|
| |
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
First published online November 1, 2006
Journal of Experimental Biology 209, 4524-4532 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02530
Identifying and quantifying prey consumption using stomach temperature change in pinnipeds
Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, Long Marine Laboratory, 100 Shaffer Road, CA 95064, USA
* Author for correspondence (e-mail: kuhn{at}biology.ucsc.edu)
Accepted 7 September 2006
 |
Summary |
|---|
 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Key words: feeding behavior, stomach temperature, northern elephant seal, California sea lion, water ingestion
|
Introduction |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
; Costa, 1993;
Kooyman, 1965;
Kooyman, 1989;
Shaffer and Costa, 2006).
Previous studies examined changes in at-sea behavior, such as movement
patterns (Le Boeuf et al.,
2000; McConnell et al.,
1999), dive shapes (Hindell et
al., 1991; Lesage et al.,
1999; Simeone and Wilson,
2003) and swim velocity (Le
Boeuf et al., 1992; Lesage et
al., 1999) to identify foraging. However, time-depth recorders and
satellite transmitters cannot provide information about when and where prey
are captured, and instead define putative foraging behavior. In order to truly
understand the foraging ecology of a species, it is necessary to combine
measures of feeding behavior with data collected on at-sea diving and
movements.
To examine at-sea feeding behavior, technology to measure stomach
temperature has been used with a variety of marine predators, such as seabirds
(Catry et al., 2004;
Grémillet and Plös,
1994; Weimerskirch et al.,
2005; Weimerskirch and Wilson,
1992; Wilson et al.,
1992), sharks (Klimley et al.,
2001; Sepulveda et al.,
2004), turtles (Tanaka et al.,
1995), and marine mammals
(Andrews, 1998;
Austin et al., 2006;
Hedd et al., 1995;
Lesage et al., 1999). This
technology is based on the assumption that ectothermic prey of marine
endotherms is colder than the predators' core body temperature. Therefore,
consumption results in a rapid decline in stomach temperature
(Fig. 1).
|
;
Catry et al., 2004;
Grémillet and Plös,
1994; Ropert-Coudert et al.,
2000; Wilson et al.,
1992; Wilson et al.,
1995). These studies have shown that identifying both prey and
water consumption is possible; however the best method to quantify prey
consumed differs among species. These instruments have been used frequently on
free-ranging marine mammals (Andrews,
1998; Austin et al.,
2006; Hedd et al.,
1995; Lesage et al.,
1999), but only limited effort has been made to validate the
technique (Bekkby and Bjørge,
1998; Gales and Renouf,
1993; Hedd et al.,
1996). Owing to the complicated nature of interpreting stomach
temperature data, including the potential need to distinguish between prey and
water ingestion, studies of feeding behavior can be misinterpreted in the
absence of validation (Catry et al.,
2004; Grémillet and
Plös, 1994; Wilson et
al., 1995).
Previous validation studies with marine mammals were limited by small
numbers of study subjects or by small numbers of experiments per animal. Fish,
ice, snow and free water intake could all be identified in four harp seals
(Phoca groenlandica) using changes in stomach temperature
(Gales and Renouf, 1993). In
this study, using only 11 feedings, a significant linear relationship was
found between meal mass and the time it took for stomach temperature to
recover to pre-ingestion temperature. The effects of meal size, fish
temperature and fish size on changes in stomach temperature were also
investigated in two harbor seals Phoca vitulina
(Bekkby and Bjørge,
1998). The response in stomach temperature was significantly
different between these individuals and data from each animal had to be
treated independently, further limiting sample size. Finally, a study
re-examining the use of stomach temperature telemetry with harp seals
(N=7), demonstrated that prey and water consumption could be
identified and distinguished based on changes in stomach temperature
(Hedd et al., 1996).
The previously described studies have attempted to measure the accuracy of
both identifying and quantifying prey consumed, but they have all been limited
to phocid seals (true seals). To date, we are unaware of published research
that has validated the use of stomach temperature records to identify and
quantify prey consumed by an otariid seal (fur seals and sea lions). With
differences in body size, metabolic rate and core body temperature
(Bartholomew, 1954;
Bartholomew and Wilke, 1956;
Nagy, 1987), it is possible
that the changes in stomach temperature, resulting from feeding, differ
between these families.
This study tested the accuracy of stomach temperature telemeters in
identifying prey consumption in both a phocid (northern elephant seal
Mirounga angustirostris) and an otariid (California sea lion
Zalophus californianus) species. In addition, we examined changes in
stomach temperature to determine if the mass of prey consumed could be
estimated and whether estimates differ between species. Based on previous
captive studies (Gales and Renouf,
1993; Hedd et al.,
1996), we hypothesized meal mass will significantly affect the
area above the curve (integral) created by the stomach temperature deflection
(Fig. 1). In addition, based on
the physics of heat transfer, the rate of the warming of stomach contents
should be related to the temperature difference between the animal and the
prey (Wilson et al., 1995).
