Buat Tuter Ikhtio

Journal of Fish Biology (2015) 87, 12711292
doi:10.1111/jfb.12829, available online at wileyonlinelibrary.com
Perspectives on elasmobranch life-history studies: a focus on

age validation and relevance to fishery managementa
G. M. Cailliet
Moss Landing Marine Laboratories, 8272 Moss Landing Road, Moss Landing, CA 95039,
U.S.A.
Life-history (age, growth, age validation, reproduction and demography) studies of elasmobranchs
date back to the middle of the last century with major early contributions made by British fishery scientists. As predicted by Holden in the early 1970s, many sharks and rays can be vulnerable to fishery
mortality because they grow slowly, mature late in life, reproduce infrequently, have relatively low
fecundities and can have relatively long life spans. As has now been found, however, not all species
exhibit these traits. Also, ageing structures (neural arches and caudal thorns), other than vertebrae and
spines, have since been evaluated. Various methods for validating age and growth estimates have been
developed and tested on numerous species of elasmobranchs. These include tagrecapture analyses,
oxytetracycline injections, centrum or spine edge and marginal increment analyses, and bomb radiocarbon dating of calcified structures. Application of these techniques has sometimes not only validated
relatively slow growth and long life span estimates, but also has produced other results. A brief historical perspective on the applications and limitations of these techniques for elasmobranchs is provided,
along with a discussion of selected species for which these techniques worked well, did not work at
all or have produced variable and conflicting results. Because many fishery management techniques
utilize age or stage-specific information, often through demographic analyses, accurate information on
the life histories of fished populations, especially age validation, is extremely important for the fishery
management of these cartilaginous fishes.
2015 The Fisheries Society of the British Isles
Key words: ageing; demography; growth; longevity; rays; sharks.
INTRODUCTION
This paper is intended to briefly trace the history of life-history studies on elasmobranchs, based upon, but not repeating, existing reviews (Cailliet et al., 1983a, 1986;
Cailliet, 1990; Cailliet & Goldman, 2004; Goldman et al., 2012). First, it will note the
early accomplishments of British and Japanese scientists. This will involve: (1) a brief
summary of the structures used for ageing, (2) how the growth zones in these structures
are analysed, verified and validated, (3) how well validation technique have worked
for groups of selected species and (4) how this information, including demographic
analyses, can be used to improve fisheries management.
The biology of the chondrichthyans is probably the least understood of the
major marine vertebrate groups. Detailed information on life history (age, growth,
reproduction and demography) is available only for a few dozen of the c. 1196 species
Tel.: +1 831 771 4432; email: Cailliet@mlml.calstate.edu
J. W. Jones Lecture.
a Twenty-fourth
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G. M. CAILLIET
of cartilaginous fishes worldwide, and this is mainly for species that are important
for directed fisheries or as by-catch (Cailliet & Ebert, 2014). There is considerable interspecific variation in life-history parameters of these cartilaginous fishes
(Compagno, 1990; Dulvy & Reynolds, 2002; Cailliet & Goldman, 2004; Goldman
et al., 2012). Studies on life-history traits are essential for understanding their population dynamics, especially as they relate to how they will respond to fishing pressure.
Accurate age estimates provide valuable information on age-specific recruitment,
maturity, reproductive output, mortality rates, longevity and growth rates of fished
populations.
The age, growth and reproduction of elasmobranchs is difficult to study because many
are large and highly mobile, difficult to sample, exhibit seasonal habitat movements and
have been, until recently, of minor commercial value. In addition, many of the conventional calcified structures used for ageing bony fishes (scales and otoliths; Cailliet et al.,
1983a) are not useful for elasmobranchs because they lack them. Scientists have, however, found and used other structures, such as vertebrae, spines and caudal thorns, to
provide age estimates of cartilaginous fishes.
