Bioenergetics and diving activity of internesting leatherback turtles Dermochelys coriacea at Parque Nacional Marino Las Baulas, Costa Rica
1 Drexel University, Department of Bioscience and Biotechnology, 3141
Chestnut Street, Philadelphia, PA 19104 USA
2 Indiana-Purdue University, Department of Biology, 2101 E. Coliseum Blvd,
Fort Wayne, IN 46805 USA
3 Cornell University, Department of Natural Resources, Ithaca, NY
14853
4 Lotek Wireless, Inc., St John's, Newfoundland, Canada A1C 1Z8
* Author for correspondence at present address: Duke University Marine Laboratory, Nicholas School of Environmental and Earth Sciences, 135 Duke University Marine Lab Road, Beaufort, NC 28516, USA (e-mail: bwallace{at}duke.edu)
Accepted 25 August 2005
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Summary |
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Key words: leatherback turtle, Dermochelys coriacea, bioenergetics, field metabolic rate, diving physiology
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Introduction |
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Leatherback turtles Dermochelys coriacea Vandelli 1761 are
critically endangered (Spotila et al.,
2000) and range circumglobally from sub-polar to tropical waters
(Goff and Lien, 1988
;
Paladino et al., 1990
). Their
unique thermoregulatory adaptations (Frair
et al., 1972
; Greer et al.,
1973
; Paladino et al.,
1990
), pan-oceanic migrations
(Morreale et al., 1996
; Hays
et al.,
2004a
,b
;
Ferraroli et al., 2004
),
prodigious growth rate (Zug and Parham,
1996
), reproductive output
(Reina et al., 2002b
) and size
(200900 kg) make quantification and understanding of the
energyactivity trade-offs of the species' distinctive physiology,
movements, and life history crucial to their conservation.
Leatherbacks utilize gigantothermy a suite of physiological
adaptations including low metabolic rate, large thermal inertia, blood flow
adjustments and peripheral insulation to maintain elevated body
temperatures in cold water and avoid overheating in the tropics
(Paladino et al., 1990). Such
thermal tolerance probably allowed leatherbacks to exploit an ecological niche
unavailable to other marine turtle species, similar to the thermal niche
expansion theory proposed by Block et al.
(1993
) to explain the multiple
and diverse origins of endothermy in the Family Scombroidei (tunas, billfish).
Leatherback metabolic rate (MR) during nesting is intermediate between
reptilian and mammalian resting metabolic rates (RMRs) scaled to leatherback
size (Paladino et al., 1990
,
1996
). However, all metabolic
measurements have been on adult leatherbacks during nesting, walking on the
beach, or while restrained in nets (Lutcavage et al.,
1990
,
1992
; Paladino et al.,
1990
,
1996
), and not during in-water
activities that constitute the vast majority of the lifespan of adult
leatherbacks. Therefore, quantification of metabolic rates for free-swimming
leatherbacks would provide ecologically relevant measures of energy
expenditure during at-sea activity.
The energetic costs of activity and maintenance physiological processes
during the internesting period are unknown. Internesting leatherbacks swim
continuously, displaying distinct swim-speed patterns for diving and traveling
(Eckert, 2002;
Reina et al., 2005
;
Southwood et al., 2005
), in
contrast to hypotheses that turtles rest or bask for extended periods at or
near the surface (Eckert et al.,
1986
,
1989
;
Southwood et al., 1999
).
Leatherbacks exhibit distinct dive patterns during different activities. For
instance, U-shaped dives, during which turtles decrease activity on or near
the ocean bottom, are thought to serve a resting or energy conservation
purpose, in contrast to V-shaped dives, which appear to serve mainly a transit
purpose (Reina et al., 2005
).
Southwood et al. (1999
)
hypothesized that leatherback metabolism at sea might be higher than during
oviposition due to other costs (reproduction, swimming, foraging, etc.);
however, swimming in other vertebrates is more energetically efficient than
walking (Schmidt-Nielsen,
1972
) and elevated water temperatures in the tropics might
constrain leatherback activity due to the possibility of overheating, as
reported for giant bluefin tuna (Blank et
al., 2004
). Furthermore, given the competing reproductive energy
requirements of round-trip migration between foraging and nesting grounds, egg
production and nesting, and internesting activity at sea, leatherbacks should
conserve energy while at sea during the internesting period in order to
enhance their seasonal reproductive success.
Aerobic dive limit (ADL) can provide estimates of physiological and
energetic constraints on activity in air-breathing, diving animals
(Costa et al., 2001). The ADL
concept specifically refers to the dive duration beyond which blood lactate
levels increase above resting levels
(Kooyman et al., 1980
).
However, direct measurements of post-dive blood lactate concentrations are
difficult to obtain from free-swimming animals, so many reports combine data
on individual total oxygen stores and at-sea metabolic rates to obtain
calculated aerobic dive limits (cADL; for a review, see
Costa et al., 2001
).
Leatherback respiratory and cardiovascular physiology allows for deep and
prolonged diving (Lutcavage et al.,
1990
; Paladino et al.,
1996
), with the deepest recorded dive to 1230 m
(Hays et al., 2004b
) and the
longest dive duration in excess of 1 h
(Southwood et al., 1999
).
Lutcavage et al. (1992
)
combined measurements of nesting leatherback metabolic rates, blood
O2-carrying capacity and tissue myoglobin concentration
(Lutcavage et al., 1990
) with
data on blood and lung volumes to calculate total O2 stores of 27
ml kg1, and estimated that leatherback cADL was between
570 min. Southwood et al.
