Vol.

8: 165–177, 2009 ENDANGERED SPECIES RESEARCH Printed October 2009

doi: 10.3354/esr00202 Endang Species Res Published online July 13, 2009

OPEN
ACCESS
Use of skeletochronological analysis to estimate the
age of leatherback sea turtles Dermochelys coriacea
in the western North Atlantic
Larisa Avens1,*, J. Christopher Taylor2, Lisa R. Goshe1, T. Todd Jones3,
Mervin Hastings3, 4
1
NOAA Fisheries, Southeast Fisheries Science Center, Center for Coastal Fisheries and Habitat Research,
101 Pivers Island Road, Beaufort, North Carolina 28516, USA
2
National Ocean Service, Center for Coastal Fisheries and Habitat Research, 101 Pivers Island Road, Beaufort,
North Carolina 28516, USA
3
University of British Columbia, Department of Zoology, 6270 University Blvd., Vancouver, British Columbia V6T 1Z4,
Canada
4
Conservation and Fisheries Department, Ministry of Natural Resources and Labour, Government of the British Virgin Islands,
Road Town, Tortola, British Virgin Islands

ABSTRACT: Although growth rate and age data are essential for leatherback management, esti-
mates of these demographic parameters remain speculative due to the cryptic life history of this
endangered species. Skeletochronological analysis of scleral ossicles obtained from 8 captive,
known-age and 33 wild leatherbacks originating from the western North Atlantic was conducted to
characterize the ossicles and the growth marks within them. Ages were accurately estimated for the
known-age turtles, and their growth mark attributes were used to calibrate growth mark counts for
the ossicles from wild specimens. Due to growth mark compaction and resorption, the number of
marks visible at ossicle section tips was consistently and significantly greater than the number visible
along the lateral edges, demonstrating that growth mark counts should be performed at the tips so
that age is not underestimated. A correction factor protocol that incorporated the trajectory of early
growth increments was used to estimate the number of missing marks in those ossicles exhibiting
resorption, which was then added to the number of observed marks to obtain an age estimate for each
turtle. A generalized smoothing spline model, von Bertalanffy growth curve, and size-at-age function
were used to obtain estimates of age at maturity for leatherbacks in the western North Atlantic.
Results of these analyses suggest that median age at maturation for leatherbacks in this part of the
world may range from 24.5 to 29 yr. These age estimates are much greater than those proposed in
previous studies and have significant implications for population management and recovery.

KEY WORDS: Sea turtle · Leatherback · Dermochelys coriacea · Skeletochronology · Skeletal growth
mark · Line of arrested growth · LAG
Resale or republication not permitted without written consent of the publisher

INTRODUCTION (Sæther et al. 1996, Chaloupka & Musick 1997, Hep-

pell et al. 2003a). Given the Vulnerable and Endan-
Knowledge of juvenile stage durations, age at matu- gered status of most sea turtle populations worldwide
ration, and reproductive longevity are essential for (IUCN 2008), the need for age data to accurately char-
understanding the life history of any organism (Stearns acterize the status of these species is vital for conser-
1992). Furthermore, the ability to relate age to repro- vation efforts (Heppell et al. 2003a,b).
ductive effort is integral to studies of population Historically, studies of sea turtle age and growth
dynamics, which in turn can inform management have predominantly focused on cheloniid sea turtle
strategies for those organisms considered at risk species such as green turtles Chelonia mydas and log-