Because the commercial exploitation of elasmobranchs has rapidly increased, this
makes information about their life histories essential for understanding and managing
their populations. The life-history parameters, longevity (length of life) and life span
(average time between birth and death), are also very important to consider when determining how to manage exploited populations (Cailliet & Andrews, 2008). If long-lived
fishes have had their ages and life spans underestimated, this could cause fishery management policies to be less effective.
Most sharks and rays have not yet been aged reliably (Cailliet & Goldman, 2004;
Goldman et al., 2012). For some species, e.g. deep-sea chondrichthyans, using the current scientific techniques on calcified structures such as vertebrae may not even be
possible, mainly due to poor calcification. Fortunately, some of the deep-sea squaliformes have calcified dorsal-fin spines.
The importance of age validation was strongly emphasized almost three decades ago
by Beamish & McFarlane (1983), who pointed out that few growth studies on fishes,
including elasmobranchs, had evaluated the temporal periodicity of growth zone (or
band pair; defined as one opaque and one translucent band) deposition in otoliths,
scales, spines and vertebral centra. This lack of information had hampered fishery scientists from obtaining an accurate and clear understanding of the growth processes that
these zones represented. This has been re-emphasized and reviewed more recently by
Campana (2001), among others. Many recent age, growth and longevity studies still
have not provided validated age estimates, making the parameters determined in their
studies less certain. Unfortunately, validation approaches such as tagging and oxytetracycline (OTC) injection studies are time-consuming and expensive, and are constrained
by small sample sizes.
Numerous elasmobranch verification and validation techniques have been reviewed
by Cailliet et al. (1986), Cailliet (1990), Cailliet & Goldman (2004) and Goldman et al.
(2012), but very few species have been convincingly studied. Although some chemical
analyses such as X-ray spectrometry and radioisotope ratios of lead 210 and radium 226
have been tried, they have met with mixed success. The radiometric technique, which
works for calcified otoliths in bony fishes (see Andrews et al., 2007 for an example of
rockfish Sebastes), and for spines in at least one deep-sea shark (Irvine et al., 2006a),
does not work in vertebral centra of cartilaginous fishes (Welden et al., 1987).
2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, 87, 12711292
C H O N D R I C H T H YA N A G E VA L I D AT I O N A N D M A N A G E M E N T
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EARLY APPROACHES AND STRUCTURES USED IN ELASMOBRANCH

AGE AND GROWTH STUDIES
Holden (1973, 1974, 1977) predicted that most elasmobranchs have life histories
making them particularly susceptible to overfishing (Cailliet, 1990; Ellis et al., 2005).
He relied on existing von Bertalanffy growth model parameters for several species that
had been studied using techniques available at that time (Ishiyama, 1951a, b; Pratt &
Casey, 1990). In most cases, he used growth parameters that were predicted by indirect
evidence, including size frequencies, body size at maturity, conception and birth, length
of the gestation period and maximum observed body size. In a few cases, however, he
had estimates of age and growth derived from growth zones (also called bands or rings;
Cailliet et al., 1983a, 1986, 2006) in calcified structures such as vertebral centra and
spines.
The basic process of ageing elasmobranchs is to remove these calcified vertebral
centra and spines (Holden & Meadows, 1962; Tucker, 1985; McFarlane & Beamish,
1987), and process them so that their growth zones could be counted (Cailliet et al.,
1983a; Cailliet, 1990; Cailliet & Goldman, 2004; Goldman et al., 2012). Once sufficient samples of all size classes are analysed, the length-at-age data are used to generate
a growth curve that represented the rate at which size (usually expressed as total length,
LT ) increases with increasing age (estimated from the number of band pairs).
Growth zones deposited in vertebral centra have been the main tools for age determination of elasmobranchs. Ridewood (1921) first described these zones in his review
of shark vertebrae, their structure and calcification processes. He also mentioned that
these zones might be useful in age determination studies. Over time, numerous authors
developed and used various techniques, including thin sectioning, to enhance these
zones (Cailliet & Goldman, 2004; Goldman et al., 2012). Either whole or sectioned
vertebral centra have been immersed in clove oil, xylene, and stained using alizarin
red, haematoxylin and silver nitrate. In one early study, Stevens (1975) estimated ages
of blue sharks Prionace glauca (L. 1758) using silver nitrate to stain growth zones in
vertebral centra, and found that his data correlated well with lengthfrequency data.