Therefore, we hypothesize that meal mass will also result in a significant
difference in the area above the curve, adjusted for temperature difference
between the prey and core body temperature
(Ancel et al., 1997). Finally,
because of opportunistic water consumption by northern elephant seals, we
hypothesized water consumption could be distinguished from prey consumption
based on the rate of recovery of stomach temperature
(Catry et al., 2004). By
examining changes in stomach temperature in a controlled environment, it will
be possible to better interpret similar data collected on free-ranging
animals.
|
Materials and methods |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
).
To increase retention time in some animals the telemeter was made bigger
using an oval foam mount [northern elephant seals, 12 cmx16 cmx1.5
cm; California sea lions, 8 cmx12 cmx1.5 cm
(Austin et al., 2006)]. In
order to minimize influence on the telemeter, the foam mount covered less than
30% of the region of the telemeter that conducted heat to the internal
thermistors. When stomach temperature telemeters were expelled, they were
immediately re-administered following the methods described above.
Northern elephant seals, Mirounga angustirostris Gill (N=10) were transported from Año Nuevo State Reserve (CA, USA) to Long Marine Laboratory (LML, University of California, Santa Cruz, CA, USA). Sub-adult male and female elephant seals (approximately 2-3 years of age) were chosen after completion of the annual molt in May-June of 2003, 2004 and 2005. Seals were chosen based on condition, as thin seals with longer new hair growth were more likely to depart for the foraging migration and would potentially be more willing to eat while in captivity. Seals were housed individually in pens with access to haulout areas and saltwater pools (2.3 mx2.3 mx1.1 m or 4.6 mx2.3 mx1.1 m). Pool temperature ranged from 10.9 to 17.8°C, with an average of 14.6±0.06°C.
For transport, and to attach recording equipment, seals were sedated with an initial intramuscular injection of Telazol (Tiletamine hydrochloride and Zolazepam hydrochloride; Fort Dodge Animal Health, Fort Dodge, IA, USA) at 1.0 mg kg-1 based on a visual estimate of mass. Sedation was maintained with intravenous doses of ketamine hydrochloride when necessary (Fort Dodge Animal Health). At the completion of the study, stomach temperature recorders were removed without sedation while the animal was held in a transport cage and animals were released at Año Nuevo State Reserve.
California sea lions Zalophus californianus Lesson (N=13) were rehabilitation animals from The Marine Mammal Center (TMMC, Sausalito, CA, USA). All animals were treated and deemed releasable by TMMC staff veterinarians before starting the study. Animals were held at either TMMC or LML. Adult females or sub-adult males of comparable body mass were selected for the study. To attach the stomach temperature recorder, sea lions were sedated using gas anesthesia (Isoflurane) from a portable anesthesia machine. Animals were briefly restrained to remove the recorder at the end of the study. Sea lions held at LML were returned to the care of TMMC for release or further treatment if necessary. Sea lions were housed individually with a haulout area and either a fresh (TMMC, range 2.2 mx0.8 m to 3.1 mx0.8 m) or saltwater pool (LML, 2.3 mx2.3 mx1.1 m or 4.6 mx2.3 mx1.1 m). Pool temperature ranged from 9.5 to 26.2°C, with an average of 17.5±0.2°C.
Feeding protocols
All animals were fed whole herring (Clupea harengus harengus), and
to mimic natural feeding, all fish were warmed to pool temperature as
determined by inserting a temperature probe into every fish
(±0.1°C; Physitemp Instruments, NJ, USA). Feeding trials were
conducted between 07:00 h and 23:30 h. Animals were fed in the water and had
to consume all fish within 8 min for a trial to be considered successful. Most
feedings were completed in less than 2 min. For each feeding, the times of
first and last fish consumption were recorded. Animals were fed exact
quantities of 0.5, 1.0, 2.0, 3.0 and 4.0 kg (±0.05 kg). Time to next
feeding ranged from a minimum of 70 min to 6 h, depending on meal size and
total food consumed for the day. To determine the minimum time between
feedings, preliminary experiments were conducted with one captive sea lion.
Time to recovery of stomach temperature was calculated and minimum time
between feedings was determined as approximately two times the maximum
recovery time for that animal. Based on this protocol we assumed that each
feeding event was independent from previous feeds. Data from the preliminary
experiments were not included in the analysis because the feeding protocol was
modified for subsequent experiments. Number of feedings per day for northern
elephant seals ranged from 1 to 6, with an average of 2.2±0.9. Sea
lions ate on average 2.9±0.1 meals per day (range 1-6). Animals were
not given access to food outside of feeding experiments.