*Email: larisa.avens@noaa.gov © Inter-Research 2009 · www.int-res.com

166 Endang Species Res 8: 165–177, 2009

gerheads Caretta caretta. As this field of research has see Fig. 1) yielded an average age at maturation of
developed, our understanding of the time frames over 13 to 14 yr for Pacific leatherbacks (Zug & Parham
which individual marine turtles exist has undergone a 1996). Subsequent analyses have supported the hypo-
significant transformation. Early on, these marine tur- thesis that marks in the scleral ossicles of loggerhead
tles were thought to possibly transition from hatchlings and Kemp’s ridley sea turtles represent annual cycles
to mid-sized juveniles within a single year (Carr 1967). (Avens & Goshe 2007). However, these analyses also
Extrapolation of short-term, rapid growth rates ob- demonstrated that, due to lateral growth mark com-
served for captive juvenile sea turtles (Caldwell 1962, pression and central resorption, growth mark counts
Uchida 1967, Hirth 1971) and wild turtles during the taken at ossicle section tips are far greater than those
summer growing season (Mendonça 1981) suggested obtained laterally, suggesting that leatherback age
ages at maturation ranging from 4 to 15 yr. might previously have been underestimated (Avens &
Subsequent growth rate data obtained from captive Goshe 2007).
marine turtles reared under semi-wild conditions Here, we present a skeletochronological analysis of
(Frazer & Schwartz 1984) and wild mark-recapture scleral ossicles obtained from leatherbacks in the
studies conducted over longer time scales (Limpus western North Atlantic Ocean, to further characterize
1979, Limpus & Walter 1980, Frazer & Ehrhart 1985, these structures and the growth marks within them.
Braun-McNeill et al. 2008) indicated greater time to We analyzed ossicles from captive-reared leather-
maturation than previously thought. Similarly, skeleto- backs of known age to calibrate interpretation of the
chronology (the analysis of skeletal growth marks) has deposition pattern and frequency of growth marks in
been applied to obtain age data (Zug et al. 1986, 1995, the ossicles of wild turtles. We then analyzed ossicles
2002, Klinger & Musick 1995, Parham & Zug 1997, Zug obtained from wild leatherbacks to estimate age at
& Glor 1998, Snover 2002, Snover & Rhodin 2008), often maturation for the species in this region.
resulting in markedly increased estimates of stage du-
rations and age at maturity. For loggerhead and green
turtles, the ‘lost year’ has been revealed to be the ‘lost MATERIALS AND METHODS
years’; estimates of oceanic stage duration range from 8
to 14 yr for loggerhead (Snover 2002, Bjorndal et al. Sample collection. From 2001 to 2008, scleral ossi-
2003) and 3 to 6 yr for green turtles (Zug & Glor 1998). cles were obtained from leatherback sea turtles that
Predictions of age at maturation for these species now stranded dead, were debilitated and later euthanized,
range from 30 to 40 yr (Limpus 1979, NMFS SEFSC or died in the course of permitted research; no turtles
2001, Snover 2002, Zug et al. 2002, Heppell et al. were purposefully sacrificed in the course of the pre-
2003b) and are as high as 40 to 50 yr in the case of sent study. Eight juvenile leatherbacks obtained as
Hawaiian green turtles (Balazs & Chaloupka 2004). hatchlings from the British Virgin Islands (Lambert’s
Despite the advances made with cheloniid marine Bay Beach: 18.4167° N, 64.5833° W) that were part of a
turtles, estimates of the time required for 6 cm captive rearing study (Jones 2009) died in the course of
leatherback sea turtle Dermochelys coriacea hatch- this research between 0.10 and 1.41 yr of age (mean ±
–
lings (van Buskirk & Crowder 1994) to grow into 145 SD, X = 0.79 ± 0.51 yr). These turtles were reared
cm or greater adults (TEWG 2007) range widely. indoors under a combination of ambient and full-spec-
Whereas early analyses extrapolating the rapid growth trum fluorescent lighting, with water temperature
rates observed for captive turtles yielded 2, 3, or 6 yr to maintained at 24 ± 1°C and salinity at 28 to 33 ppt
maturity (Deraniyagala 1952, Birkenmeier 1971, Bels (Jones 2009). One eye was collected from each of the
et al. 1988), more recent captive growth data indicate sea turtles, along with straight line carapace length
that leatherbacks may not mature until 12 to 18 yr of (SCL) as measured in cm from the nuchal notch of the
age (Jones 2009). The presence of vascularized carti- carapace to the tip of the caudal peduncle (9.71 to
–
lage in leatherback limb bones, a characteristic associ- 34.7 cm, X = 28.1 ± 15.6 cm).
ated with rapid growth and more typical of endo- For each wild, stranded sea turtle, participants in the
therms, has suggested the potential for early matu- national Sea Turtle Stranding and Salvage Network
ration, perhaps between 3 and 6 yr of age (Rhodin (STSSN) collected either one or both eyes. Observers
1985, reviewed by Snover & Rhodin 2008). However, typically recorded curved carapace length (CCL) and
genetic analyses describing possible mother–daughter whenever possible, necropsies were conducted to
relationships in a Caribbean nesting population esti- ascertain sex. For analyses necessitating direct com-
mate 12 to 14 yr to maturation (Dutton et al. 2005). parison of carapace length for both captive and wild
Skeletochronological analysis of putative growth leatherbacks, CCL for wild sea turtles was converted
marks observed at the lateral edge of sectioned scleral to SCL using the following formula derived from 17 sea
ossicles (small bones surrounding the pupil of the eye; turtles for which both CCL and SCL were available:
 Avens et al.: Leatherback sea turtle age and growth 167