Also, X-radiography and X-ray spectrometry (to measure calcium and phosphorus in
growth zones; Jones & Geen, 1977) have been used.
MORE RECENT APPROACHES AND STRUCTURES IN ELASMOBRANCH

AGE AND GROWTH STUDIES
Sectioning the structures to enhance visibility of the growth zones has been one of
the major innovations in elasmobranch age and growth studies, along with staining
and X-radiography (Cailliet et al., 1983a; Cailliet, 1990). More recently, a histological approach has been employed (Natanson et al., 2007) and has often produced more
growth zones than in structures that have only been sectioned.
In those chondrichthyans for which neither vertebrae nor spines were useful for ageing, other structures, such as caudal thorns (Gallagher & Nolan, 1999; Gallagher et al.,
2006), and neural arches (McFarlane et al., 2002) have been used. Counts of growth
bands in the dorsal-fin spines of squaloids and chimaeras and in the neural arches of
hexanchiformes (McFarlane & Beamish, 1987) have proven useful, although they have
only been validated for a few species (Cailliet & Goldman, 2004; Goldman et al.,
2012). Gallagher & Nolan (1999) investigated the suitability of caudal thorns as an
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ageing structure for four species of skates and found that age estimates were similar between thorns and vertebral bands. The use of this alternative structure, although
successful in some skate species (Matta & Gunderson, 2007), has resulted in a high
degree of disagreement between thorn and vertebral band counts (Davis et al., 2007;
Ainsley et al., 2011, 2014; Perez, et al., 2011; James, et al., 2014; Winton et al., 2014).
Therefore, although caudal thorns may provide a non-lethal approach to ageing, their
use may not be appropriate for some species and should be investigated further before
being widely applied.
Therefore, one of the answers to Holdens (1977) plea for establishing acceptable
techniques for the age determination and validation of elasmobranchs lies in counting
the concentric zones found in their centra, spines and other calcified structures, and
various age validation techniques applied to them.
VERIFICATION AND VALIDATION OF GROWTH ZONES

Once calcified structures or their sections have been prepared, the process of identifying and counting the growth bands involves agreement on how to identify the birthmark
(the point in the structure at which embryonic growth changes to growth after birth),
and then on criteria for determining opaque and translucent bands (Goldman, 2004).
This is then followed by counts, either multiple by one reader or between or among
readers.
Verification involves consistent reproducibility of estimates of ages that will help
achieve high precision, but their accuracy must be determined using other means. Two
papers provide useful definitions of verification and validation for fishes in general
(Campana, 2001; Kimura et al., 2006). Goldman (2004) describes verification for
elasmobranchs as confirming an age estimate by comparison with other indeterminate methods. More specifically, verification encompasses two different elements:
reproducibility (which can be judged by multiple readings of the same structure) and
corroboration (which usually involves comparison of age estimates among two or
more independent sources, such as vertebral ages and growth of tagged animals, or
lengthfrequency modal analysis) (M. Francis, pers. comm.).
Basic tools used in verification first include precision assessments, such as average
per cent error (APE), per cent reader agreement (P), age-bias plots and tests of symmetry (Goldman, 2004). These provide a measure of precision of multiple readings of
growth zones.
Techniques that are used to evaluate the periodicity of band formation are called
validation (Campana, 2001). Some of these have been termed indeterminate validation, because they assess the outer edge of the calcified structure and its characteristics
over seasons, but do not directly validate the actual periodicity with which they are
deposited. The reader characterizes the structures edge as being opaque or translucent
and assesses how that changes over time. This is best done for as many sizes, seasons, locations and individuals as possible to see if there are ontogenetic, geographic or
seasonal changes in growth. For elasmobranchs, this usually involves vertebral centra,
and the process is called centrum edge analysis (CEA). A more quantitative technique
is marginal increment analysis (MIA), in which the structures margin is measured and
expressed as a portion of the last fully formed band pair (Natanson et al., 1995; Conrath et al., 2002), and plotted against the month of capture to evaluate the temporal
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periodicity of band-pair formation. A good example of a study in which both CEA

and MIA have been well described and used successfully is Smith et al. (2007) on the
diamond stingray Dasyatis dipterura (Jordan & Gilbert 1880).