(1999
) recorded the longest
dive duration for a leatherback (67.3 min) and refined the cADL estimate to
3367 min, based on heart rates and dive patterns of free-swimming adult
female leatherbacks during the internesting period. In order to better
estimate the cADL, however, measurements of metabolic rates of free-swimming
leatherbacks are necessary.
Using conventional respirometry to measure metabolic rates of free-ranging
marine animals is logistically infeasible in most cases. However, the doubly
labeled water (DLW) method has proved a useful tool for studying field
energetics and diving activity of marine animals
(Costa, 1988;
Arnould et al., 1996
; Costa and
Gales, 2000
,
2003
). The DLW method
estimates CO2 production (rCO2) from the divergence
between washout curves of hydrogen (deuterium, D or tritium, T) and oxygen
(18-oxygen, 18O) isotopes introduced into an animal's total body
water (Lifson et al., 1955
).
Disadvantages of the method include the high cost of the isotopes and the
reliance of the method on significant divergence of the isotope washout curves
that is created by a relatively higher rCO2 than water turnover
rate (rH2O). The accuracy of the DLW method decreases considerably
as the ratio of rCO2 to rH2O decreases
(Butler et al., 2004
). Although
the DLW method has been used to measure the field metabolic rate (FMR) and
water turnover of many terrestrial reptilian species (for a review, see
Speakman, 1997
), Booth
(2002
) concluded that DLW would
not work for aquatic turtles because their water turnover rates are too high
(approximately 1.64.3xTBW day1, where TBW=total
body water). Clusella Trullas et al. (in
press
) recently reported DLW-derived FMRs and water turnover rates
during dispersal in hatchling olive ridley turtles Lepidochelys
olivacea, but there are no published reports of DLW being used to
quantify the FMRs of free-swimming adult marine turtles. However, since marine
turtles face a different osmoregulatory challenge from freshwater turtles, and
osmoregulate efficiently (Reina,
2000
; Reina et al.,
2002a
), they should have a lower water turnover rate than their
freshwater counterparts and sufficient divergence in the isotopes should occur
to allow measurement of FMRs in this species.
Therefore, using highly enriched DLW, we measured for the first time the FMRs and water turnover rates for free-swimming adult marine turtles and used electronic archival tags to record diving activity of 18 adult female leatherbacks during the internesting period. Here we combine metabolic and diving data to examine relationships between physiology, environment and activity in leatherbacks.
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Materials and methods |
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Because the DLW method requires recapture to measure final plasma isotope
levels, and female leatherbacks at PNMB nest on average 68 times in a
season (Reina et al., 2002b),
we selected female turtles that were early in their nesting season (first to
fourth nest), to ensure return and recapture upon subsequent nesting. We took
a final blood sample (
5 ml) from a rear flipper and albumen samples from
shelled albumen gobs (SAGs; Wallace et
al., 2004
) when the turtles returned to nest in order to measure
final isotope concentrations remaining in turtle body water at the end of the
study period. While recent blood biochemistry analyses on reptiles indicate
more variability in samples taken from hind limbs than from jugular veins
(Jacobson et al.,
http://accstr.ufl.edu/blood_chem.htm),
we found that isotopic concentrations in samples taken from the hind flippers
were similar to those from the cervical sinus. We sampled mainly from a rear
flipper because it was a less invasive procedure and we only needed small
volumes of blood. All blood and albumen samples were later analyzed for
D2 and 18O isotope concentrations by Metabolic
Solutions, Inc. (Nashua, NH, USA), which ensures the accuracy of their
analyses to 2% of 1 S.D. for deuterium and 0.4% of 1
S.D. for 18O.
We calculated total body water (TBW) from oxygen dilution space and water
turnover (rH2O) using TBW derived from deuterium dilution space
(Speakman, 1997). We
calculated CO2 production (rCO2) assuming an RQ of 0.7
for nesting leatherbacks (Paladino et al.,
1996
) and using a 2-pool equation 7.43 from Speakman
(1997
), recommended for large
animals.
We used LTD (lighttemperaturedepth) 2310 archival tags (Lotek
Wireless, Inc., Newfoundland, Canada) attached to the anterior portion of the
pygal process (Morreale, 1999)
of 18 turtles, four of which were also subjects of the DLW experiments, to
record their diving activity. The LTDs were programmed to record time, depth,
water temperature and light level data at intervals of 460 s (depending
on the tag) and had a maximum depth rating of 2000 m, with 1% accuracy to full
scale. We analyzed dive data using Surface Adjust and Dive Analysis Programs
from Lotek Wireless, Inc. To improve the reliability of classifying true
surfacing events for the purposes of dive analysis, the automated Surface
Adjust program was arbitrarily limited to search within areas of the data
containing readings of <10 m when referenced to the daily minimum depth
value. This assumes that the zero offset error on any given day will be not
fluctuating by more than 10 m. Regions of data that met this condition were
processed and the median depth values determined as estimates of the zero
offset error. The zero offset error for a given dive was then calculated by
averaging the median value from the surface events that preceded and followed
each dive.