SCL = 0.9781CCL – 0.7714 (r2 = 0.9982). Samples were Analysis. Hematoxylin-stained ossicle sections were
obtained from a total of 33 wild leatherbacks: 6 hatch- viewed under a trinocular compound microscope
lings, 2 small juveniles (16.6 and 27.3 cm CCL), and 25 (Olympus BX41, OPELCO) at 10× magnification.
large juveniles and adults ranging from 122 to 173 cm Sequential, partial digital images of each ossicle were
–
CCL ( X = 147.5 ± 13.9). Of the larger sea turtles, 10 obtained using a Colorcube-12 Color CCD, 1.4 mega-
were female, 9 male, and 6 were of unknown sex. With pixel digital camera (OPELCO) and then stitched
the exception of 1 leatherback stranded in the Gulf of together in Adobe Photoshop LE (Adobe Systems) to
Mexico, the remainder were distributed along the US form a high-magnification composite image to be used
Atlantic coast as follows: Massachusetts (7), New Jer- for further analysis. Ossicle and growth mark measure-
sey (2), Virginia (2), North Carolina (11), South Car- ments were obtained using Microsuite Basic image
olina (1), and Florida (9, including the 6 hatchlings). analysis software (OPELCO). For comparisons of
Sample processing. Ossicles were dissected from growth mark counts and measurements, the Mann-
surrounding tissue, maintaining position within the Whitney U-test was used when sample sizes differed,
ossicle ring in cases where the orientation of the eye and the Wilcoxon test was applied to pair-wise com-
relative to the head was known. After all ossicles had parisons (Zar 1996). Relationships between ossicle and
been removed from a given eye, they were pho- carapace lengths were compared among wild and cap-
tographed using a digital camera with a macro lens tive turtles, accounting for multiple ossicle measure-
(Canon EOS 10D digital camera with Canon Telephoto ments within individuals by using unbalanced
EF 100 mm f/2.8 USM Macro Autofocus lens) before repeated measures.
further processing, to document the characteristics of Counts of lines of arrested growth (LAGs), which
individual ossicles and the entire ring (Fig. 1). Ossicles delimit the outer boundaries of skeletal growth marks
were then immersed alternately in tap water and a 1:1 (Castanet et al. 1993), were conducted by a single
bleach:water solution and gently scraped with a metal observer (L. Avens). Initial examination of the wide
probe to remove any remaining tissue. tips of ossicles obtained from wild, stranded leather-
Ossicles were fixed in 10% neutral buffered formalin backs revealed a large number of marks whose depo-
(Fisher Scientific), rinsed in tap water, decalcified by sition appeared to follow a distinct pattern: one or
immersion in RDO (Apex Engineering Corporation), more lighter, diffuse marks followed by a darker, dis-
and then allowed to soak in water overnight to remove tinct mark (Fig. 2). It seemed unlikely that each of
any decalcifier remaining in the tissue. A freezing these marks represented an annual cycle, as this would
stage microtome (Leica Microsystems) was used to have resulted in unexpectedly high age estimates (e.g.
obtain 25 µm thick sections (plane of sectioning shown 63 marks observed for a 156 cm CCL female, just
in Fig. 1), which were stained using modified Mayer’s above the mean size for nesting females).
hematoxylin (Myrick et al. 1983). Stained sections
were mounted in 100% glycerin on microscope slides
under glass coverslips sealed with Cytoseal 280
(Thermo Fisher Scientific).

Fig. 2. Dermochelys coriacea. Partial, high-magnification

(10×) image of wide ossicle tip obtained from a leatherback
Fig. 1. Dermochelys coriacea. Leatherback skull, showing 156 cm in curved carapace length, showing alternating dif-
location of ossicle ring. Dashed line through ossicle denotes fuse light (white bars) and well-defined dark (black bars)
plane of sectioning lines of arrested growth
168 Endang Species Res 8: 165–177, 2009

Although the small size of the ossicles sometimes 2002, Cailliet et al. 2006). Based on these findings, each
made it difficult to resolve the fine-scale pattern of LAG LAG group was conservatively counted as 1 annual
deposition, concurrent skeletochronological analysis of mark, delimited by the dark, distinct LAG, and these
larger leatherback phalanges (finger bones) processed counts were used to obtain our age estimates. Indepen-
using the same methods as for sea turtle humeri (Avens dent counts were done both laterally and at the wide tips
& Goshe 2007) revealed remarkable spatial consistency of ossicle sections (Fig. 4) at 5 d intervals or longer, until
for the LAG groupings (Fig. 3). Such a regular pattern a consensus count was obtained (within 3 or 4 counts).
would not be expected if the marks were deposited as a Average percent error was calculated for these counts as
result of sporadic events such as prey scarcity or harsh described by Beamish & Fournier (1981).
environmental conditions. Therefore, for the purpose of Ossicles from the 8 captive leatherbacks were ana-
these analyses, we instead hypothesize that the LAG lyzed without prior knowledge of age. Ages assigned
groupings result from the repeated, multiple migrations through skeletochronology were then compared with
undertaken by North Atlantic leatherbacks each year actual ages, and the appearance of the annual marks in
among breeding/nesting areas and various foraging ar- the ossicles of the known-age leatherbacks were then
eas around the ocean basin (e.g. Hays et al. 2004, Eckert used to characterize early marks deposited in the ossi-
2006). Growth mark deposition corresponding with mi- cles of the wild turtles.
grations has been found in North Atlantic tuna species Although some wild leatherback ossicles exhibited no
(Compeán-Jimenez & Bard 1983). Also, annual cycles resorption, and age for these turtles could be calculated
are reflected as multiple marks in the hard structures of directly from LAG counts, in many ossicles resorption
many vertebrates (Casselman 1983, Klevezal 1996, Hohn had destroyed early LAGs. The correction factor protocol
described by Zug & Parham (1996) was used
to calculate the number of lost marks. This in-
volved measuring LAGs throughout those
wild ossicles in our sample exhibiting little to
no resorption, in order to characterize early
LAG growth patterns. Total LAG lengths
could not be measured because lateral LAG
compression made it impossible to follow
marks around their entire circumference;
therefore, LAG radii were measured instead
(Fig. 4). The relationship between LAG num-
ber and LAG radius was then modeled to pre-
dict the number of missing LAGs in each
resorption core, which was added to the ob-
served number of LAGs to yield an age esti-
mate for each turtle.
Median ages at maturation were estimated
assuming 3 carapace lengths reported for
Fig. 3. Dermochelys coriacea. (a) Phalanges from right, front flipper of a nesting female leatherbacks in the western
leatherback 144.5 cm in curved carapace length. Roman numerals signify North Atlantic (Stewart et al. 2007, TEWG
phalange number; phalanges in ‘I’ constitute the group of fingerbones po- 2007): (1) 125 cm as the minimum size; (2)
sitioned closest to the flipper’s anterior edge. Dashed line in ‘II’ denotes 145 cm as the average size at first nesting;
plane of sectioning. (b) Partial image of phalange section (4×) demonstrat-
ing spatial regularity of line of arrested growth groupings. Black lines and
and (3) 155 cm as the average size of nesting
corresponding numbers denote the location and number of marks within females. Sex-specific analyses were not con-
growth mark groups ducted due to the large number of unknown-