Stomach temperature analysis
Stomach temperature changes were analyzed using Sable Systems DataCan V
software (Sable Systems, NV, USA). For each drop in stomach temperature, a
group of variables were defined for analysis
(Fig. 1). Initial temperature
was defined as the baseline temperature preceding the sharp decline resulting
from feeding or drinking. Minimum temperature was identified and time to
minimum was calculated as the interval between time at first fish consumption
and the time at minimum temperature. Temperature difference
(
T) was calculated as the difference between pre-ingestion
body temperature and fish (water) temperature. Recovery in the stomach
temperature was determined when temperature became stable over a 10 min period
(±0.1°C). Time at recovery was then defined as the first
temperature reading in the 10 min period. Area above the curve created by the
decline in stomach temperature (area) was calculated using the Sable Systems
software based on a trapezoidal integration algorithm from the initial
temperature to the recovery temperature. When the initial and recovery
temperatures were different, area was calculated based on the methods of
Wilson et al. (Wilson et al.,
1995). Essentially, area was calculated based on the lowest
temperature (initial or recovery) and added to one half of the area above this
curve (Fig. 2).
|
A general linear mixed model was used to test the hypotheses that mass
consumed can be estimated by (1) area or (2) area/T. We tested
a random factor (individual) to examine whether this improved the models, as
it is necessary to know the impact of individual variation when applying these
models to field studies. Models with and without the random factor were
compared using a log-likelihood ratio test. The model with the lowest AIC
(Akaike's information criterion) was selected as the best model, unless there
was no significant difference between models based on the likelihood ratio
test (Burnham and Anderson,
2002). When no impact of individual was found,
r2 values were used to compare area and area/T to
determine which showed the stronger relationship to meal mass. In addition,
when the random factor was considered significant we tested animal mass and
sex as fixed factors.
To determine whether water and prey consumption could be distinguished from
one another we followed published methods
(Catry et al., 2004), using
the equation:
 |
where I is an index of the rate of stomach temperature recovery
(lower I corresponds with faster recovery), t0.5
is the time (s) from the start of the temperature decline to the half-way
point of temperature recovery, and Tinitial is the stomach
temperature prior to deflection from feeding or drinking. In albatross,
I values for liquid consumption were found to be significantly lower
than for prey consumption and I values of less than 30 s
°C-1 always denoted water ingestion
(Catry et al., 2004).
I values were calculated for all water ingestion events and a
subsample of feeding events.
Summary data are reported as means ± s.e.m. Statistical analysis was conducted using SYSTAT 10 (SPSS Inc., 2000) or R2.2.1 (R. Gentleman and R. Ihaka, http://www.r-project.org). All data were tested for normality and homogeneity of variance. Data that were non-normal or displayed unequal variances were log10 or square root transformed. Contrasts were considered significantly different at P<0.05.
|
Results |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Nine adult female and four sub-adult male California sea lions were used for the feeding study. Sea lions ranged in mass from 63.0 to 102 kg (average 80.1±2.6 kg). Sub-adult males were significantly larger than females (F1,12=21.6, P=0.001); however, these animals were within the range of free-ranging adult females and therefore, the difference was not considered biologically significant for the study. Sea lions retained stomach temperature telemeters for 11.8±2.5 days (range 1-53 days). Three animals retained telemeters for the duration of the study (range 10-22 days) and were released without recovering the telemeters.
Core body temperatures, in the absence of feeding or water ingestions, were variable for both species. Northern elephant seals had an average core body temperature of 36.7±0.2°C, with a range of 36.7-37.9°C. California sea lions had an average core body temperature of 38.1±0.1°C, with a range of 38.1-39.0°C. Average core body temperatures were significantly different between species (F1,21=35.9, P<0.001).
Identifying feeding events
For the ten northern elephant seals, 432 feeding events were recorded. Data
from 17 feedings (4.0%) were determined to be unusable because of missed data
points, erroneous values, or instrument failure. Nine feedings (2.1%) showed
no change in stomach temperature (range 0-7.3% per animal, N=6
individuals). Of the feedings that showed no change in stomach temperature,
six were 0.5 kg and the largest meal not identified was 2.0 kg (N=2).
Missed feeding occurred after one or two prior feedings (average
1.2±0.1), however multiple feedings per day were often easily
identified (Fig. 3). This
resulted in an average of 40.5±0.86 feedings analyzed per animal (range
36-46).
|
For the California sea lions, 497 feeding events were recorded. Data from 149 feedings (30.0%) were determined to be unusable due to missed data points, erroneous values, or instrument failure. Thirteen feedings (3.8%) showed no change in stomach temperature (range 0-25%, per animal, N=3 individuals). Eight of the feeds that showed no change in stomach temperature were from one individual. Of the feedings that showed no change, seven were 0.5 kg and 11 were less than or equal to 1.0 kg. The largest meal size not identified was 2.0 kg (N=2). Feedings that showed no change occurred after one to three prior feedings (average 1.9±0.2 meals). This resulted in an average of 38.2±2.4 feedings analyzed per animal (range 7-43).