Validation is very important in life-history studies of fish (Campana, 2001; Kimura
et al., 2006). Accuracy of age determination requires that absolute ages are validated,
not simply the frequency of increment formation in the calcified structure. Campana
(2001) and Goldman (2004) define validation as proving the accuracy of age estimates
by comparison with a determinate method. They go on to state that, strictly speaking,
validation of absolute age is only complete when it has been done for all age classes
available, with validation of the first growth increment being the critical component
for obtaining absolute ages, as mentioned in earlier papers by Beamish & McFarlane
(1983) and Cailliet (1990).
Several methods of age validation have been developed for elasmobranchs (Cailliet
et al., 1986; Cailliet, 1990; Cailliet & Goldman, 2004; Goldman, 2004; Goldman et al.,
2012). In early studies, Ishiyama (1951a, b) evaluated seasonal changes in the centrum
edge of vertebrae of two species of skates, and tentatively concluded that the alternating
bands were laid down in winter, with band pairs probably being deposited annually.
Other early studies used a combination of tagrecapture growth data (Holden, 1972),
both in the field and laboratory, CEA over seasons and OTC injections coupled with
laboratory and field growth data to validate ages in the thornback ray Raja clavata
L. 1758 (Holden & Vince, 1973). OTC is deposited in calcifying structures as they
develop and remain there until stimulated by ultraviolet light to glow so that the OTC
mark is visible in the growth zones that were being deposited at the time of injection.
This validation technique and its application have been summarized by Smith et al.
(2003).
Another relatively new validation technique is the use of bomb radiocarbon (14 C),
which was produced during atomic weapon testing in the 1950s and 1960s in the
Pacific Ocean, and can serve as a marker for specific years (i.e. ages) in the life history (or vertebral centra) of individual sharks (Campana, 2001; Campana et al., 2002,
2006; Goldman, 2004). As discussed below, this is becoming more common in chondrichthyan age validation studies, with one of the first applications on elasmobranchs
done by Campana et al. (2002) on two species of relatively long-lived mackerel sharks
(Lamnidae). Several recent studies have utilized this technique, providing useful information on elasmobranch age, growth and longevity. Combinations of these approaches
can be either very robust or they can produce conflicting results.
VALIDATION STUDIES FOR SELECTED SPECIES

In this section, three types of outcome observed in growth studies are reviewed. (1)
For some species, ageing was successful in that the growth zones have been validated
for all size or age classes and both sexes, and accurate growth parameters are achieved.
These are termed valid growth zones. (2) For some species, growth zones were found
not to represent time or age, based upon unsuccessful validation attempts. These are
termed non-valid growth zones. (3) For several species, age validation studies produced
variable, and often conflicting, results. These are termed partially valid growth zones.
In the two last categories, further studies using different techniques will be necessary
to provide sufficiently accurate life-history parameters for use in fishery management.
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VA L I D G R O W T H Z O N E S
In this first category, studies of three types of elasmobranchs for which age estimates
appear to be valid for all size and age classes, both sexes and for which the growth
curves and longevity estimates are accurate and should be quite useful are summarized.
Batoids
Age estimates for several skate and ray species have been validated, using combinations of several techniques, including CEA, MIA, field tagrecapture growth and
utilizing OTC marks (Ishiyama, 1951a, b; Holden & Vince, 1973; Gallagher & Nolan,
1999; Matta & Gunderson, 2007). Smith et al. (2007) used both CEA and MIA to
validate the growth of D. dipterura.
