only slightly negatively buoyant might preclude
address a suite of additional questions. their use of burst glide as an energy saving mechanism.
Examination of the vertical movements, especially The shallow, repetitive vertical excursions, which
in relation to temperature, provides important insights were observed predominantly at night, could be asso-
into foraging strategies, thermal biology and habitat ciated with nocturnal foraging. The sharks may swim
preferences of the YOY white shark. The range of depth down and then slowly swim up while searching for pro-
and temperature experienced by this white shark are files against any down-welling light. The presence of
more extensive than might have been expected based sufficient light at night against which to observe profiles
on the limited and potentially biased data available. is supported by the dive-associated variations in light
Catch records in the California Bight for white sharks that were apparent in the tag’s light record two nights
smaller than 2 m have primarily occurred in less than away from the new moon. That is, even two nights
25 m of water (Klimley 1985). Also, given the size of before the new moon the light level recorded by the
the juvenile white shark, one would expect a lower tol- tag increased as the shark approached the surface. The
erance for cold waters due to a relatively low thermal tags are sensitive to 10 log units of light, which is sim-
inertia. Although the majority of time was spent in the ilar to sharks’ eyes (Gruber & Cohen 1978). It should
warm waters of the mixed layer, movement into deeper be mentioned that while feeding may occur at night in
waters was prevalent throughout the record and on the mixed layer, stomach content data indicate benthic
some days time spent below the thermocline exceeded foraging is more important (Tricas & McCosker 1984,
30%. This indicates that ambient temperature does not Casey & Pratt 1985, Klimley 1985).
prohibit the young white sharks from using the entire Other potential explanations for shallow repetitive
water column when the animal is over the continen- vertical excursions include thermoregulation, orient-
tal shelf. If the shallow vertical distribution observed ing to the earth’s magnetic field or searching the water
primarily on the days shortly after release represents column for chemical cues (Carey & Scharold 1990,
a recovery period, then the summarized data are a Klimley et al. 2002). Chemical cues might either indi-
conservative estimate of time at depth. Note however, cate the presence of prey or be used to navigate, as
that the shark was released in relatively shallow water with salmon returning to their natal stream (Carey &
(∼20 m). Recent data on adult white sharks indicate Scharold 1990, Klimley et al. 2002). However, most of
that they are also not constrained to the mixed layer these excursions were constrained to the mixed layer
but spend large portions of time below the thermocline and top of the thermocline and the chemical stratifi-
when offshore (Boustany et al. 2002). cation and temperature fluctuations will be minimal in
Detailed examination of the depth records revealed this region.
a number of interesting patterns that may be related There are a number of diurnal migrators present in
to foraging. Although at first glance the shallow cyclic the surface waters at night that are potential prey for a
excursions (Figure 3a) appear similar to the burst-glide small white shark including squid and teleosts such
swimming observed in many pelagic animals (Carey & as mackerel, anchovies, sardines and hake. In fact,
Olson 1982, Holland et al. 1990, Block et al. 1997) the California Bight is an important spawning ground139 for a number of species that have been documented including a number of flatfish, Pacific hake and a in white shark stomach contents (Tricas & McCosker large range of smaller elasmobranchs. California hal- 1984, Casey & Pratt 1985, Klimley 1985). Chub mack- ibut, Paralichthys californicus, are found primarily erel, Scomber japonicus, is most abundant south of from the surf zone to 60 m overlapping with the appar- Point Conception within 20 miles of shore and spawn- ent foraging depth of the white shark (MBC Applied ing occurs in near-shore surface waters from April to Environmental Sciences 1987). Additional flatfish August (Hernandez & Ortega 2000, Konno et al. 2001). common in the area include sanddabs, Citharichthys For the Pacific sardine, Sardinops sagax, the peak spp. (Allen & Leos 2001) and turbot, Pleuronichthys in spawning occurs south of Point Conception from spp. (Leos 2001). The cabezon, Scorpaenichthys April to August in the top 50 m of the water column marmoratus, occurs from the intertidal zone to 80 m (Wolf et al. 2001). Pacific hake, Merluccius productus, (Wilson-Vandenberg & Hardy 2001). Also, a number also common off Southern California, move inshore of small elasmobranchs including the round stingray, after spawning in May and follow their prey (krill) to Urolophus halleri, the California skate, Raja inornata, the surface each night (MBC Applied Environmental (Zorzi et al. 2001), the leopard shark, Triakis semifas- Sciences 1987, Quirollo et al. 2001). A large squid fish- ciata and the smooth dogfish, Mustelus canis, (Castro ery exists in Southern California, and although the peak 1983, Smith 2001) are found in high numbers off occurs earlier in the year, the fishery can extend into Southern California in shallow, near-shore habitats. the summer months (Yaremco 2001). The vertical movement patterns of this young female While foraging may occur in the mixed layer and differ considerably from published data for