Water consumption
Since sea lions were held at a rehabilitation facility employing numerous
volunteers with access to the animals, we cannot be completely certain whether
additional drops in stomach temperature were due to water ingestion or extra
feedings by volunteers. These drops in stomach temperature only occurred five
times for all animals in the 133 days of experiments. Conversely, access to
northern elephant seals was limited and all drops in stomach temperature
outside of feeding experiments were assumed to be water consumption
(N=49, Fig. 3). One
northern elephant seal showed no water ingestion events, while the other nine
animals consumed water on average 5.8±1.3 times during the study (range
2-13). Water consumption occurred on 9.1 to 43.8% of the days in captivity
(average 20.0±4.6%). When animals consumed water, it occurred
1.4±0.1 times per day (range 1-6 ingestions per day) and
70.1±8.2% of the time in the morning prior to the first feed (range for
individuals 33.3-100%).
Water consumption (N=49) resulted in significantly lower
I values than fish consumption (N=97,
F1,142=79.2, P<0.01). I values for
fish ranged from 55.1 to 4380.0 s °C-1 and water ranged from
37.8 to 764.0 s °C-1. To distinguish between fish and water
consumption we used a threshold of 250 s °C-1, which resulted
in the lowest error rate, with fish consumption being accurately identified
83.5% (N=81) of the time and water misidentified as fish 30.6% of the
time (N=15). There was no relationship between meal size and
misclassification (
2=3.4, P=0.50). Water ingestions
showed a faster overall recovery time and smaller area than the smallest meal
consumed (0.5 kg; Table 1).
|
Quantifying feeding events
Feeding events resulted in an average drop in temperature of
4.7±0.1°C and 4.4±0.1°C, for northern elephant seals and
California sea lions, respectively. For both species, quantity consumed
resulted in differences in all of the variables measured for both species
(Table 1).
For northern elephant seals, there was a relationship between meal mass and
both 
area and area/T
(Table 2). There was no
significant effect of individual for these relationships (area:
log-likelihood ratio=1.92, d.f.=1, P=0.17,
area/T: log-likelihood ratio=0.88, d.f.=1,
P=0.35). Based on r2 values
area/T shows a slightly stronger relationship with meal
size (area: r2=0.29, area/T:
r2=0.30; Fig.
4). Therefore, the best equation to estimate quantity consumed is:
quantity= 0.57(area/T)-0.12.
|
|
For California sea lions, both area and area/T were
also related to meal mass. Unlike northern elephant seals, there was a
significant effect of individual for both models (area: log-likelihood
ratio=131.9, d.f.=1, P<0.01, area/T:
log-likelihood ratio=53.0, d.f.=1, P<0.01). The impact of
individual was not a result of animal mass or sex, as these parameters
resulted in higher AIC values. Since it was not possible to account for the
impact of individual, the two best models that explain quantity consumed are:
quantity= 0.028(area)-0.13 and
quantity=0.67(area/T)-0.54. The equation based on area
adjusted for temperature (area/T) was not significantly
different from the equation calculated for the northern elephant seals
(Fig. 4; 95% confidence
intervals for elephant seals: slope 0.56-0.79, constant -1.02 - -0.06).
To test the use of these equations to predict meal size we calculated the percentage error between actual mass and estimated mass. Owing to the variability in stomach temperature responses, the percentage error was high, at 76.9±4.8% for northern elephant seals, and 79.9±5.2% for California sea lions. However, the largest proportion of this error was for feedings of 0.5 kg and resulted from meal mass being overestimated for the smallest meals. When feedings of 1.0 to 4.0 kg were examined the error improves to 42.5±2.3% and 45.6±2.6%, for elephant seals and sea lions, respectively.
|
Discussion |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
; Bekkby and Bjørge,
1998; Gales and Renouf,
1993; Hedd et al.,
1995; Hedd et al.,
1996; Lesage et al.,
1999), only one study used this technology with otariid seals
(Andrews, 1998). Previous
studies using stomach temperature measurement technology to measure feeding
have described its challenges in detail
(Ancel et al., 1997;
Grémillet and Plös,
1994; Wilson et al.,
1992; Wilson et al.,
1995). Among these challenges are: retaining the stomach
temperature telemeter in the animal, and identifying feeding as the stomach
fills (Ancel et al., 1997;
Austin et al., 2006;
Grémillet and Plös,
1994; Wilson et al.,
1995). In the present study, retention times for the stomach
temperature telemeter averaged 7 days for elephant seals and 12 days for sea
lions. Retention time varied among individuals as some regularly lost
telemeters in 1 to 3 days, while others retained telemeters for the length of
the study (greater than 22 days). Therefore, the successful use of stomach
temperature telemetry in free-ranging animals requires further study to find a
reliable method of increasing retention time.