Once the depth data were adjusted based on the zero offset, the entire data
set was processed by Dive Analysis, which classified surfacing events as those
regions of the data where the corrected depth records were exactly zero. We
further filtered the adjusted data and accepted only dives >3 m to limit
our analyses to true diving events. We calculated bottom time as the portion
of a dive at or below 85% of maximum depth. A dive was counted as a U-dive if
the turtle spent 1 min on the `bottom'
(Reina et al., 2005
). Based on
video footage of breathing episodes at the surface
(Reina et al., 2005
), and
because extended surface intervals correspond to traveling periods near the
surface, not necessarily breathing or basking
(Eckert, 2002
), we only
included surface events of >12 s and
20 min in calculation of post-dive
surface intervals. We excluded less than 6% of all surface intervals using
these criteria.
We used least-squares linear regressions to analyze relationships between mean dive variables and Student's t-tests to compare dive variables between treatment groups (DLW vs LTD turtles; SPSS 11.5.1, Chicago, USA), and accepted significance at P=0.05 level. We arcsine transformed percentage data and values are presented as means ± 1 S.D. unless otherwise noted. We conducted all procedures under permits 288-2002-OFAU and 273-2003-OFAU from the Costa Rican Ministerio del Ambiente y Energía (MINAE) and Drexel University IACUC Approval 02183 and 02185.
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Results |
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Diving activity during the internesting period
We recorded diving activity of four of five DLW turtles and 14 `control'
(LTD) turtles, totaling 23 402 total dives. Individual turtles demonstrated
different diving patterns in terms of mean dive variables and water
temperature Tw (Table
2). Across all turtles, mean maximum dive depth was
22.6±7.1 m, with mean dive depth 14.6±4.6 m and mean dive
duration 7.8±2.4 min. The deepest single dive was 200 m(Turtle 16) and
the longest was 44.9 min (Turtle 2). Turtles reached maximum depths of 20
m on approximately 60% of all dives, and approximately 43% of all dive
durations were
5 min. The mean water temperature leatherbacks encountered
was 26.6°C, while the minimum encountered was 13.6°C (Turtle 16).
|
Turtles with LTDs attached that underwent DLW experiments had significantly
longer internesting periods than turtles that only had LTDs attached
(Student's t-test: t17=7.951,
P<0.001; DLW turtles: 13.1±1.4 days, LTD turtles:
9.1±0.8 days). Additionally, DLW turtles spent a significantly higher
proportion of time in Tw24°C than LTD turtles
(t16=3.165, P=0.006; DLW: 16.0±2.6%, LTD:
7.6±5.0%), especially during the early phase of the internesting
period, which directly followed nesting and the restraint portion of the
experiment (t16=3.508, P=0.003; DLW:
25.5±4.5%, LTD: 10.4±6.9%). Furthermore, DLW turtles made
significantly more total dives (t16=3.325,
P=0.004; DLW: 1671±324, LTD: 1194±233), and
particularly more U-dives during the internesting period than LTD turtles
(t16=5.125, P<0.001; DLW: 1206±242,
LTD: 750±130).
FMRs, diving physiology and activity
Although we had a small sample size, (1 FMR for Turtles 1 and 4, 2 FMRs for
Turtle 3), we used statistical analyses (Pearson ProductMoment
Correlation) to examine the relationships between FMR, diving physiology and
activity. We found several suggestive of strong positive relationships between
FMRs and mean dive durations (r2=0.991), bottom times
(r2=0.992), percentage of time spent in
Tw24°C (r2=0.990), and surface
interval (r2=0.999, P=0.027).
Combining the FMRs acquired by us with the value for adult leatherback
total O2 stores reported by Lutcavage et al.
(1992), cADLs for internesting
female leatherbacks were between 11.7 min and 44.3 min
(Table 3A).
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Discussion |
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Adult female leatherbacks in this study exhibited high rH2O
values (1630% TBW), but within the range of values for leatherbacks and
other marine turtle species obtained with isotopically labeled water
(Clusella Trullas et al., in
press; Ortiz et al.,
2001
; Jones et al., in
press
) and by analyses of lachrymal gland secretion rates
(Reina, 2000
;
Reina et al., 2002a
;
Fig. 3). The rH2O
values for female leatherbacks reported here are understandable considering
that internesting leatherbacks produce massive egg clutches, which contain
large amounts of water. Indeed, the female leatherbacks in this study laid
subsequent clutches of approximately 38 kg inmass (B. P. Wallace,
unpublished data). Moreover, leatherbacks possess highly effective
osmoregulatory capabilities that allow them to drink seawater without
incurring negative water and ionic balance
(Reina et al., 2002b
). Turtle
3 exhibited a higher rH2O during the first 3 days of her
internesting period than for the entire 14 days period
(Table 2), which corresponded
to the high frequency of water/prey ingestion events during the first few days
after nesting reported by Southwood et al.
(2005
).
Efficacy of DLW method in studies of marine turtle energetics
While the rH2O values for all turtles in this study were within
the range of water fluxes for other marine turtles
(Fig. 3), we were unable to
calculate FMRs for Females 2 and 5 using DLW. Female 2 turned over 27.2% of
her TBW daily, or nearly 3 times during her 11-day internesting period, while
Female 5 completely washed out the deuterium isotope, also indicating a high
rH2O. In other studies using isotopically labeled water to
calculate rH2O values for olive ridley (Lepidochelys
olivacea; Clusella Trullas et al., in
press), Kemp's ridley (L. kempii;
Ortiz et al., 2001
), and green
turtles (Jones et al., in
press
), no animals turned over their TBW more than 2.5 times
during the study period. Apparently, there exists a threshold ratio of
rCO2 to rH2O (where rH2O must be <27.2%
TBW day1) necessary for the DLW method to be able to measure
rCO2 in leatherbacks and perhaps marine turtles in general.