McPhie & Campana (2009) reported the only direct validation for a skate species
using 14 C to provide evidence of annual band-pair formation in four species of skates
off the eastern coast of Canada. They concluded that the age of 28 years for one of
these was the oldest validated age reported for any batoid species. White et al. (2014)
used tagrecapture age data to produce reasonable age and growth parameters for four
species of shark-like batoids of conservation concern.
Leopard shark Triakis semifasciata Girard 1855
Several studies have shown that the growth zones in T. semifasciata are annual.
Smith (1984) tagged and OTC-injected close to 2000 T. semifasciata in South San
Francisco Bay, and got recaptures over time with OTC injections demonstrating growth
and time-at-liberty agreed (Smith & Abramson, 1990). These validated growth zones
allowed Kusher et al. (1992) to produce growth curves and an estimate of longevity
for this species. Finally, Smith et al. (2003) reported on the recapture of an individual
after 20 years at large, with band-pair counts agreeing completely with time-at-liberty.
Spiny dogfishes Squalus acanthias L. 1758 and Squalus suckleyi (Girard 1855)
In the eastern North Atlantic Ocean, Tucker (1985) utilized tag-recapture with OTC
marks in dorsal-fin spines to validate the growth of S. acanthias. In the eastern North
Pacific Ocean, Beamish & McFarlane (1985) validated band deposition as annual
in dorsal spines for S. suckleyi also using spines from tag-recaptured, OTC-injected
specimens.
Age validation using 14 C was further provided by Campana et al. (2006), who utilized
14
C to validate age estimates in both the eastern North Pacific and eastern and western
North Atlantic. Their results showed slower growth rates and higher longevity using
14
C data than was found with vertebral band counts. Indeed, the differences between
the Atlantic and Pacific Squalus spp. age and longevity estimates may be due to the
recent discovery that the species of Squalus in the eastern North Pacific is S. suckleyi
not S. acanthias (Ebert et al., 2010). The western North Atlantic population is the same
species as the eastern North Atlantic, so the results of Tucker (1985) agree with the 14 C
data in Campana et al. (2006).
N O N- VA L I D G R O W T H Z O N E S
Of the elasmobranch species studied, several have proven difficult or impossible to

age using conventional methods, even for species in which vertebral banding is evident.
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Some studies have shown that there is no temporal periodicity related to the deposition
of vertebral growth zones.
Pacific angel sharks Squatina californica Ayres 1859
Natanson & Cailliet (1990) found that vertebral growth zones in S. californica were
not useful for ageing since tag-recaptured and OTC-injected specimens did not support
an annual deposition pattern, and their band counts differed along the vertebral column.
This led them to propose a somatic growth hypothesis for band formation.
Unable to age S. californica with vertebral centrum bands, Cailliet et al. (1992)
applied Gulland & Holt (1959) methodology to tagrecapture data to derive von Bertalanffy growth parameters for this species.
Basking shark Cetorhinus maximus (Gunnerus 1765)
Natanson et al. (2008) found that young C. maximus had similar band-pair counts
along the vertebral column, while older, larger ones had different band-pair counts (up
to 24 band-pair differences) occurring along their vertebral columns. They termed this
ontogenetic vertebral growth. Even though Parker & Stott (1965) were convinced that
their vertebrae had valid growth zones in them, Pauly (2002 and unpubl. data) used a
length-based growth model to contradict this idea. Nonetheless, Natanson et al. (2008)
used vertebral band-pair counts to conservatively estimate growth of this species.
Deep-water elasmobranchs
A common problem with ageing many deep-dwelling shark and ray species is that
banding patterns in vertebral centra are difficult to discern due to poor vertebral calcification (Cailliet et al., 1983a; Cailliet & Goldman, 2004; Goldman et al., 2012). Several
vertebral staining techniques have been used in attempts to improve band clarity, with
little success. When available, dorsal-fin spines of squaliforms have been used.