Fig. 4. Dermochelys coriacea. Entire ossicle section showing lateral edges, and narrow and wide tips. Growth mark and/or line of
arrested growth radius measurements were taken starting from the location of the dotted line, which represents the average
location of the core mark center relative to the wide tip (proportionally 0.56 total ossicle length)
 Avens et al.: Leatherback sea turtle age and growth 169

sex turtles in the sample. Two methods were used to central 95% of the predictions of size at estimated age.
model the growth of leatherbacks. First, size at esti- For both the smoothing spline and von Bertalanffy
mated age was fit using a non-parametric smoothing models, predictions were generated and estimated
spline model and a von Bertalanffy growth curve. ages were determined that included the assumed size
Smoothing splines were fit using the generalized cross- at maturation (i.e. 125, 145, and 155 cm CCL) within
validation procedure to optimize the fit, while minimiz- the 95% confidence regions.
ing the chance of oversmoothing (Wood 2001), and Finally, an age-maturation function was estimated
confidence regions were generated using Bayesian using a generalized smoothing spline logistic model
posterior probabilities. Second, a parametric model was incorporating estimated ages and assumed sizes of
fit to the data adopting the following form of the von mature nesting females (where individuals greater
Bertalanffy growth model: than assumed size are considered mature). The gener-
alized smoothing spline was fit and confidence bounds
CCL = L∞{1 – e [–k(Age – t0)]}
estimated using Bayesian posterior probabilities
where CCL is the curved carapace length, L∞ is the (Bishop et al. 2006, Zug et al. 2006).
maximum length, k is the intrinsic growth rate, and t0
is the intercept parameter (von Bertalanffy 1938). The
model was fit using non-linear least squares; confi- RESULTS
dence regions were constructed using a delta method
for estimating uncertainty using the means and vari- Ossicle rings from leatherbacks for which we
ance–covariance matrix of parameter estimates. As an received entire eyes contained between 10 and 13
–
alternative method to characterize uncertainty, we ossicles (X = 12.1 ± 1.1, n = 29). The relationship be-
estimated model parameters and model predictions by tween SCL and ossicle length (OL) was linear and
randomly resampling from the data with replacement there was no significant difference between the slopes
(bootstrap), and refitting the von Bertalanffy model to for wild and captive leatherbacks (p > 0.70). The equa-
the sample data 10 000 times. To maintain general con- tion describing the grouped data was OL = 0.0551 SCL
sistency in the shape of the fitted model, we assumed + 1.472 (r2 = 0.9216).
that each resampling would contain a hatchling (age = Preliminary observations using stained sections from
0, carapace length = 6 cm; van Buskirk & Crowder all ossicles within individual eyes and/or rings revealed
1994). Confidence regions were calculated using the a great deal of variation in the amount of resorption;

Fig. 5. Dermochelys coriacea. Sections of all ossicles from a single eye, displaying resorption levels ranging from minimal (e.g.
ossicle 1) to extensive (ossicle 5)
170 Endang Species Res 8: 165–177, 2009

