Fisheries Research 99 (2009) 203–209

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Fisheries Research
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Difficulties associated with modeling growth in the Atlantic angel shark

(Squatina dumeril)
Ivy Elizabeth Baremore ∗ , Kate Irene Andrews, Loraine Frances Hale
National Marine Fisheries Service, Southeast Fisheries Science Center, 3500 Delwood Beach Road, Panama City, FL 32408 USA

a r t i c l e i n f o a b s t r a c t

Article history: Several methods were used in an attempt to develop an age and growth model for the Atlantic angel
Received 23 March 2009 shark (Squatina dumeril). Band counts from vertebral sections, which were fit to the traditional von Berta-
Received in revised form 5 June 2009 lanffy growth equation, the Gompertz growth equation, and the two-parameter von Bertalanffy growth
Accepted 9 June 2009
equation, did not produce realistic parameter estimates. Additionally, a length-based Bayesian model was
applied to fishery-independent length–frequency data, and a full Bayesian model was fitted to length-
Keywords:
at-age data to estimate parameters for von Bertalanffy growth equation. Both the length-based and full
Age
Bayesian models failed to converge; the length–frequency data showed high bimodality unrelated to sea-
Growth
Squatina dumeril
son, year, or other factors, and band counts were not predictable by length. Vertebral band counts were
Bayesian not valid for ageing Atlantic angel sharks, and length-based methods, which require normally distributed
Length-based von Bertalanffy length–frequencies, were not appropriate for this data set. This study represents the first attempt at
modeling age and growth for this species and provides research guidelines for future research initiatives.

© 2009 Elsevier B.V. All rights reserved.

1. Introduction extensively used in modern marine fisheries research, where age-

Age and growth information for fishes is necessary for age-
structured stock assessment models (Siegfried and Sansó, 2006),
and is used to estimate a host of parameters that are vital to fish-
eries management, including longevity and vulnerability to fishing
mortality (Jennings et al., 2001). Unfortunately, individual ages for
many species of fishes, especially elasmobranchs, can be difficult to
obtain. Deep water, tropical, and Arctic fishes are the most challeng-
ing to age, mostly due to lack of calcification of hard parts and/or
temporally unpredictable banding patterns (Cailliet and Goldman,
2004; Treble et al., 2008).
Sharks and other elasmobranchs are generally aged using band
counts of vertebral centra, spines, or other calcified structures
(Cailliet and Goldman, 2004). This method has been validated for
several species of sharks (Carcharhinus obscurus (Simpfendorfer
et al., 2002), Lamna nasus, Campana et al., 2002), Prionace glauca
(Skomal and Natanson, 2003), and C. acronotus (Driggers et al.,
2004)), skates (Amblyraja radiata (Sulikowski et al., 2005)), and rays
(Urobatis halleri (Hale and Lowe, 2008)), but some elasmobranchs
have proven more problematic (Squatina californica (Natanson and
Cailliet, 1990). Despite a call from Pauly (1987) to develop and
implement more length-based growth models, they have not been
∗ Corresponding author. Tel.: +1 850 234 6541; fax: +1 850 235 3559.
E-mail address: Ivy.Baremore@noaa.gov (I.E. Baremore).
based methods dominate. However, the inability to obtain ages
from many fishes lends to the necessity of using length data for
growth estimates. Siegfried and Sansó (2006) developed a length-
based Bayesian model that provided a statistically sound estimate
of the asymptotic size parameter (L∞ ) from the von Bertalanffy
growth equation (VBGE). This method is most useful when age
data are not available but growth estimates are required for assess-
ment.
Angel sharks (Squatinidae) are benthic elasmobranchs that
occur circumglobally in tropical and temperate waters and have
been found at depths ranging from near shore to as deep as 3400 m
(FAO, 2002). While little species-specific information is available,
angel sharks are known to be aplacentally viviparous (Compagno,
1984), with up to a three-year reproductive cycle (Colonello et
al., 2006). The Pacific angel shark (S. californica) has a maximum
age of 35 years (Cailliet et al., 1992), and a maximum size of
1500 mm total length (TL). The only published study examining age
structures of angel sharks found that S. californica “do not deposit
vertebral bands annually or in a temporally predictable manner”
(Natanson and Cailliet, 1986). Von Bertalanffy parameters were
estimated for S. californica through tag returns and captive-held
animals (L∞ = 1270 mm TL, k = 0.15, sexes combined) (Cailliet et al.,
1992). The Atlantic angel shark (Squatina dumeril) occurs through-
out the Gulf of Mexico and in the U.S. Atlantic Ocean. Males and
females mature at around 850 mm TL (Baremore, in review), but
their reproductive cycle has yet to be determined. The only pub-