Validation experiments of the accuracy of the DLW method have been
performed for several animal species over a wide size range (reviewed in
Speakman, 1997). Performing
simultaneous metabolic measurements (DLW and respirometry, for example) on
adult marine turtles is extremely difficult, due to factors such as their
marine lifestyle, large size, endangered status, and the high cost of the
large volume of enriched DLW required. In general, validations indicate that
although individual variation might account for serious discrepancies between
DLW measurements and those acquired by reference methods, the DLW method tends
to overestimate rCO2 by less than 5% among different animal clades
(Butler et al., 2004
). Only one
truly simultaneous validation study has been performed for marine turtles to
date, which reported that the global mean of DLW-derived rCO2
values for juvenile green turtles was not significantly different and only
varied by 5.2% from that obtained by gas respirometry for the same period from
the same animals (Jones et al., in
press
).
A ratio of deuterium to oxygen-18 isotopic washout
(kD:kO) that exceeds 0.9 implies that
90% of oxygen elimination is tied to water losses, and therefore the DLW
method might not accurately quantify CO2 production
(Speakman, 1997
). In this
study, the combination of long study durations, high rH2Os and low
metabolic rates resulted in insufficient divergence (Female 2;
kD:kO=1.04) or complete washout
(Female 5) of the isotopes, rendering the DLW method unable to calculate
rCO2 (Butler et al.,
2004
) for these two leatherbacks. The other
kD:kO ratios that we calculated ranged
from 0.700.93, slightly above or within the recommended range
(Speakman, 1997
). The
relatively high water turnover rates and
kD:kO ratios that we measured indicate
the need for caution when interpreting our results
(Speakman, 1997
;
Butler et al., 2004
). However,
Jones et al. (in press
)
reported kD:kO ratios between
0.840.92 for juvenile green turtles, and the DLW-derived MRs were not
significantly different from MRs obtained by respirometry in that study.
Considering existing DLW validation information
(Jones et al., in press
) and
the fact that our FMRs fell within the range of measured MRs for leatherbacks
during various activities (Paladino et al.,
1990
,
1996
), we conclude that our
measurements were accurate and biologically realistic, despite the lack of
simultaneous validation data via respirometry.
Internesting diving activity
Dives tended to be shorter and shallower for Pacific Costa Rican
leatherbacks (mean durations 78 min, mean depths
1519 m;
Southwood et al., 1999
,
2005
; this study) than dives
for leatherbacks in the Caribbean near St Croix (mean durations
1015 min, mean depths
60100 m; Eckert et al.,
1986
,
1989
;
Eckert, 2002
). Dive variables
from leatherbacks in the South China Sea off Malaysia were intermediate (mean
durations
812 min, mean depths
2645 m;
Eckert et al., 1996
). These
differences were probably due to relatively shallower depths available to
internesting leatherbacks on the continental shelf near PNMB, Costa Rica,
relative to other sites (Morreale,
1999
; Southwood et al.,
1999
). Increasing mean maximum dive depths were associated with
increased mean dive duration and decreased mean dive rates
(Fig. 4), similar to trends
reported for leatherbacks worldwide (Eckert et al.,
1986
,
1996
;
Southwood et al., 1999
;
Reina et al., 2005
). Similar
trends were reported for New Zealand sea lions Phocarctos hookeri
(Costa and Gales, 2000
) and
Australian sea lions Neophoca cinerea
(Costa and Gales, 2003
).
Therefore, while leatherback diving activity patterns appear to be constrained
primarily by different depths encountered in different internesting habitats
(Eckert et al., 1996
;
Morreale, 1999
;
Southwood et al., 1999
), some
general patterns in dive behavior exist globally between and among taxa of
diving animals.
We found that post-dive surface intervals lengthened with increased dive
duration for all dives across all turtles, contrary to some findings (Eckert
et al., 1989,
1996
;
Southwood et al., 1999
; but
see Reina et al., 2005
).
However, this relationship had a low r2 value (0.159),
indicating >80% of the variance in post-dive surface interval durations
that was not explained simply by preceding dive durations. Given the
relatively short dive durations and surface intervals of leatherbacks in this
study, turtles were probably not using the post-dive surface interval to
recover from CO2 accumulation during diving apnea.
Leatherbacks occasionally exhibited extremely long surface intervals
(maxima 21.8108.3 min). These long surface intervals represented
periods of traveling within the upper few meters of the water column, and not
resting or basking behavior, as previously hypothesized (Eckert et al.,
1986,
1989
;
Southwood et al., 1999
). This
is supported by swim speed and location data off Playa Grande
(Southwood et al., 2005
) and
St Croix (Eckert, 2002
) and
video footage (Reina et al.,
2005
) for internesting leatherbacks. Moreover, Penick
(1996
) measured minimal blood
flow to the carapace surfaces of nesting leatherbacks, indicating that
leatherbacks would have limited ability for heat gain while basking.