whereas some ossicles exhibited little to no growth mark tion, a greater number of marks was visible at the wide
resorption, others were almost entirely remodeled, with tip and therefore all counts used for age analyses were
few LAGs remaining (Fig. 5). For those ossicle rings obtained from this region.
where orientation relative to the head was known (n = Age was accurately predicted for the 8 known-age,
13), no significant relationship was found between ossi- captive-reared leatherbacks and this allowed charac-
cle position and the number of retained LAGs (r2 = 0.004, terization of the first annual LAG (LAG 1), which was
p > 0.20, n = 159 ossicles). This lack of predictive power the first faint, but complete, mark that could be fol-
made it necessary to process every ossicle from each sea lowed continuously starting at the lateral edges down
turtle to ensure that the best ossicle (i.e. that with the through the wide tip (Fig. 7a). Similar marks outside
least resorption) was found and analyzed. the core marks were observed in those wild
The ossicles with little to no resorption at the center leatherback ossicles that exhibited little resorption
contained a distinct mark (Fig. 6) similar to the core (Fig. 7b,c). LAG 1 radius measurements for captive and
mark described for Kemp’s ridley and loggerhead sea wild sea turtles were not significantly different (Mann-
turtles (Avens & Goshe 2007) and which appears to be Whitney U-test, 0.10 > p > 0.05, n = 3 known-age, n =
deposited at hatching for these species. Comparison of 11 wild). However, captive LAG 1 radius measure-
leatherback core mark and leatherback hatchling ossi- ments occurred at the larger end of the size distribu-
cle lengths revealed no significant difference (Mann- tion, perhaps reflecting the captive sea turtles’ proba-
Whitney U-test, p > 0.20, n = 12 hatchling ossicles, n = ble larger size relative to wild juveniles of the same
11 core marks), indicating that the leatherback core age. Early LAGs following LAG 1 in the wild ossicles
mark is also a hatch mark and should be used as the
starting point for estimating age, representing age 0.
Average percent error for grouped growth mark
counts was 4%. Comparison of LAG counts made lat-
erally with those from the wide tips of ossicle sections
revealed a highly significant difference (Wilcoxon
paired sample test, p < 0.0005, n = 18). Without excep-

Fig. 7. Dermochelys coriacea. Wide

ossicle tips for (a) a captive-reared
leatherback, 24.9 cm straight cara-
pace length (SCL), and 1.28 yr old,
(b) a wild leatherback, 27.3 cm
curved carapace length (CCL),
stranded 28 Feb 2006, estimated age
1+ yr, and (c) a wild leatherback,
133.4 cm CCL, estimated age 24 yr.
Dark lines denote location of Year 1
Fig. 6. Dermochelys coriacea. (a) Core mark (dotted line) growth mark in (a–c) and dashed
observed at the center of those ossicles exhibiting little to no lines in (c) indicate 3 subsequent
resorption. (b) Hatchling ossicle section marks interpreted as annual
 Avens et al.: Leatherback sea turtle age and growth 171

The general shapes of the smoothing

spline and von Bertalanffy growth func-
tions were nearly identical (Fig. 9).
Parameter estimates for the von Berta-
lanffy growth models were similar be-
tween the delta method and bootstrap
uncertainty analysis (estimate 95% CI):
L∞ = 169.2 (158.65 to 185.6), k = 0.07
(0.05 to 0.09), t0 = –0.46 (–0.70 to
–0.30). Although it is not common, fe-
males as small as 125 cm CCL are occa-
sionally observed on nesting beaches.
The 95% confidence regions for the
smoothing spline model predicted that
turtles of this size are 18 to 22 yr of age
(Fig. 9a), while the von Bertalanffy
Fig. 8. Dermochelys coriacea. Plot of line of arrested growth (LAG) number curve estimates ranged from 16 to 20.5
versus LAG radius (n = 202) for 11 leatherbacks whose ossicles exhibited little
yr (Fig. 9b). Age estimates for sea tur-
to no resorption and in which the earliest growth marks (beginning with
LAG 1) were visible. Different symbols represent individual ossicle growth tles 145 cm in CCL, a more typical size
trajectories for different individuals. The relationship between LAG number for first-time nesters, ranged from 24.5
and LAG radius for the grouped data was best described by the logarithmic to 29 yr of age for both models (Fig.
equation y = 1.028ln(x) + 1.5167 (R2 = 0.862) 9a,b). Finally, the smoothing spline and
von Bertalanffy curve predicted that
were similar in appearance, lending confidence to average-sized nesting sea turtles 155 cm in CCL may
their interpretation as annual marks (Fig. 7c). be > 29 or 31 to 43 yr old, respectively (Fig. 9a,b).
The relationship between LAG number and LAG The age-specific maturation function performed
radius within wild leatherback ossicles was described poorly for 125 and 155 cm CCL where sample sizes
by a logarithmic curve (Fig. 8). Resorption core radius were low. For 145 cm CCL, the model predicted that
was substituted for LAG radius within the equation to median age at maturation would be 27 yr (95% CI =
yield an estimate of the number of resorbed LAGs, 20 to 30 yr; Fig. 10), which was within the range of
which was then added to the observed number of estimates predicted by the smoothing spline model
LAGs to yield an age estimate for each sea turtle. and the von Bertalanffy curve.