0165-7836/$ – see front matter © 2009 Elsevier B.V. All rights reserved.
doi:10.1016/j.fishres.2009.06.006
204 I.E. Baremore et al. / Fisheries Research 99 (2009) 203–209
lished information for this species is on feeding habits (Baremore
et al., 2008).
The objectives of this study were to (1) determine if vertebrae
are valid ageing structures for Atlantic angel sharks and (2) explore
non-traditional age and growth methods for a species belonging to
a genus that is notoriously difficult to age.
2. Materials and methods
2.1. Sampling and vertebrae preparation
Atlantic angel sharks were collected from a butterfish trawl
fishery in the northeastern Gulf of Mexico from November 2003
through November 2005. Sharks were placed on ice and trans-
ported to the NOAA Fisheries Service Panama City Laboratory for
dissection. At the laboratory, the sharks were assigned a refer-
ence number, sexed, weighed (±0.02 kg), measured for precaudal
(PCL), fork (FL), and total (TL) lengths (mm), and their maturity was
assessed by internal examination. All lengths taken were straight-
line measurements starting from the tip of the snout. Portions of the
middle of the vertebral column (∼10–15 vertebrae) were removed
and frozen until they could be processed. Upon thawing, vertebral
centra were separated, cleaned of excess tissue with a scalpel and
placed in a 3% solution of sodium hypochlorite for 30–45 min, or
until all muscle and viscera had disintegrated. Once clean, vertebrae
were rinsed in fresh water and placed in 70% ethanol for storage.
To determine the best method for reading band counts, ten indi-
viduals were selected at random, and five vertebral centra from
each individual were used for comparison. Vertebral centra were
mounted to slides using melted resin and sectioned sagittally in
five ways: (1) cut in half, (2) sectioned at 0.9 mm, (3) sectioned at
0.6 mm, (4) sectioned at 0.3 mm, and (5) sectioned at 0.6 mm sagit-
tally, but not between the neural arches. All sections were made
with a Bueller isomet saw fitted with two Norton® Diamond Wheel
blades with spacers in between the blades. Sections were mounted
to microscope slides using Cytoseal® mounting medium, and band
counts were made with transmitted light using a Meiji® Techno
dissecting microscope at ×25 magnification. Vertebral centra that
were cut in half were mounted cut-side-up and band counts were
read using reflected light. Band counts were made for the sections
and halved vertebrae for each individual and compared. Digital
images were also taken for reference.
Because bands on the edge of the centra were obscured for
many of the halved centra (Fig. 1A) and therefore caused under-
estimation of band count, this method was rejected for band count
analysis. Additionally, the bands in the centra for 0.9 mm sections
were difficult to read and in many cases appeared blurry (Fig. 1B),
and the 0.3 mm sections were very fragile and often split or fell
apart (Fig. 1C). Overall the sections made between the neural arches
at 0.6 mm provided the clearest bands with the most consistently
robust samples (Fig. 1D). No change in angle was detected in any
sections, so no birthmark could be identified. Therefore, sections
were read starting at the foci with the first detectable band and
moving outward to the edge of the centra.
2.2. Band count analysis
A subsample of 150 individuals was chosen at random for band
count analysis from a pool of approximately 700 samples. An addi-
tional 50 vertebrae were then selected according to the size of the
shark to fill in size classes that were missing or inadequately rep-
resented. Band counts were made by two readers independently
and without knowledge of the size or sex of the individual animal.
If band counts differed between readers, the slides were viewed
again by both readers in concert until a consensus was reached. If
no agreement could be made, the section was discounted and not
used in the analysis. A 1:1 plot of the readers’ original band counts
was analyzed with a chi-square test of symmetry to assess whether
systematic reader bias occurred (Cailliet and Goldman, 2004).
The percent reader agreement (PA = [No. agreed/No. read] × 100)
between readers and PA ±1 year were also calculated to determine
reader precision (Cailliet and Goldman, 2004).
2.3. Age and growth models
Two traditional growth models were applied to the band count
data: the von Bertalanffy growth equation (von Bertalanffy, 1938,
1957) and the Gompertz growth equation (GGE) (Goldman, 2004;
Ricker, 1979). The formula for the VBGE is written as:
Lt = L∞ (1 − e−k(t−t0 ) )
where t is age, L∞ is asymptotic length, k is the growth coefficient,
and t0 is the x-intercept. The GGE is simply a modified VBGE using
weight rather than length and is written as:
g(t−t0 )
Wt = W∞ e−e
where W∞ is the asymptotic weight and g is the growth coeffi-
cient. The residual mean square error values (MSE), coefficient of
determination (r2 ), and level of significance were compared among
models. Additionally, a two-parameter VBGE was fitted to the data
using known length-at-birth (L0 = 300 mm TL) in lieu of the t0 value:
Lt = L∞ − (L∞ − L0 )e−kt
All age models were run using the R 2.6.2 nls function and estimated
by least-squares non-linear regression analysis.
A length-based Bayesian model was also applied to length
data. The model estimated the L∞ parameter of the VBGE
using length–frequency data (n = 989) obtained from fishery-
independent Southeast Area Monitoring and Assessment Program
(SEAMAP) trawl surveys and one additional fishery-independent
survey run by the National Oceanic and Atmospheric Adminis-
tration (NOAA) in the northern Gulf of Mexico. These surveys
use a random stratified design for trawl locations with propor-
tional allocations for depth, and take place in June–July and
October–November. The length data were collated from three ves-
sels conducting surveys over a period of 20 years (1988–2007). The
model is written as:
 