Leatherbacks that had undergone the experimental handling required by the
DLW methodology had significantly longer internesting periods, made
significantly more U-dives, and spent more time in
Tw24°C than leatherbacks to which we only attached
data loggers. This was especially evident during the early third of the
internesting period. Corticosteroid hormone concentrations increase in
response to stress related to prolonged handling
(Gregory and Schmid, 2001
),
and this can inhibit various physiological functions, including egg production
(Owens, 1997
;
Rostal et al., 2001
; Milton
and Lutz, 2003). Such hormonal inhibition of reproductive function would
account for the extended internesting period of the DLW turtles (13.1 days)
relative to the LTD turtles (9.1 days). Turtle 3 re-emerged 3 days after
nesting, which was probably another manifestation of the hormonal inhibition
of the natural egg production process during the internesting period in
response to this prolonged stress. This turtle went through the entire nesting
process, but did not lay eggs. Although this was a rare occurrence in this
population, the turtle's field metabolic rates (FMRs) were similar to the
others we obtained (Table 1)
and her diving behavior was similar to the behavior of other turtles
(Table 2). Furthermore, Turtle
3 returned to nest successfully 11 days later (14 days after the previous
nesting), which was her fifth and final nest of the season. A season total of
five nests is within the normal range for nesting leatherbacks in this
population (see Reina et al.,
2002b
).
According to Reina et al.
(2005), U-dives chiefly serve
a resting purpose, and almost 20% of these dives involve the turtles remaining
stationary on the ocean bottom for up to 1 min. Furthermore, Southwood et al.
(2005
) reported decreases in
body temperature Tb during relative inactivity on or near
the ocean bottom, indicating physiological heat dissipation. For all turtles
in our study, as the number of U-dives that turtles made increased, so did the
percentage of time spent in Tw
24°C
(r2=0.311, P=0.016). However, DLW turtles made
significantly more U-dives than LTD turtles
(Table 2), thus accounting for
the increased percentage of time that DLW turtles spent in colder waters than
LTD turtles. We hypothesize that the prolonged restraint in cargo nets and
sequential blood-drawing procedures caused the experimental turtles to incur
elevated corticosteroid levels and increased heat loads, which resulted in
protracted internesting periods and compensatory thermoregulatory behavior
during the first few days at sea after the experiment. What effects, if any,
the experimental stress had on the FMR values themselves is unknown,
especially since DLW-derived FMRs are integrations of metabolism during the
entire study period, not for particular activities. However, DLW turtles
performed within the range of dive variables for all turtles
(Table 2), indicating that
their diving activities (and presumably their FMRs) were representative of
internesting leatherbacks in general. It is important to point out that DLW
turtles returned to nest successfully and also resumed normal internesting
periods after the experiment. While the prolonged restraint was necessary and
the DLW experiment likely imposed stress on leatherbacks, it did not interfere
with their long-term reproduction or behavior. Nonetheless, these factors
should be taken into consideration when conducting this type of experiment
with marine turtles because of their endangered status and the unavoidably
stressful nature of the experiment.
FMRs, diving physiology and activity
Our proposed upper limit on leatherback cADL (44.3 min) corroborates the
findings of Hays et al.
(2004a), who reported an
apparent ceiling on leatherback migratory dive durations at around 40 min.
Mean dive durations for all four DLW turtles were below the cADL range
(11.744.3 min), and DLW turtles exceeded their cADL on only 033%
of their dives (Table 3A). We
then calculated the percentage of dives for all 18 turtles exceeding the lower
(11.7 min) and upper limits (44.3 min) of the FMR-derived cADLs. All turtles
regularly dived below or within the cADL range, and on the average 25% of
dives exceeded the lower limit (Table
3B, Fig. 5). Only
one dive exceeded the upper limit (44.9 min; Turtle 2), but none exceeded the
upper limits proposed by Lutcavage et al. (70 min;
1990
) and Southwood et al. (67
min; 1999
).
|
We found positive relationships between FMRs and mean dive durations,
bottom times, surface intervals, and the proportion of time turtles spent in
Tw24°C (all r2>0.99). These
results raise interesting questions about leatherback thermoregulation, diving
physiology and behavior. Leatherbacks might dive more actively, thereby
increasing metabolic rates (since increased muscle activity automatically
results in higher metabolism) in order to exploit colder waters, presumably to
forage. Eckert et al. (1986
,
1989
,
1996
) hypothesized that
diurnal differences in dive patterns represented foraging activity following
the deep-scattering layer (DSL). However, Hays et al.
(2004a
) pointed out that
leatherbacks migrate great distances away from nesting grounds to increase
foraging success because prey abundance is presumably greater on pelagic
foraging grounds than along tropical coasts. In addition, Reina et al.
(2005
) did not observe any
feeding activity in video footage of the first day after nesting, and
Southwood et al. (2005
) found
no relationship between ingestion events and diel dive patterns, which were
previously thought to be related to vertical movements of the DSL (Eckert et
al., 1986
,
1989
,
1996
). If leatherbacks were
actively foraging, an increase in FMR over RMR of 1030% might be
expected due to specific dynamic action
(Withers, 1992
). However, the
fact that FMRs that we obtained were not significantly elevated relative to
nesting leatherback MRs (Fig.
2) renders the possibility that leatherbacks were foraging during
the internesting period highly unlikely.
According to the gigantothermy model, leatherbacks must maintain low MRs
and increase blood flow to peripheral tissues to dissipate heat generated
internally to avoid overheating in the tropics
(Paladino et al., 1990).
Southwood et al. (2005
)
recorded subcarapace and gastrointestinal tract temperatures of internesting
leatherbacks and surmised that their measured gradients between
Tb and Tw for leatherbacks in the
tropics supported the predictions of the gigantothermy model. While data on
blood flow adjustments by leatherbacks at sea are not available, the
relatively low FMR values that we report in the present study for internesting
leatherbacks reinforce the conclusions of Paladino et al.
(1990
) and Southwood et al.