Thus, studies on deep-sea catsharks (Correia & Figueiredo, 1997), skates
(Natanson et al., 2007) and squaliform elasmobranchs (Clarke et al., 2002; Clarke &
Irvine, 2006; Irvine et al., 2006a, b, 2012; Cotton et al., 2013; Rigby et al., 2014),
have not been successful at age validation. Irvine et al. (2006a, b) described banding
patterns in the dorsal-fin spines of the southern lantern shark Etmopterus baxteri
Garrick 1957 and the longnose velvet dogfish Centroselachus crepidater (Barbosa
du Bocage & de Brito Capello 1864), in which there are more bands in larger specimens, but their age estimates have only been preliminarily validated for the latter
using radiometric estimates of Fenton (2001). Therefore, it has not been possible to
determine their ages and longevity and how these might be influenced by the deep-sea
conditions.
It is commonly thought that deep-dwelling fishes have life-history traits that make
them vulnerable to fishing, especially since fisheries are targeting deeper habitats
(Roberts, 2002). Even with the difficulties of ageing deep-water elasmobranchs,
sufficient life-history information was available for Simpfendorfer & Kyne (2009),
Kyne & Simpfendorfer (2010) and Rigby & Simpfendorfer (2015) to analyse the
life-history traits of these fishes and found them to typically have lower growth rates,
later ages at maturity and higher longevity than in both shelf and pelagic species.
Indeed, Simpfendorfer & Kyne (2009) had sufficient life-history information to
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G. M. CAILLIET
calculate intrinsic rebound potentials (IRPs; Smith et al., 1998) for over a dozen
species, demonstrating the relationship between low productivity (IRPs) and late age
of maturity and depth of occurrence. Nonetheless, age validation is still necessary for
deep-sea elasmobranchs.
PA RT I A L LY VA L I D G R O W T H Z O N E S
The final category includes studies on species for which confusing or inconsistent age
validations results have been obtained. This includes species with valid age estimates
that cover part of the life cycle of a species well, but not other parts. As a result, only part
of the life cycle is validated, or two parts validated with different techniques and producing differing results. In many of these cases, attempts to validate ages of sharks and
rays with OTC, tagrecapture, edge analysis and 14 C have produced mixed, often contradictory or conflicting, results. Therefore, the growth functions, curves, age-specific
life-history parameters and longevity are uncertain.
Characteristic results from such studies include: (1) vertebral band patterns that are
difficult to read, especially in older, larger individuals; (2) techniques of preparation
(e.g. sectioning, histology, staining and other zone enhancements) that can produce
different results; (3) ontogenetic stages that appear to produce different band-pattern
determination and hence age estimates; (4) sharks that may occupy different horizontal
(latitude and longitude) and vertical (temperature, depth and food) habitats, thus causing banding patterns to differ; (5) populations that might differ in their band deposition
patterns before and after high fishing morality, perhaps due to density-dependent factors; (6) growth that might continue somatically in larger, older sharks, but bands that
either cease being deposited or become less obvious.
The last category, called the age underestimation (Francis et al., 2007) or missing time (Passerotti et al., 2014) hypotheses is best described by Francis et al. (2007)
as the process of underageing adults, usually via ceased band-pair deposition in the
vertebrae of older sharks. This has also been described by Natanson et al. (2014) as
increasing evidence that band-pair deposition does not remain annual through life
and that growth zones are missed in vertebral centra, especially without histological
techniques for older specimens. Another apt description of the problem was stated by
Passerotti et al. (2014) that growth band deposition cannot be universally assumed to
represent annual growth and reinforces the need for age validation through ontogeny
in every species. The species for which these descriptions apply are presented next.
Shortfin mako Isurus oxyrinchus Rafinesque 1810
This species has a long history of age and growth studies with differing assumptions about, and evidence for, band-pair deposition. Pratt & Casey (1983) used
size-frequency and tagging data to conclude that two band pairs were deposited per
year in vertebral centra (biannual deposition rate). Cailliet et al. (1983b) assumed that
one band pair was deposited per year (annual deposition rate) and derived growth
curves using X-rayed vertebral centra that were slower than those of Pratt & Casey
(1983).