Fig. 9. Dermochelys coriacea. (a) Smoothing spline and (b) von Bertalanffy growth curve fit to age estimate and curved carapace
length (CCL) data. Dashed lines following the curves denote 95% credible intervals. Horizontal dashed lines correspond to 125,
145, and 155 cm CCL, respectively. Size at estimated age data are shown as open circles. Gray shading in (b) shows results from
10 000 bootstrap permutations of the size at estimated age data
172 Endang Species Res 8: 165–177, 2009

as errors in interpretation can confound age estimates

and resulting interpretation of individual and popula-
tion vital rates (Ardizzone et al. 2006).
Prior to conducting age analyses using hard struc-
tures, it is necessary to determine the most appropriate
axis along which to conduct growth-mark counts
(Lagardère et al. 1995). Zug & Parham (1996) de-
scribed and analyzed marks visible at the lateral edges
of leatherback ossicle sections. However, as predicted
from a recent analysis of cheloniid turtle ossicles
(Avens & Goshe 2007), mark clarity and spacing was
better at the wide tips of leatherback ossicle sections
due to lateral mark compression and relatively greater
resorption at ossicle centers (Fig. 2). As a result, this
was the axis along which we obtained our LAG counts
and we recommend that future analyses also focus on
this region.
Despite the confidence in the location of the growth
Fig. 10. Dermochelys coriacea. Plot of size-at-age function fit-
ted assuming size at first nesting of 145 cm. The model was fit mark counts, some uncertainty regarding the fre-
to the data using a generalized smoothing spline (solid line). quency of mark deposition in the ossicles remains.
Size at estimated age data are shown as open circles. Dashed Growth-mark deposition has been most strongly
lines following the curve denote 95% credible intervals. Hori- linked to variations in ectotherm growth rates that are
zontal dashed line corresponds to 0.50 proportion mature
caused by seasonal temperature fluctuations (e.g. Hut-
ton 1986). However, leatherbacks are atypical for rep-
tiles in that they are able to maintain their body tem-
DISCUSSION perature well above ambient (James et al. 2006). In
theory, the elevated body temperature and high vascu-
The analyses presented here indicate that median larization of leatherback skeletal elements might allow
age at maturation for leatherbacks in the western more or less continuous growth, as is the case for most
North Atlantic Ocean ranges from 24.5 to 29 yr (Figs. 9 birds (Turvey et al. 2005), with mark deposition result-
& 10). These ages are far greater than the early esti- ing from other factors influencing growth rates. How-
mates of 2 to 6 yr (Deraniyagala 1952, Birkenmeier ever, hard structures in mammals (reviewed by
1971, Rhodin 1985, Bels et al. 1988). However, the Klevezal 1996) and tropical reptiles and amphibians
lower end of our predicted 16 to 22 yr age range for (Zug & Rand 1987, Chinsamy et al. 1995, Kusrini &
125 cm CCL sea turtles does approach the span of 12 to Alford 2006) experiencing less annual thermal vari-
18 yr that encompasses more recent results from skele- ability than the leatherback have been found to con-
tochronology, genetic analyses, and captive rearing tain annual growth marks. Furthermore, controlled
(Zug & Parham 1996, Dutton et al. 2005, Jones 2009). laboratory experiments have not revealed a positive
Sex-specific differences in growth and maturation relationship between degree of vascularization and
have been demonstrated for other marine turtle spe- growth rates in bird bones (Starck & Chinsamy 2002).
cies, with males tending toward faster growth rates Growth mark deposition appears to be predominantly
and earlier maturation (Chaloupka & Limpus 1997, driven by endogenous cycles that function even in the
Limpus & Chaloupka 1997, Snover 2002). Given that absence of environmental influence (Schauble 1972,
our sample of large juveniles and adults included both Simmons 1992). As a result, it would be expected that
males and females, if a similar dichotomy in growth the hard structures of leatherbacks, like most other
patterns exists for leatherbacks, this would negatively non-avian vertebrates studied to date (Castanet et al.
bias our age estimates for nesting females. 1993, Secor et al. 1995, Klevezal 1996), would also
exhibit annual cycles of deposition. This supposition is
supported by the observation that annual growth
Growth mark interpretation marks were observed in the captive leatherbacks >1 yr
old, although they had been reared under fairly con-
As with all skeletochronology studies, the estimates stant environmental conditions (Jones 2009).
of age at maturation presented herein are dependent Another issue is the interpretation of the light and
upon interpretation of the growth marks within the dark marks within the ossicles. Aside from the influ-
scleral ossicles. Accurate reads are of course essential, ence of endogenous factors on growth mark deposi-
 Avens et al.: Leatherback sea turtle age and growth 173