xi /
Yi = log for xi < 
1 − (xi /)
where xi s are the lengths,  is a proxy for L∞ , and Yi ∼ N(,  2 ).
A full description of the model and likelihood can be found in
Siegfried and Sansó (2006). A plot of the transformed data was used
to assess normality of the Yi s, and the mean of the normal prior for
L∞ ( = 1345 mm TL,  2 = 145) was based on maximum observed
size of captured S. dumeril in this study and from S. californica that
were recaptured and held in captivity (Cailliet et al., 1992). Finally, a
full Bayesian model, which fits the VBGE with Markov Chain Monte
Carlo methods (Gelman et al., 2004; Hastings, 1970), was applied to
the Atlantic angel shark length-at-band count data. The full model,
described in Siegfried and Sansó (2006), used informative priors for
t0 and k based on the published estimates of S. californica, as stated
above (Cailliet et al., 1992).
3. Results
Atlantic angel sharks included in the band count analysis ranged
in size from 275 to 1160 mm TL, with 87 females and 93 males
(Fig. 2). All lengths are reported in TL because the hypocercal
tail shape of angel sharks likely makes this measurement the
least variable. Morphometric relationships used to convert length
 I.E. Baremore et al. / Fisheries Research 99 (2009) 203–209 205

Fig. 1. Digital images of an Atlantic angel shark vertebra sectioned (A) in half, (B) at 0.9 mm, (C) at 0.3 mm, and (D) 0.6 mm.

and weight measurements are as follows: FL = 0.9501(TL) + 0.1607
(n = 1069, r2 = 0.99, p < 0.0001) and weight = 6.696e − 6(TL)3.033
(n = 988, r2 = 0.99, p < 0.0001). ANCOVA tests showed no signifi-
cant differences in these relationships between sexes (p > 0.05 for
both length–length and length–weight regressions), and pregnant
females were excluded from the length–weight regression.
Vertebral sections exhibited poor calcification, and in many
cases the intermedialia separated from the corpus calcarius after
the sections were glued to the slides (e.g. Fig. 1C). The APE between
readers was 5.81%, with a PA of 27.37%, PA ±1 band of 60.34%, and
PA ±2 bands of 72.63%. An age-bias plot showed little bias between
readers (Fig. 3), a chi-square contingency table showed equal bias
along all band counts (p > 0.10), and McNemar’s test found no bias
between readers at +1 or +2 band counts (p > 0.10), or at different
grouped band counts (p > 0.10).
Overall, band counts failed to produce realistic growth curves
regardless of which growth equation was used. The VBGE produced

Fig. 2. Length–frequency histogram of Atlantic angel sharks used for band count Fig. 3. Bias plot between Reader 1 and Reader 2 for band count analysis showing
analysis for females and males. little fundamental bias between readers. The line indicates a 1:1 relationship.
206 I.E. Baremore et al. / Fisheries Research 99 (2009) 203–209

Table 1
Results for the von Bertalanffy growth equation, Gompertz growth equation, and two-parameter VBGE. SE is the residual standard error of the model for the present study
and the standard error for Cailliet et al. (1992). Results are presented for combined sexes.