adult white near the surface at night, the daytime dive patterns sharks. Acoustic telemetry studies conducted near suggest that diurnal feeding occurs at or near the bot- the Farallon Islands with adults showed a signifi- tom. The deep profiles with minimal vertical excursions cant correlation between swimming depth and the in Figure 3b are similar to those observed for other bottom in waters less than 30 m. When depths were species documented to be at the bottom including adult greater, sharks strayed from the bottom remaining white sharks (Goldman & Anderson 1999) and tiger within ∼30 m of the surface, seldom venturing to the sharks (Holland et al. 1999). An affinity for the ben- surface (Goldman & Anderson 1999). One large white thic habitats is confirmed by the occurrence of white shark tracked offshore in the western Atlantic (Carey sharks as by-catch in the bottom set net fishery as et al. 1982) spent most of its time in the thermocline, well as their diet, which consists primarily of demersal making only infrequent excursions to the surface or species (Tricas & McCosker 1984, Casey & Pratt 1985, below the thermocline to ∼50 m. There was no diur- Klimley 1985). The range of bottom depths observed nal pattern apparent in the depth records and the larger indicates that demersal feeding occurs from relatively sharks did not spend protracted periods at the surface. shallow, near-shore waters to the continental slope at Only one acoustic track has been conducted with a 165 m, although most bottom dives were from 30 to juvenile white shark (Klimley et al. 2002), however, 60 m. It is likely that this benthic foraging is primar- the short track duration (3.6 h) makes comparisons dif- ily restricted to daylight hours due to visibility. White ficult. The behavior of fish following release is often sharks are suggested to have retinal structure most aberrant for a matter of hours (Arnold & Dewar 2001). consistent with a diurnal lifestyle (Gruber & Cohen The patterns observed for the small white shark were 1985). similar to those observed for blue sharks acoustically There were a number of deep dives during the day- tracked by Carey & Scharold (1990). At night the blue light hours where the plateau in vertical movements sharks tended to remain in the thermocline or mixed at depth was not observed. These dives may be asso- layer but made deep dives during the day into water ciated with swimming near the bottom but along the as cool as 7◦ C. The deep dives were punctuated by steep relief of the shelf slope, possibly indicating search periods either at the surface or in the mixed layer that behavior to locate the bottom. It is also possible that served to prevent muscle temperature from dropping the shark was orienting to the earth’s magnetic field too low, which was evident through the use of mus- or searching for chemical cues as discussed above cle thermistors in a number of sharks. The durations (Carey & Scharold 1990, Klimley et al. 2002). in warmer waters varied from only a few minutes to There are numerous potential prey items that the 30 min before subsequent dives. The blue sharks were YOY white shark would encounter at depth during reported to be feeding on cephalopods in the deep scat- daylight hours over the California continental shelf tering layer during daylight hours. Thus, the diurnal
140 pattern was associated with prey availability and not a 11◦ C cooler than surface waters. A number of surface- difference in visibility, which appears to be a contribut- oriented, pelagic fish including yellowfin tuna, striped ing factor for the small white shark when feeding on marlin and blue marlin have been demonstrated to be the bottom. limited to temperature ranges from SST to 8◦ C cooler In addition to the white shark, the California Bight than SST (Brill et al. 1993, 1999, Block et al. 1997). is an important nursery ground for the short-fin This is a narrower temperature range than observed in mako, Isurus oxyrinchus, another endothermic lam- this study. nid (Holts & Bedford 1993, Taylor & Bedford 2001). Although this juvenile white shark showed a con- The two species, however, appear to be differenti- siderable tolerance for cold waters, vertical movement ated by niche separation as indicated both by diet patterns indicated some thermal constraints on behav- and behavior. Juvenile mako sharks feed primarily on ior. The positive relationship between thermal dive small schooling pelagics such as mackerel, anchovies magnitude (as indicated by Tintegral ) and the subsequent and sardines (Holts 1988, Taylor & Bedford, 2001) surface interval as well as the pattern of regular ver- where as the white sharks focus mainly on demer- tical excursions are indicative of behavioral thermal sal species. Acoustic tracks for three 2-year-old mako regulation (Carey & Scharold 1990, Holland et al. sharks (Holts & Bedford 1993) indicated that they 1992). During longer dives a greater thermal debt was remained in the mixed layer for 90% of the time mak- incurred presumably requiring a more extensive sur- ing only short excursions below the thermocline to less face interval to thermally recharge prior to subsequent than 40 m. The coldest temperature encountered was dives. The variation in Sinterval is likely explained by the 12◦ C, and then only for a brief period of time. Also, multitude of factors that will influence behavior includ- no diurnal pattern was observed (although the tracks ing the presence of predators, feeding and digestion. were relatively short). In a second study by Klimley As well as influencing subsequent behaviors, feed- et al. (2002), three additional juvenile mako sharks ing has