tion, this process can also be affected by physiological for the larger, cheloniid sea turtle species (Limpus
and environmental stressors; aestivation, disease, food 1979, NMFS SEFSC 2001, Snover 2002, Zug et al.
shortage, and adverse climatic conditions may all alter 2002, Heppell et al. 2003b, Balazs & Chaloupka 2004).
somatic growth and yield mark formation (Klevezal It may seem difficult at first to draw direct parallels
1996, Sinsch et al. 2007). Furthermore, long and ener- between leatherback life history and that of cheloniid
getically expensive migrations, such as those exhibited sea turtles because the lineages diverged at least 100
by Atlantic tuna species, have been linked to mark million years ago (Bowen & Karl 2007). Furthermore,
deposition (Compeán-Jimenez & Bard 1983). In many leatherbacks display some unusual characteristics,
other cases, although the factors underlying deposition such as their enormous size as adults, and their lack of
are not necessarily well understood, annual cycles are a true carapace (Eckert & Luginbuhl 1988, Stewart et
also represented by more than one mark (e.g. salaman- al. 2007). Also unlike cheloniid sea turtles, leather-
ders, Castanet et al. 1993; cetaceans [growth layer backs are able to maintain their body temperatures
groups], reviewed by Hohn 2002; terrestrial mammals, well above that of their surroundings, allowing them to
Klevezal 1996; chondrichthyans [band pairs], Cailliet forage at high latitudes (Spotila et al. 1997, James et al.
et al. 2006; fish otoliths, Casselman 1983). 2006). In the course of their movements between these
In the North Atlantic, leatherbacks undertake sea- feeding areas and tropical breeding sites, leatherbacks
sonal migrations that span the ocean basin (Hays et al. transit over exceptionally long distances (Eckert 2006,
2004, Eckert 2006) and their behavior suggests that Hays et al. 2006). Finally, for all their large size and
foraging may occur to some extent during these move- presumed metabolic requirements, leatherbacks sub-
ments (Hays et al. 2006). However, if the energetic sist almost solely on an ‘energetically improbable’ diet
requirements of continuous, high-speed swimming of gelatinous prey (Houghton et al. 2006).
and diving exceed the level of prey intake during Despite these singular qualities, many fundamental
travel, this could result in cessation of somatic growth similarities exist between leatherbacks and their clos-
and mark deposition within the bones during migra- est extant relatives. Resting metabolic rates of leather-
tion. The leatherback’s spring/early summer migration backs do not differ from those of green sea turtles (or
to northern foraging areas (periodically after directing other reptiles); their elevated body temperature results
considerable resources toward reproduction) might instead from anatomical adaptations that very effec-
correspond with deposition of the annual, dark LAG, tively retain behaviorally generated heat (Wallace &
while the lighter marks within the groups could relate Jones 2008). In addition, leatherbacks display an itero-
to additional migrations undertaken by these sea tur- parous reproductive strategy similar to that of che-
tles each year. In light of these precedents, we counted loniid sea turtles, in which females lay 2 to 10 nests
each group of LAGs in leatherback scleral ossicles as a each reproductively active year at intervals of 2 to 5 yr
single, annual growth mark, presuming that the (van Buskirk & Crowder 1994). Nesting occurs on
darker, more distinct mark demarcated the annual oceanic beaches and, as for all other marine turtle spe-
cycle and was deposited in winter/spring (Klevezal cies, stochastic environmental conditions combined
1996), as found for cheloniid sea turtles (Snover & with predation can yield low nest and/or hatchling
Hohn 2004). survival (Frazer 1987, Leslie et al. 1996). Once in the
Recent isotopic analyses have begun to investigate water, hatchling leatherback and cheloniid turtles
potential differences in the microchemistry of the light alike are vulnerable to predators, and survival rates
and dark LAGs, which could provide information can be low (Gyuris 1994, Spotila et al. 1996, TEWG
about the timing of mark deposition (R. Day unpubl. 2007, but see Stewart & Wyneken 2004). By contrast,
data). However, additional work is needed to address large juvenile and adult survival probabilities are esti-
the frequency of deposition, possibly through bone- mated to be relatively high (Frazer 1986, 1987, Troëng
marking studies (reviews in Frazier 1985, Klevezal et al. 2007, TEWG 2007).
1996) or bomb radiocarbon analysis (e.g. Campana Given this extensive concurrence, it is possible that
1997, Ardizzone et al. 2006). the selective pressures leading to the life-history char-
acteristics described above, including delayed matura-
tion, may have acted similarly for all marine turtle spe-
Delayed maturation and life-history considerations cies. Growing to and maintaining a large size is
energetically expensive and only worthwhile if this
Although our proposed age at maturation estimate of increased size also yields a corresponding increase in
24.5 to 29 yr for leatherbacks contrasts sharply with reproductive success (Gadgil & Bossert 1970, Stearns
earlier estimates of 2 to 6 yr (Deraniyagala 1952, 1992, Charnov et al. 2001). Total egg output does
Birkenmeier 1971, Rhodin 1985, Bels et al. 1988), our increase with body size for green (Broderick et al.
results do approach the 30 to 40 yr range established 2003) and leatherback (Price et al. 2006) sea turtles,
174 Endang Species Res 8: 165–177, 2009