(2005
). Furthermore, we found
relationships between FMRs, increased activity levels (mean maximum depth,
dive duration, bottom time) and proportion of time spent in
Tw
24°C. This suggests that leatherbacks with
increased activity levels (and perhaps higher metabolic rates) might avoid
overheating while in the tropics by increasing the proportion of time spent in
cool water, thus behaviorally moderating their body temperatures by using
cooler water as a heat sink (Fig.
6). Southwood et al.
(2005
) reported
Tb values that were consistently elevated above
Tw, but Tb could be affected by
modifications in swimming and diving activity and fluctuating
Tw. Tuna also experience limitations on activity in warm
water in the tropics (Blank et al.,
2004
), and modulate heat transfer both physiologically and
behaviorally (Dewar et al.,
1994
). Leatherbacks in this study spent the highest percentage of
time in cooler waters in the early third of the internesting period after
nesting, implying that increased heat loads incurred during increased activity
associated with nesting necessitated shuttling to colder
Tw. Southwood et al.
(2005
) recorded frequent
ingestion events during this segment of the internesting period, potentially
indicating internal heat dissipation through ingestion of cooler water and/or
prey. It is plausible that dive patterns of leatherbacks foraging in cold
waters would be opposite to those for internesting leatherbacks, in that
turtles might spend more time at the surface in warmer water in response to
prolonged periods submerged in colder water, as documented in bigeye
(Holland et al., 1992
) and
bluefin tuna (Gunn and Block,
2001
). Additional experiments simultaneously measuring leatherback
body temperatures, metabolism and diving activity in cold water are needed to
distinguish between these possibilities.
|
In order for female leatherbacks to reproduce, they must harvest and store
sufficient energy to facilitate nest construction, egg production and survival
at sea between nesting events. Of those components, only energy expenditure
during the internesting period can be flexible, since compromises in egg
production and nest construction would decrease reproductive success. The
relatively low FMRs reported here, almost exclusively aerobic diving, and
apparent thermal constraints on activity imposed by warm tropical water
exhibited by leatherbacks in this study, suggest minimized energy expenditure
during the internesting period. This might facilitate increased energy
allocation to egg production and nesting, as reported for internesting green
turtles (Hays et al., 2000).
Future studies should incorporate more data on metabolism, body temperatures
and diving behavior of migrating and foraging turtles in cooler waters in
order to understand how environmental and life history demands affect marine
turtle energetics and activity.
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List of abbreviations |
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Acknowledgments |
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Footnotes |
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References |
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Aquarone, M. (2004). Body composition, field metabolic rate, and feeding ecology of walrus (Odobenus rosmarus) in northeast Greenland. PhD thesis, National Environmental Research Institute, Ministry of the Environment, Denmark.
Arnould, J. P. Y., Boyd, I. L. and Speakman, J. R. (1996). The relationship between foraging behaviour and energy expenditure in Antarctic fur seals. J. Zool. Soc. Lond. 239,769 -782.
Bjorndal, K. A. and Jackson, J. B. C. (2003). Roles of sea turtles in marine ecosystems: reconstructing the past. In The Biology of Sea Turtles, Vol.2 (ed. P. L. Lutz, J. A. Musick and J. Wyneken), pp.259 -274. Boca Raton, FL: CRC Press.
Blank, J. M., Morrissette, J. M., Landeira-Fernandez, A. M.,
Blackwell, S. B., Williams, T. D. and Block, B. A.
(2004). In situ cardiac performance of Pacific bluefin
tuna hearts in response to acute temperature change. J. Exp.
Biol. 207,881
-890.
Block, B. A., Finnerty, J. R., Stewart, A. F. R. and Kidd, J. (1993). Evolution of endothermy in fish: mapping physiological traits on a molecular phylogeny. Science 260,210 -213.[Medline]
Booth, D. T. (2002). The doubly-labeled water technique is impractical for measurement of field metabolic rate in freshwater turtles. Herp. Rev. 33,105 -107.
Butler, P. J., Green, J. A., Boyd, I. L. and Speakman, J. R. (2004). Measuring metabolic rate in the field: the pros and cons of the doubly labelled water and heart rate methods. Func. Ecol. 18,168 -183.[CrossRef]
Clusella Trullas, S., Spotila, J. R. and Paladino, F. V. (in press). Energetics during hatchling dispersal using doubly labelled water. Physiol. Biochem. Zool.
Costa, D. P. (1988). Methods for studying the energetics of freely diving animals. Can. J. Zool. 66, 45-52.
Costa, D. P. and Gales, N. J. (2000). Foraging
energetics and diving behavior of lactating New Zealand sea lions,
Phocarctos hookeri. J. Exp. Biol.
203,3655
-3665.
Costa, D. P. and Gales, N. J. (2003). Energetics of a benthic diver: seasonal foraging ecology of the Australian sea lion, Neophoca cinerea. Eco. Monogr. 73, 27-43.
Costa, D. P., Gales, N. J. and Goebel, M. E. (2001). Aerobic dive limit: how often does it occur in nature? Comp. Biochem. Physiol. 129A,771 -783.
Dewar, H., Graham, J. B. and Brill, R. W.
(1994). Studies of tropical tuna swimming performance in a large
water tunnel. II. Thermoregulation. J. Exp. Biol.
192, 33-44.
Eckert, S. A. (2002). Swim speed and movement
patterns of gravid leatherback sea turtles (Dermochelys coriacea) at
St Croix, US Virgin Islands. J. Exp. Biol.
205,3689
-3697.