Study Model L∞ /W∞ k/g t0 SE

Present VBGE 2606 0.0146 −3.8372 10.73

Present GGE 9.76 0.1452 18.9981 1.58
Present Two-parameter VBGE Did not converge
Cailliet et al. (1992) VBGE (Gulland and Holt 1959) 1270 0.1460 2.5
Cailliet et al. (1992) Two-parameter VBGE 1252 0.1010

Fig. 4. Plots of band counts (A) by total length with the von Bertalanffy growth
equation fitted to the data and (B) the Gompertz growth equation fitted to weight-
at-band count data.

an overinflated L∞ of 2606 mm TL (Table 1, Fig. 4A), however, plots

of the residuals showed no systematic bias in length-at-band count.
Removal of outlier points did not produce a more favorable result.
The GGE produced an underestimated W∞ of 9.76 kg and unrealis-
tic t0 value of 18.99 (Table 1, Fig. 4B), and the residual plot showed
increasing error with weight. The two-parameter VBGE did not con-
verge.
The length-based Bayesian model also failed to converge, likely
due to the bimodal distribution of the transformed data (Fig. 5A).
Previous successful applications of this model were to data that
were normally distributed after the transformation. Furthermore,
the log of the variance increased exponentially (Fig. 5B), and
Fig. 5. Plots from the length-based Bayesian model: (A) histogram of the trans-
increasing the variance of the jumping distribution in the model
formed data showing the bimodality of the data, and (B) plot showing the
produced very different and unpredictable results (Figs. 6A–F), as exponential increase of the variance of the model.
the model could not compensate for both peaks in the data. Like-
wise, the full Bayesian model did not produce any reasonable results to length or weight using traditional or Bayesian growth mod-
for the VBGE, indicating that length-at-age analysis for this species els. Sections of vertebrae frequently had large holes or separations
was not realistic. between bands, making consistent band counts difficult. Though
band counts are most likely not predictive of age for S. dumeril,
4. Discussion there was an increase in band number with size. Atlantic angel
sharks smaller than 300 mm TL (neonates) had between two and
The vertebrae of Atlantic angel sharks did not appear to be valid six bands, and no change in angle associated with a birthmark was
ageing structures, as the band formation was not predictably related seen. Bands were, for the most part, evenly spaced and began very
 I.E. Baremore et al. / Fisheries Research 99 (2009) 203–209
Fig. 6. Plots of the first 100 iterations of the length-based Bayesian model with variance of the jumping distributions of (A) 1.50, (B) 1.75, (C) 2.00, (D) 2.50, (E) 2.75, and (F)
3.0. The lines represent the mean of the prior for L∞ (1345 mm TL).
close to the focus of the vertebral centra. However, there were many
cases in which double, and some cases, triple splitting of bands
occurred at the edge of the intermedialia (see Fig. 1). Additionally,
some vertebral centra had differing numbers of bands on either
side of the intermedialia. The band counts differed in some cases
by as many as four, depending on which side of the section was
read. Natanson and Cailliet (1990) found that growth band counts
of S. californica differed along the vertebral column, and that edge
formation was not temporally predictable. Similarly Natanson et al.
(2008) showed that basking sharks (Cetorhinus maximus) could not
be aged using band counts, and found a difference of up to 24 band
pairs among centra along the vertebral column of one specimen.
The authors suggested that band deposition for S. californica was
related to somatic growth, rather than time or age, based on cap-
tive growth and tag-recapture studies. Because no Atlantic angel
sharks were held in captivity for this study, it is unclear whether
this is the case in this species. Analyzing differences in band counts
along the vertebral column is an important step when assessing
the validity of vertebrae as ageing structures (Piercy et al., 2006),
however because the use of angel shark vertebral centra was dis-
counted, this method was not considered necessary for this study.
Centrum edge analysis was also not attempted because the edge
formation could not be characterized.
The lack of an asymptote in size with increasing band count
caused the VBGE to produce biologically unreasonable estimates
of L∞ and k, the GGE estimates were also unrealistic, and the
two-parameter VBGE did not converge. The length-based Bayesian
model was not successful due to the bimodal distribution of the
length data, and the model could only be forced to run through a
maximum 150 iterations. Several attempts made to find the source
of the bimodality were unsuccessful; when assessed separately by
vessel, sex, region (eastern vs. western Gulf of Mexico), depth, and
207
season, the data were always highly bimodal with the trough in
the length–frequency roughly corresponding with the estimated
size at maturity (Figs. 7A–E). The most plausible explanation for
this occurrence is sampling bias, though the length–frequency
of trawl-caught S. guggenheim in the Argentine-Uruguayan Com-