indicating that such a benefit may exist. Large adult earlier published values (Deraniyagala 1952, Birken-
size can confer a size refuge from predation (Takada & meier 1971, Rhodin 1985, Bels et al. 1988, Zug &
Caswell 1997), yielding increased adult survival rates, Parham 1996, Dutton et al. 2005). However, the ten-
which in turn have been found to correlate positively dency toward increasing estimates of age at matura-
with age at maturation (e.g. for squamate reptiles, tion as the techniques used to study age and growth
Shine & Charnov 1992). Low juvenile survival can are refined over time is consistent with the pattern
result in selection against reproductive effort at seen for hard-shelled marine turtle age estimates over
smaller sizes and/or younger ages (Law 1979, Michod the past several decades (Caldwell 1962, Uchida 1967,
1979, Reznick et al. 2002) so that all available energy is Hirth 1971, Limpus 1979, Mendonça 1981, NMFS
devoted to growth during this time, to move beyond SEFSC 2001, Snover 2002, Zug et al. 2002, Heppell et
the vulnerable stage(s) (Takada & Caswell 1997). The al. 2003b, Balazs & Chaloupka 2004). Discrepancies
effects of stochastic environmental conditions on re- among results from the various leatherback age stud-
productive success are thought to select for bet-hedg- ies are likely due to a number of factors. Early studies
ing, where organisms are long-lived to distribute of captive leatherback hatchlings reared in constant
reproductive effort over space and time, maximizing conditions and fed unusual diets yielded rapid growth
the probability of offspring survival over the course of rates not necessarily representative of wild individuals,
the reproducer’s life span (Stearns 1992, Sæther et al. and analyses of these data did not always take into
1996). Finally, the trait of delayed age to maturity in account growth rate decay through ontogenetic stages
sea turtles might simply be phylogenetically con- (Deraniyagala 1952, Birkenmeier 1971, Bels et al.
strained (Stearns 1984, 1992, Dunham & Miles 1985), 1988). The results of our skeletochronological analysis
as is thought to be the case for their metabolic rates of leatherback ossicles indicate that growth mark com-
(Wallace & Jones 2008). paction and resorption may have resulted in a lower
It should be noted, however, that despite the conver- estimate of age at maturation for an earlier Pacific
gence of delayed age at maturation estimates among leatherback skeletochronology study (Zug & Parham
the larger sea turtle species, the growth rates of 1996), although population-specific differences in age
leatherbacks remain accelerated relative to those of and growth are possible. Finally, although DNA fin-
cheloniid turtles (Snover & Rhodin 2008). Although gerprinting data for a Caribbean nesting population
Atlantic leatherback hatchlings are only slightly larger provide compelling evidence for a minimum reproduc-
than those of loggerhead or green sea turtles, the tive age of 12 to 14 yr, the mixture of possible mother–
mean carapace length of nesting female leatherbacks daughter and sister–sister relationships can confound
exceeds that of the other 2 species by approximately interpretation of lineages (Dutton et al. 2005).
50% (Buskirk & Crowder 1994, Stewart et al. 2007). As Leatherbacks are listed as Critically Endangered
a result, it appears that leatherbacks are still conferred worldwide (IUCN 2006), with nesting populations in
some advantage by reaching large size more quickly, the Pacific having undergone catastrophic collapse in
perhaps related to the thermoregulatory capacity that the past few decades (Chan & Liew 1996, Spotila et al.
allows them to exploit a foraging niche not available to 1996, 2000, Hitipeuw et al. 2007, Sarti Martínez et al.
other sea turtle species. 2007). By contrast, some western North Atlantic nest-
ing populations are increasing dramatically, while oth-
ers remain stable (TEWG 2007), or are perhaps even
Implications for conservation decreasing (Troëng et al. 2007). The increasing trends
are encouraging and in some cases have been attrib-
Accurate information relating age to reproductive uted to recently implemented protective measures tak-
effort is essential to understanding population dynam- ing effect over the presumed short generation time of
ics and assessing the effectiveness of potential man- the leatherback (Dutton et al. 2005). However, some
agement strategies (Sæther et al. 1996, Chaloupka & conservation efforts that have been in place for 15 to
Musick 1997, Heppell et al. 2003a). When age at matu- 20 yr in the Pacific have yet to yield an increase in
ration is underestimated, as has occurred on a number nesting populations (Huppert & Mittleman 1993,
of occasions for various fish species, this can intro- Hitipeuw et al. 2007, Sarti Martínez et al. 2007).
duce inaccurate assumptions regarding population re- Although this lack of recovery might be due to contin-
silience to negative impacts, which in turn can have ued low survival rates, it is also possible that sufficient
disastrous management implications (see Summerfelt time has not passed for the hatchlings and juveniles
& Hall 1987, Secor et al. 1995, Cailliet et al. 2006 for impacted by these recovery efforts to have matured
reviews). and returned to nest.
The age at maturation estimates presented here for Despite some uncertainty associated with the esti-
leatherbacks may seem unexpectedly high relative to mates of age at maturation proposed here, they might
 Avens et al.: Leatherback sea turtle age and growth 175

serve as a caution for researchers and managers, as ➤ Bishop SDH, Francis MP, Duffy C, Montgomery JC (2006)
they carry with them potentially significant implica- Age, growth, maturity, longevity, and natural mortality of
the shortfin mako shark (Isurus oxyrinchus) in New
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Editorial responsibility: Matthew Godfrey, Submitted: November 28, 2008; Accepted: April 2, 2009
Beaufort, North Carolina, USA Proofs received from author(s): May 26, 2009