Eckert, S. A., Nellis, D. W., Eckert, K. L. and Kooyman, G. L. (1986). Diving patterns of two leatherback sea turtles (Dermochelys coriacea) during internesting intervals at Sandy Point, St Croix, U.S. Virgin Islands. Herpetologica 42,381 -388.
Eckert, S. A., Eckert, K. L., Ponganis, P. and Kooyman, G. L. (1989). Diving and foraging behavior of leatherback sea turtles (Dermochelys coriacea). Can. J. Zool. 67,2834 -2840.
Eckert, S. A., Liew, H. C., Eckert, K. L. and Chan, E. H. (1996). Shallow water diving by leatherback turtles in the South China Sea. Chel. Cons. Biol. 2, 237-243.
Ferraroli, S., Georges, J. Y., Gaspar, P. and Maho, Y. L. (2004). Where leatherback turtles meet fisheries. Nature 429,521 -522.[CrossRef][Medline]
Frair, W., Ackman, R. G. and Mrosovsky, N. (1972). Body temperature of Dermochelys coriacea: warm turtle from cold water. Science 177,791 -793.
Goff, G. P. and Lien, J. (1988). Atlantic leatherback turtles, Dermochelys coriacea, in cold water off Newfoundland and Labrador. Can. Field Nat. 102, 1-5.
Greer, A. E., Lazell, J. D. and Wright, R. M. (1973). Anatomical evidence for a countercurrent heat exchanger in the leatherback turtle (Dermochelys coriacea). Nature 244,181 .[CrossRef]
Gregory, L. F. and Schmid, J. R. (2001). Stress responses and sexing of wild Kemp's ridley (Lepidochelys kempii) in the northwestern Gulf of Mexico. Gen. Comp. Endocrinol. 124,66 -74.[CrossRef][Medline]
Gunn, J. S. and Block, B. A. (2001). Advances in acoustic, archival, and satellite tagging of tunas. In Tuna: Physiology, Ecology, and Evolution (ed. B. A. Block and E. D. Stevens), pp. 167-224. San Diego, CA: Academic Press.
Hays, G. C., Adams, C. R., Broderick, A. C., Godley, B. J., Lucas, D. J., Metcalfe, J. D. and Prior, A. A. (2000). The diving behaviour of green turtles at Ascension Island. Anim. Behav. 59,577 -586.[CrossRef][Medline]
Hays, G. C., Houghton, J. D. R., Isaacs, C., King, R. S., Lloyd, C. and Lovell, P. (2004a). First oceanic dive profiles for leatherback turtles, Dermochelys coriacea, indicate behavioural plasticity associated with long-distance migration. Anim. Behav. 67,733 -743.[CrossRef]
Hays, G. C., Houghton, J. D. R. and Myers, A. E. (2004b). Pan-Atlantic leatherback turtle movements. Nature 429,522 .[CrossRef][Medline]
Holland, K. N., Brill, R. W., Chang, R. K. C., Sibert, J. R. and Fournier, D. A. (1992). Physiological and behavioural thermoregulation in bigeye tuna (Thunnus obesus). Nature 35,410 -411.
Jackson, D. C. (1985). Respiration and respiratory control in the green turtle, Chelonia mydas.Copeia 1985,664 -671.
Jacobson, E., Bjorndal, K., Bolten, A., Herren, R., Harman, G. and Wood, L. Establishing plasma biochemical and hematocrit reference intervals for sea turtles in Florida. [http://accstr.ufl.edu/blood_chem.htm].
Jones, D. R., Southwood, A. L. and Andrews, R. D. (2004). Energetics of leatherback sea turtles: a step toward conservation. In Experimental Approaches to Conservation Biology (ed. M. S. Gordon and S. M. Bartol), pp.66 -82. Berkeley, CA: University of California Press.
Jones, T. T., Hastings, M., Andrews, R. and Jones, D. R. (in press). Validation of the use of doubly labeled water in the green turtle (Chelonia mydas): measurements of body water, water turnover, and metabolism. Proceedings from the 25th Annual International Symposium on Sea Turtle Conservation and Biology. Savannah, GA, USA.
Kooyman, G. L., Wahrenbrock, E. A., Castellini, M. A., Davis, R. W. and Sinnett, E. E. (1980). Aerobic and anaerobic metabolism during voluntary diving in Weddell seals: evidence of preferred pathways from blood chemistry and behavior. J. Comp. Physiol. B 138,335 -346.
Lifson, N., Gordon, G. B. and McClintock, R.
(1955). Measurement of total carbon dioxide production by means
of D2O18. J. Appl. Physiol.
7, 704-710.
Lutcavage, M. E., Bushnell, P. G. and Jones, D. R. (1990). Oxygen transport in the leatherback sea turtle Dermochelys coriacea. Physiol. Zool. 63,1012 -1024.
Lutcavage, M. E., Bushnell, P. G. and Jones, D. R. (1992). Oxygen stores and aerobic metabolism in the leatherback sea turtle. Can. J. Zool. 70,348 -351.
Miller, J. D. (1997). Reproduction in sea turtles. In The Biology of Sea Turtles (ed. P. L. Lutz and J. A. Musick), pp. 51-82. Boca Raton, FL: CRC Press.
Miton, S. L. and Lutz, P. L. (2003). Physiological and genetic responses to environmental stress. In The Biology of Sea Turtles, Vol. 2 (ed. P. L. Lutz, J. A. Musick and J. Wyneken), pp. 163-197. Boca Raton, FL: CRC Press.