The process of identifying and quantifying prey consumed could also be
influenced by many factors such as the location of the telemeter in the
stomach, the amount of stomach mixing, and the animals' activity level
(Wilson et al., 1995). In
addition, the prey species, and more specifically the composition of the prey
(fish versus squid) is likely to influence the warming process in the
stomach (Wilson et al., 1995).
Both northern elephant seals and California sea lions consume fish and squid
species (Antonelis et al.,
1984; Antonelis et al.,
1987; Condit and Le Boeuf,
1984; Lowry and Carretta,
1999; Lowry et al.,
1991), which may have different thermal and digestive properties.
For consistency, all animals in the present study were fed the same fish
(herring), which has a similar body composition as other prey species found in
the diet these two animals (Antonelis et
al., 1984; Antonelis et al.,
1987; Condit and Le Boeuf,
1984; Lowry and Carretta,
1999; Lowry et al.,
1991).
Despite the limitations of stomach temperature technology, its use can
still provide valuable information about the foraging behavior of free-ranging
seals and sea lions that is currently not available for many species
(Andrews, 1998;
Austin et al., 2006;
Hedd et al., 1995;
Lesage et al., 1999).
Identifying consumption
For both species, the identification of feeding occurred with high accuracy
(97.9% northern elephant seals, 96.2% California sea lions). Feedings that
were not identified tended to be small meals of 1.0 kg or less. Although it is
not known what a `normal' meal size is for either species in the wild, it
appears that stomach temperature telemetry can accurately be used to identify
prey consumed when feeding events are separated in time. Interestingly, the
ability to identify ingestion appears to differ among individuals, as one sea
lion had a much greater number of unidentified feedings than the others. In
addition, although feeding regimes were similar for all animals, four elephant
seals and seven sea lions did not have unidentified feedings. It is not known
whether this variation was a result of differences in activity level between
individuals, location of the telemeter in the stomach, or other factors not
measured in this study.
In addition to identifying feeding events, it was possible to distinguish
between prey and water consumption with a relatively high accuracy in northern
elephant seals. In grey-headed albatross Thalassarche chrysostoma, an
index of the rate of recovery of stomach temperature (I) was used to
distinguish between prey and water ingestion, with 100% accuracy
(Catry et al., 2004). However,
with the small sample size evaluated (N=6 water, N=8
feeding), the authors may not have measured the full variation in recovery
rates. Although our accuracy was not as high (16.5% of fish ingestion and
30.6% water ingestion misclassified), previous research suggests free-ranging
phocids can maintain water balance without free water consumption
(Depocas et al., 1971;
Ortiz, 2004). Studies with
northern elephant seals during both molt and lactation have also found that
animals do not consume water during these fasting periods on land
(Costa et al., 1986;
Worthy et al., 1992).
Therefore, the small possibility of misidentification of water consumption as
prey may not be a problem when deciphering northern elephant seal stomach
temperature data for free-ranging animals.
Quantifying consumption
Previous research with seabirds and marine mammals have used a variety of
factors to quantify prey consumed, such as recovery time, total area created
by the deflection, and area for only the recovery phase
(Fig. 1B-C)
(Ancel et al., 1997;
Bekkby and Bjørge, 1998;
Catry et al., 2004;
Gales and Renouf, 1993;
Grémillet and Plös,
1994; Hedd et al.,
1996; Pütz et al.,
1998). Ancel et al. (Ancel et
al., 1997) found a significant relationship when the difference
between prey temperature and body temperature was incorporated in the estimate
of meal mass (area=massxtemp). For elephant seals this equation
provided the best-fit model for estimating mass consumed
[quantity=0.57(area/T)-0.12]. Given that it is possible
to measure environmental temperature when dive recorders are used in
conjunction with stomach temperature recorders, and fish temperature is
similar to the temperature of the environment, all the necessary parameters
can be acquired to estimate quantity consumed.
As observed for northern elephant seals, both the area under the curve created by the change in stomach temperature and the area adjusted for temperature difference, were related to mass consumed for sea lions. However, unlike elephant seals, there was a significant effect of individual in both models (Table 2). This difference between individuals was not related to sea lion mass or sex but could be a result of a variety of variables not measured in this study, including differences in metabolic rates, stomach churning, or activity levels. For sea lions, the model using area corrected for temperature difference was not significantly different from that for the northern elephant seals. Therefore, we suggest using area corrected for temperature to estimate mass consumed. Although the added uncertainty of individual differences makes the estimate of meal mass more variable, the similar relationship between stomach temperature change and quantity fed for both species provides support for the use of this technology to estimate mass consumed in free-ranging pinnipeds.
As previously stated, the goal of this study was to examine independent
feeding events to test the accuracy of identifying consumption and to
determine a method of estimating mass consumed. However, it is important to
note that the nature of feeding behavior in the wild may strongly influence
the ability to detect and quantify prey consumed when using stomach
temperature. Both northern elephant seals and California sea lions show bout
structure in their diving behavior, suggesting prey consumption occurs within
distinct windows of time (Feldkamp et al.,
1989; Le Boeuf et al.,
1988; Le Boeuf et al.,
1992). To estimate mass consumed using the equations presented in
this study it is necessary to identify the time to recovery
(Fig. 1C) as this is used to
calculate area above the curve (Fig.