mon Fishing Zone was also bimodal (R. Vogler, pers. comm.). The
SEAMAP and other fishery-dependent trawl surveys took place in
the early summer and fall, therefore it is possible that migration
or depth-stratification of the mid-sized Atlantic angel sharks take
them out of the sampling areas during these times. These trawl
surveys were fairly extensive, however, and together covered most
of the U.S. Gulf of Mexico from depths of approximately 25–500 m.
Despite the fact that the trawls fished differently and were of differ-
ent sizes, the length–frequencies of angel sharks among the vessels
were always bimodal. The failure to converge shows an obvious
limitation with this method, which has performed well for several
other species.
The mechanisms of chondrichthyan vertebral growth remain
largely unknown, though the seasonal nature of growth band depo-
sition in temperate fishes is likely influenced by internal “biological
clocks” which regulate growth (Gelsleichter, 1998). Of the species
that have shown poor calcification of vertebral centra, most are
either primitive or deep water (Cailliet, 1990). Although angel
sharks are among the most derived of the shark-like elasmobranchs
(Compagno et al., 1990), they are benthic-associated, mostly deep
water species (McEachran and Fechhelm, 1998). Hypotheses for
the poor calcification of vertebrae in deep water elasmobranchs
include lack of photoperiod and temperature changes, food lim-
itation, and low calcium concentration (Cailliet, 1990). There is,
however, evidence that Atlantic angel sharks spend at least part
of their life history in shallow water, as they are known to have
an inshore–offshore migration in the U.S. north Atlantic Ocean
208 I.E. Baremore et al. / Fisheries Research 99 (2009) 203–209
Fig. 7. Plots of length–frequency data showing the bimodal distribution among factors (A) sex, (B) location, (C) depth, and (D) season.
(Compagno, 1984), and were captured in the Gulf of Mexico as shal-
low as 25 m in this study. Food limitation is also unlikely because the
Gulf of Mexico continental shelf has high productivity and Atlantic
angel sharks are top predators (Baremore et al., 2008; Cortés, 1999).
Additionally, Natanson and Cailliet (1990) collected all Pacific angel
sharks for their ageing study in depths of less than 77 m. Annual
band formation in elasmobranchs may be unrelated to tempera-
ture, as found in the little skate (Raja erinacea) (Natanson, 1993), and
may instead be influenced more by hormonal levels (Gelsleichter
and Musick, 1999).
A lack of a calcified structure (i.e. otolith) that can be used for
ageing analysis is rare among fishes, but is more common among
deep water, and especially slow-growing species (Treble et al.,
2008). However, more species are being aged in what are com-
monly thought to be ‘aseasonal’ environments, such as the deep sea
and tropical areas, as sampling and ageing techniques become more
sophisticated (Morales-Nin and Panfili, 2005). Laser ablation induc-
tively coupled plasma mass spectroscopy (LA-ICP-MS) is a relatively
new method for assessing the spatial distribution of elements in
cartilage of elasmobranchs, and has been demonstrated to effec-
tively elucidate band counts for round stingrays with fewer than
five band counts (Hale et al., 2006). This method could be applied to
angel shark vertebrae as it allows for detection of very small changes
in the elemental signature of cartilage, even when calcification is
poor.
The failure to find a valid age and growth method for the Atlantic
angel shark presents particular challenges to biologists and man-
agers. Though listed as a prohibited species (NMFS, 1999), S. dumeril
is impacted by at least one fishery, and the potential for future inter-
actions with other fisheries is high. Given the problems associated
with interpreting basic life history parameters using conventional
means, future studies on the age, growth, and reproduction of squa-
tinids should focus on large-scale tagging projects, captive growth
experiments, and/or novel ageing techniques such as LA-ICP-MS.
Squatinids throughout the world have seen catastrophic declines
due to heavy trawling activities, and several species have been listed
as endangered, threatened, or locally extirpated (IUCN, 2002). Alter-
native strategies for assessment of the life history of this species,
and potentially other squatinids, should be addressed before such
declines occur, rather than after the species has been impacted.
Acknowledgements
Thanks to Raffield Fisheries for their help and supply of angel
sharks throughout the years. L. Hollensead and D. Bethea helped
with processing of animals, and M. Winton, H. Moncrieff, H.
McCann, and T. Dillon sectioned the vertebrae. G. Pellegrin pro-
vided the SEAMAP data used in the analysis. Thanks also to M.
Passerotti for reviewing a previous version of this manuscript. All
Atlantic angel sharks were collected with a NOAA Fisheries Service
Exempted Fishing Permit (HMS-EFP-0301, EFP-04-01, EFP-05-01).
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