a direct impact on thermal biology. Because were tracked near a submarine canyon. Although these prey consumed is at ambient temperature, feeding can sharks spent most of their time near the bottom of the cause a drop in visceral temperature (McCosker 1987, thermocline below the mixed layer, they did appear to Goldman 1997, Lowe & Goldman 2001). Some sharks be constrained to waters above 14◦ C and never ven- may also exhibit an elevation in stomach temperature tured below 65 m. The available data suggest that the with feeding as has been observed in a number of juvenile mako forages primarily in the thermocline and teleosts (Carey et al. 1984, McCosker 1987). Thus, above. successful foraging will complicate interpretation of The differences between temperatures encountered the link between time at depth and subsequent surface by the mako and white shark may reflect an enhanced intervals. ability of the white shark to tolerate cold water while The punctuated vertical excursions observed in foraging at depth. This thermal tolerance it likely linked Figure 3b are similar to patterns that have been to the white shark’s greater endothermic capacity in observed in a number of species employing both comparison to mako sharks, as suggested by the higher behavioral (blue sharks, Carey & Scharold 1990) and elevation in stomach temperatures reported for adults. physiological (bigeye tuna, Holland et al. 1992, Dagorn The maximum elevation of stomach temperature above et al. 2000) thermoregulation. Measurements of body ambient temperature reported from adult white sharks temperature are necessary to verify the behavioral ther- is 14.3◦ C (Goldman 1997) where as for mako sharks it moregulation as well as to document the white shark’s is 8◦ C (Carey et al. 1981). capacity for modifying the efficiency of their counter- The YOY white shark exhibited a surprising toler- current heat exchangers and physiological thermoreg- ance for large changes in ambient water temperature ulation (Holland et al. 1992, Dewar et al. 1994). Recent despite her small size. This is particularly impres- evidence indicating that both salmon sharks (Goldman sive when one considers that although white sharks pers. comm.) and mako sharks (Bernal et al. 2001) can are endothermic, not all body regions are supported modify heat transfer suggests that their close relative by countercurrent heat exchangers. The temperature the white shark will be capable of the same. In fact, of tissues, such as the heart will parallel water tem- it has been suggested that adult white sharks may be perature, but must continue to function and support homeothermic given their relatively constant body tem- systems that are thermo-conserving. This small female perature over a broad range of ambient temperatures was able to spend up to 80 min in waters at 9◦ C, which is (Lowe & Goldman 2001). While this may hold true for
141
the adults, the apparent thermal constraints to diving a good start, more effort is needed to increase the
suggest this may not be the case for the juveniles. Both sample size and to address a number of important ques-
the thermal inertia and absolute heat production will be tions. What is the rate of encounter with fishing nets
less for these smaller animals. Further research on the and the associated mortality? What are the larger-scale
thermal physiology of juvenile white sharks will eluci- movement patterns and what is the southern extent of
date ontogenetic changes in thermoregulatory abilities their range? What are the fine-scale geographic move-
and as well as thermal tolerances. ments? Do the juvenile white sharks exhibit diurnal
The YOY white shark stayed within the Southern onshore/offshore movements apparent for some blue
California Bight over the 28-day record moving sharks? When and where are the sharks feeding? One
between Long Beach and San Diego, California and additional tool that could be useful is an acoustic
spent a large portion of its time in near-shore waters stomach temperature or pH sensor, which is currently
over the continental shelf and slope. The occurrence of under development (Y. Papastamatiou & C. Lowe pers.
sharks in these areas is confirmed by both the by-catch comm.). Measurements of muscle temperature during
data and strandings that occur from Point Conception diving will further illuminate potential thermoregula-
to San Diego (Klimley 1985, Klimley et al. 2002, tory mechanisms and thermal constraints on behavior.
California Department of Fish and Game, unpubl. This information is not only important for improving
data). The Southern California Bight appears to be our understanding of white shark biology but also for
an ideal nursery ground. The juveniles are separated their long-term conservation and management.
from the adults and are in warmer waters, which may
help to maximize growth. Additionally, their occur- Acknowledgements
rence in these waters coincides with the high abundance
of a number of important and diverse prey items. We express our thanks to C. Winkler of the Southern
While the risk from adult predation may be reduced Californian Marine Institute as well as the fishermen
in the Southern California Bight, the local bottom set that caught and released the white shark and returned
net fishery is an added source of mortality, although the PAT tag. Thanks also go to Ken Goldman for his
reported catch rates are low (Klimley 1985). Klimley valuable comments on this manuscript.
reported that 44 white sharks smaller than 2 m had
been caught between 1955 and 1985. From 1985 to
2000 the California Department of Fish and Game References
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