1). If animals feed during the recovery period this disrupts the
recovery curve and could influence the ability to estimate mass consumed. By
comparing recovery times with the diving behavior measured in free-ranging
animals it is possible to examine the extent of feeding that might occur
during the recovery period.
Northern elephant seal females dive on average for 20 min
(Kuhn, 2006;
Le Boeuf et al., 1988;
Le Boeuf et al., 2000).
Therefore, for the recovery period to be unaltered by further feedings,
animals would have to feed only once every four dives, for the range of meal
sizes examined. Although foraging success rates are not known for northern
elephant seals, grey seals have been reported to feed on average just twice
per day (Austin et al., 2006).
For California sea lions dive times average 2.2±0.2 min
(Kuhn, 2006). In order to
measure full recovery periods unaltered by additional feeding events, feedings
for this species would have to be separated by 25-45 dives. Since females
average 54 dives in a foraging bout
(Feldkamp et al., 1989), it is
unlikely that they would only successfully capture prey on one or two dives
while foraging. Therefore, while consecutive feeding events may be identified
(Fig. 3)
(Austin et al., 2006;
Grémillet and Plös,
1994; Pütz et al.,
1998), it is necessary to consider the impacts of bout feeding
when estimating quantity consumed by California sea lions.
Recent data from stomach temperature telemeters in free-ranging animals of
both species show feeding does occur in bouts, but animals also display single
feeding events separated in time by further consumption
(Kuhn, 2006) (C.E.K. and
D.P.C., unpublished). For these single feeding events the application of the
equations presented here could provide an estimate of quantity consumed. For
bout feeding periods, additional models are required if researchers are
interested in estimating the mass of prey consumed
(Wilson et al., 1995).
Conclusions
Without the ability to identify when and where an animal feeds it is
difficult to truly understand foraging behavior. Using instruments to measure
feeding events, it is possible not only to fill these gaps, but also to test
the validity of the indirect methods currently used to examine foraging
behavior, such as changes in dive shape or movement patterns. For northern
elephant seals, a great deal of information has been gathered on at-sea
behavior through the use of time-depth recorders and satellite telemetry
(Crocker et al., 2006;
Le Boeuf et al., 1988;
Le Boeuf et al., 2000;
Le Boeuf and Laws, 1994).
Using specific changes in behavior, `focal' foraging areas have been
identified during foraging migrations (Le
Boeuf et al., 2000). To date, the extent of foraging within these
`focal' areas versus outside these areas is still not known, and
direct measures of feeding behavior can help provide the answer.
Because of the variability measured in stomach temperature change
(Fig. 4) and the potential to
overestimate small meals, we strongly suggest using these data as a tool to
compare feeding behavior, rather than to calculate exact quantities consumed
for both northern elephant seals and California sea lions. In addition,
because of the challenges estimating mass consumed when animals bout feed, the
use of stomach temperature change to estimate meal size appears to be most
effective with animals that feed on single large prey, such as albatrosses or
grey seals (Halichoerus grypus)
(Weimerskirch et al., 2005;
Weimerskirch and Wilson, 1992;
Austin et al., 2006). For
example, in grey seals significant sex differences were described for both
feeding frequency and estimated meal size, using stomach temperature change
(Austin et al., 2006). This
type of analysis could provide a great opportunity to compare feeding behavior
between sexes, individuals, seasons or years. In addition to addressing
questions of foraging in the species of interest, measures of feeding behavior
have also been used to examine prey distribution and behavior
(Austin et al., 2006;
Fuiman et al., 2002;
Hennicke and Culik, 2005;
Weimerskirch et al., 2005),
providing greater insight into the behavior of both marine predators and their
prey.
|
Acknowledgments |
|---|
|
References |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Ancel, A., Horning, M. and Kooyman, G. L. (1997). Prey ingestion revealed by oesophagus and stomach temperature recordings in cormorants. J. Exp. Biol. 200,149 -154.[Abstract]
Andrews, R. D. (1998). Remotely releasable instruments for monitoring the foraging behaviour of pinnipeds. Mar. Ecol. Prog. Ser. 175,289 -294.
Antonelis, G. A., Fiscus, C. H. and DeLong, R. L. (1984). Spring and summer prey of California sea lions, Zalophus californianus, at San Miguel Island, California, 1978-79. Fish. Bull. 82,67 -76.