Morreale, S. J. (1999). Oceanic migrations of sea turtles. PhD dissertation, Cornell University, Ithaca, NY, USA.
Morreale, S. J., Standora, E. A., Spotila, J. R. and Paladino, F. V. (1996). Migration corridor for sea turtles. Nature 384,319 -320.[CrossRef]
Ortiz, R. M., Patterson, R. M., Wade, C. E. and Byers, F. M. (2001). Effects of acute fresh water exposure on water flux rates and osmotic responses in Kemp's ridley sea turtles (Lepidochelys kempii). Comp. Biochem. Physiol. 127A,81 -87.
Owens, D. W. (1997). Hormones in the life history of sea turtles. In The Biology of Sea Turtles (ed. P. L. Lutz and J. A. Musick), pp. 315-342. Boca Raton, FL: CRC Press.
Owens, D. W. and Ruiz, G. J. (1980). New methods of obtaining blood and cerebrospinal fluid from marine turtles. Herpetologica 36,17 -20.
Paladino, F. V., O'Connor, M. P. and Spotila, J. R. (1990). Metabolism of leatherback turtles, gigantothermy, and thermoregulation of dinosaurs. Nature 344,858 -860.[CrossRef]
Paladino, F. V., Spotila, J. R., O'Connor, M. P. and Gatten, R. E., Jr (1996). Respiratory physiology of adult leatherback turtles (Dermochelys coriacea) while nesting on land. Chel. Cons. Biol. 2,223 -229.
Penick, D. N. (1996). Thermoregulatory physiology of leatherback (Dermochelys coriacea) green sea turtles (Chelonia mydas). PhD dissertation, Drexel University, Philadelphia, PA, USA.
Plotkin, P. (2003). Adult migrations and habitat use. In The Biology of Sea Turtles, Vol.2 (ed. P. L. Lutz, J. A. Musick and J. Wyneken), pp.225 -242. Boca Raton, FL: CRC Press.
Prange, H. D. and Jackson, D. C. (1976). Ventilation, gas exchange and metabolic scaling of a sea turtle. Resp. Physiol. 27,369 -377.[CrossRef][Medline]
Reina, R. D. (2000). Salt gland blood flow in the hatchling green turtle, Chelonia mydas. J. Comp. Physiol. B 170,573 -580.[Medline]
Reina, R. D., Abernathy, K. J., Marshall, G. J. and Spotila, J. R. (2005). Respiratory frequency, dive behavior and social interactions of leatherback turtles, Dermochelys coriacea during the inter-nesting interval. J. Exp. Marine Biol. Ecol. 316, 1-16.[CrossRef]
Reina, R. D., Jones, T. T. and Spotila, J. R.
(2002a). Salt and water regulation by the leatherback sea turtle
Dermochelys coriacea. J. Exp. Biol.
205,1853
-1860.
Reina, R. D., Mayor, P. A., Spotila, J. R., Piedra, R. and Paladino, F. V. (2002b). Nesting ecology of the leatherback turtle, Dermochelys coriacea, at Parque Nacional Marino Las Baulas, Costa Rica: 1988-1989 to 1999-2000. Copeia 2002,653 -664.
Rostal, D. C., Grumbles, J. S., Palmer, K. S., Lance, V. A., Spotila, J. R. and Paladino, F. V. (2001). Changes in gonadal and adrenal steroid levels in the leatherback sea turtle (Dermochelys coriacea) during the nesting cycle. Gen. Comp. Endocrinol. 122,139 -147.[CrossRef][Medline]
Schmidt-Nielsen, S. (1972). Locomotion: energy cost of swimming, flying, and running. Science 177,222 -227.[Medline]
Southwood, A. L., Andrews, R. D., Lutcavage, M. E., Paladino, F.
V., West, N. H., George, R. H. and Jones, D. R.
(1999). Heart rates and diving behavior of leatherback sea
turtles in the Eastern Pacific Ocean. J. Exp. Biol.
202,1115
-1125.
Southwood, A. L., Andrews, R. D., Paladino, F. V. and Jones, D. R. (2005). Effects of swimming and diving behavior on body temperatures of Pacific leatherbacks in tropical seas. Physiol. Biochem. Zool. 78,285 -297.[CrossRef][Medline]
Speakman, J. R. (1997). Doubly Labelled Water: Theory and Practice. London: Chapman & Hall.
Spotila, J. R., Reina, R. D., Steyermark, A. C., Plotkin, P. T. and Paladino, F. V. (2000). Pacific leatherback turtles face extinction. Nature 405,529 -530.[CrossRef][Medline]
Thompson, D. and Fedak, M. A. (2001). How long should a dive last? A simple model of foraging decisions by breath-hold divers in a patchy environment. Anim. Behav. 61,287 -296.[CrossRef]
Wallace, B. P., Sotherland, P. R., Spotila, J. R., Reina, R. D., Franks, B. R. and Paladino, F. V. (2004). Biotic and abiotic factors affect the nest environment of embryonic leatherback turtles, Dermochelys coriacea. Physiol. Biochem. Zool. 77,423 -432.[CrossRef][Medline]
Withers, P. C. (1992). Comparative Animal Physiology. Orlando, FL: Saunders College Publishing, Harcourt Brace Jovanovich Publishers.
Zug, G. R. and Parham, J. F. (1996). Age and growth in leatherback turtles, Dermochelys coriacea (Testudines: Dermochelyidae): a skeletochronological analysis. Chel. Cons. Biol. 2,244 -249.