Antonelis, G. A., Lowry, M. S., Demaster, D. P. and Fiscus, C. H. (1987). Assessing northern elephant seal feeding-habits by stomach lavage. Mar. Mamm. Sci. 3, 308-322.[CrossRef]
Austin, D., Bowen, W. D., McMillan, J. I. and Boness, D. J. (2006). Stomach temperature telemetry reveals temporal patterns of foraging success in a free-ranging marine mammal. J. Anim. Ecol. 75,408 -420.
Bartholomew, G. (1954). Body temperature and respiratory heart rates in the northern elephant seal. J. Mammal. 35,211 -218.[Medline]
Bartholomew, G. and Wilke, F. (1956). Body temperature in the northern fur seal, Callorhinus ursinus. J. Mammal. 37,327 -337.[CrossRef]
Bekkby, T. and Bjørge, A. (1998). Variation in stomach temperature as indicator of meal size in harbor seals, Phoca vitulina. Mar. Mamm. Sci. 14,627 -637.[CrossRef]
Boyd, I. L. and Croxall, J. P. (1996). Dive durations in pinnipeds and seabirds. Can. J. Zool. 74,1696 -1705.
Burnham, K. P. and Anderson, D. R. (2002). Model Selection and Multimodel Inference: A Practical Information-theoretic Approach. New York: Springer.
Catry, P., Phillips, R. A., Phalan, B., Silk, J. R. D. and Croxall, J. P. (2004). Foraging strategies of grey-headed albatrosses Thalassarche chrysostoma: integration of movements, activity and feeding events. Mar. Ecol. Prog. Ser. 280,261 -273.
Condit, R. and Le Boeuf, B. J. (1984). Feeding-habits and feeding grounds of the northern elephant seal. J. Mammal. 65,281 -290.[CrossRef]
Costa, D. P. (1993). The secret life of marine mammals: novel tools for studying their behavior and biology at sea. Oceanography 6,120 -128.
Costa, D. P., Le Boeuf, B. J., Huntley, A. C. and Ortiz, C. L. (1986). The energetics of lactation in the northern elephant seal Mirounga angustirostris. J. Zool. Series A 209,21 -34.
Crocker, D., Costa, D., Le Boeuf, B. J., Webb, P. M. and Houser, D. S. (2006). Impact of El Niño on the foraging behavior of northern elephant seals. Mar. Ecol. Prog. Ser. 309,1 -10.
Depocas, F., Hart, J. and Fisher, H. D. (1971). Seawater drinking and water flux in starved and fed harbor seals, Phoca vitulina. Can. J. Physiol. Pharmacol. 49, 53-62.[Medline]
Feldkamp, S. D., Delong, R. L. and Antonelis, G. A. (1989). Diving patterns of California sea lions, Zalophus californianus. Can. J. Zool. 67,872 -883.
Fuiman, L. A., Davis, R. W. and Williams, T. M. (2002). Behavior of midwater fishes under the Antarctic ice: observations by a predator. Mar. Biol. 140,815 -822.[CrossRef]
Gales, R. and Renouf, D. (1993). Detecting and measuring food and water-intake in captive seals using temperature telemetry. J. Wildl. Manage. 57,514 -519.
Grémillet, D. J. H. and Plös, A. L.
(1994). The use of stomach temperature records for the
calculation of daily food-intake in cormorants. J. Exp.
Biol. 189,105
-115.
Hedd, A., Gales, R. and Renouf, D. (1995). Use of temperature telemetry to monitor ingestion by a harbor seal mother and her pup throughout lactation. Polar Biol. 15,155 -160.
Hedd, A., Gales, R. and Renouf, D. (1996). Can stomach temperature telemetry be used to quantify prey consumption by seals? A re-examination. Polar Biol. 16,261 -270.[CrossRef]
Hennicke, J. C. and Culik, B. M. (2005). Foraging performance and reproductive success of Humboldt penguins in relation to prey availability. Mar. Ecol. Prog. Ser. 296,173 -181.
Hindell, M. A., Slip, D. J. and Burton, H. R. (1991). The diving behavior of adult male and female southern elephant seals, Mirounga leonina (Pinnipedia, Phocidae). Aust. J. Zool. 39,595 -619.[CrossRef]
Klimley, A. P., Le Boeuf, B. J., Cantara, K. M., Richert, J. E., Davis, S. F., Van Sommeran, S. and Kelly, J. T. (2001). The hunting strategy of white sharks (Carcharodon carcharias) near a seal colony. Mar. Biol. 138,617 -636.[CrossRef]
Kooyman, G. L. (1965). Techniques used in measuring diving capacities of Weddell seals. Polar Rec. 12,391 -394.
Kooyman, G. L. (1989). Diverse Divers: Physiology and Behavior. Berlin: Springer-Verlag.
Kuhn, C. E. (2006). Measuring Feeding to Understand the Foraging Behavior of Pinnipeds. PhD thesis, University of California, Santa Cruz, USA.
Le Boeuf, B. J. and Laws, R. M. (1994). Elephant Seals: Population Ecology, Behavior and Physiology. Berkeley: University of California Press.
Le Boeuf, B. J., Costa, D. P., Huntley, A. C. and Feldkamp, S. (1988). Continuous, deep diving in female northern elephant seals, Mirounga angustirostris. Can. J. Zool. 66,446 -458.
Le Boeuf, B. J., Naito, Y., Asaga, T., Crocker, D. and Costa, D. P. (1992). Swim speed in a female northern elephant seal - metabolic and foraging implications. Can. J. Zool. 70,786 -795.
Le Boeuf, B. J., Crocker, D. E., Costa, D. P., Blackwell, S. B., Webb, P. M. and Houser, D. S. (2000). Foraging ecology of northern elephant seals. Ecol. Monogr. 70,353 -382.[CrossRef]
Lesage, V., Hammill, M. O. and Kovacs, K. M. (1999). Functional classification of harbor seal (Phoca vitulina) dives using depth profiles, swimming velocity, and an index of foraging success. Can. J. Zool. 77, 74-87.[CrossRef]
Lowry, M. S. and Carretta, J. V. (1999). Market squid (Loligo opalescens) in the diet of California sea lions (Zalophus Californianus) in Southern California (1981-1995). CalCOFI Rep. 40,196 -207.
Lowry, M. S., Stewart, B. S., Heath, C. B., Yochem, P. K. and Francis, J. M. (1991). Seasonal and annual variability in the diet of California sea lions Zalophus californianus at San Nicolas Island, California, 1981-86. Fish. Bull. 89,331 -336.
McConnell, B. J., Fedak, M. A., Lovell, P. and Hammond, P. S. (1999). Movements and foraging areas of grey seals in the North Sea. J. Appl. Ecol. 36,573 -590.[CrossRef]
Nagy, K. A. (1987). Field metabolic-rate and food requirement scaling in mammals and birds. Ecol. Monogr. 57,111 -128.[CrossRef]
Ortiz, R. M. (2004). Osmoregulation of marine mammals. J. Exp. Biol. 204,1831 -1844.
Pütz, K., Wilson, R. P., Charrassin, J. B., Raclot, T., Lage, J., Le Maho, Y., Kierspel, M. A. M., Culik, B. M. and Adelung, D. (1998). Foraging strategy of king penguins (Aptenodytes patagonicus) during summer at the Crozet Islands. Ecology 79,1905 -1921.[CrossRef]
Ropert-Coudert, Y., Baudat, J., Kurita, M., Bost, C. A., Kato, A., Le Maho, Y. and Naito, Y. (2000). Validation of oesophagus temperature recording for detection of prey ingestion on captive Adelie penguins (Pygoscelis adeliae). Mar. Biol. 137,1105 -1110.[CrossRef]
Sepulveda, C. A., Kohin, S., Chan, C., Vetter, R. and Graham, J. B. (2004). Movement patterns, depth preferences, and stomach temperatures of free-swimming juvenile mako sharks, Isurus oxyrinchus, in the Southern California Bight. Mar. Biol. 145,191 -199.
Shaffer, S. A. and Costa, D. P. (2006). A database for the study of marine mammal behavior: gap analysis, data standardization, and future directions. IEEE J. Oceanic Eng. 31,82 -86.[CrossRef]
Simeone, A. and Wilson, R. P. (2003). In-depth studies of Magellanic penguin (Spheniscus magellanicus) foraging: can we estimate prey consumption by perturbations in the dive profile? Mar. Biol. 143,825 -831.[CrossRef]
Tanaka, H., Sato, K., Matsuzawa, Y., Sakamoto, W., Naito, Y. and Kuroyanagi, K. (1995). Analysis of possibility of feeding of loggerhead turtles during internesting periods based on stomach temperature-measurements. Nippon Suisan Gakkai Shi 61,339 -345.
Weimerskirch, H. and Wilson, R. P. (1992). When do wandering albatrosses Diomedea exulans forage. Mar. Ecol. Prog. Ser. 86,297 -300.
Weimerskirch, H., Gault, A. and Cherel, Y. (2005). Prey distribution and patchiness: factors in foraging success and efficiency of wandering albatrosses. Ecology 86,2611 -2622.
Wilson, R. P., Cooper, J. and Plotz, J. (1992).
Can we determine when marine endotherms feed - a case-study with seabirds.
J. Exp. Biol. 167,267
-275.
Wilson, R. P., Pütz, K., Grémillet, D., Culik, B. M., Kierspel, M., Regel, J., Bost, C. A., Lage, J. and Cooper, J. (1995). Reliability of stomach temperature changes in determining feeding characteristics of seabirds. J. Exp. Biol. 198,1115 -1135.[Abstract]
Worthy, G. A., Morris, P. A., Costa, D. P. and Le Boeuf, B. J. (1992). Moult energetics of the northern elephant seal (Mirounga angustirostris). J. Zool. 227,257 -265.
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