Bomb radiocarbon data were obtained for a vertebral centrum of I. oxyrinchus by
Campana et al. (2002), which indicated the one-band-pair-per-year (annual) hypothesis
was correct. This was followed by another 14 C study of I. oxyrinchus vertebrae by
Ardizzone et al. (2006), which also found good evidence for that hypothesis. Neither
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of these two studies eliminated the possibility of two band pairs per year for the earliest
growth. It appears, however, that for most of its life only one band pair was deposited
per year.
Meanwhile, age and growth studies were carried out on the same species elsewhere
using various validation techniques. Ribot-Carballel et al. (2005) studied young
(15 year-old) I. oxyrinchus off Baja California Sur, Mexico, and used CEA to
support their annual band-pair assumption. Bishop et al. (2006) studied this species
off New Zealand and assumed annual band-pair deposition. They got similar growth
estimates to those by authors who used the same assumption, and they aged the one
14
C-dated specimen from Campana et al. (2002), getting the same age of 21 years.
Natanson et al. (2006) assumed that the 14 C age validation (Campana et al., 2002;
Ardizzone et al., 2006) was correct, and combined that information with additional
size-frequency analysis and tagrecapture data (some with OTC injection data), to
come up with similar band counts at various sizes, but interpreted the early band-pair
data differently than Pratt & Casey (1983). Semba et al. (2009) used CEA to document
one band pair per year and obtained similar growth curves. These were backed by a
new statistical analysis technique of Okamura & Semba (2009), who used their data
on centrum edge opacity over months and statistically demonstrated that CEA did differ
over seasons, supporting the annual band-pair hypothesis. Cerna & Licandeo (2009)
produced similar CEA results, along with size-frequency analysis, for I. oxyrinchus
from the south-eastern Pacific Ocean off Chile and supported the annual band-pair
hypothesis.
Additional tagrecapture data, along with OTC marking and lengthfrequency analysis of the eastern North Pacific I. oxyrinchus, were analysed by Wells et al. (2013).
They could only examine tag-recaptured mako that were under 200 cm fork length
(LF ), but for those, the OTC-marked vertebrae support a pattern of biannual deposition for the first 5 years of life. They summarized the work to date and thought that the
differences in rates of band-pair deposition could be due to factors such as study location, methods and ontogeny, especially if different age classes of I. oxyrinchus occupy
different oceanographic regions during life.
Doo et al. (2015) utilized significant CEA but non-significant relative marginal
increment (a type of MIA) analyses to document annual band-pair deposition in I.
oxyrinchus in the western South Atlantic Ocean. They used Bayesian analysis to produce growth curves that varied depending on ontogenetic stage.
Thus, for I. oxyrinchus, it appears that growth rates, based upon band-pair deposition,
vary with size and age, thus making interpretation of their growth characteristics, age at
maturity and longevity somewhat difficult. This emphasizes the need to study a species
at various locations across its distribution range and to validate, when possible, all age
classes, using several techniques.
White shark Carcharodon carcharias (L. 1758)
The first study on the age and growth of C. carcharias was carried out by Cailliet
et al. (1985), in which growth zones were counted from X-rays of half vertebrae from
only 21 specimens off California. There was no validation, and the assumption of one
band pair per year was made. Longevity was roughly estimated to be 30 years, with
the oldest shark aged at 14+ years old. Wintner & Cliff (1999) found similar results
for C. carcharias off South Africa, but they had a larger sample size. One tagged
and OTC-injected shark was recaptured that grew c. 27 cm year1 but it was among
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G. M. CAILLIET
the smaller and younger specimens. An MIA analysis was not significant. Thus, they
assumed one band pair per year.
Kerr et al. (2006) used some of the same specimens as Cailliet et al. (1985) and analysed growth zones for 14 C and stable isotopes. Their results were similar to those in
the original study, but the 14 C appeared to demonstrate uptake of carbon sources that
are not directly tied to the surface waters, and that C. carcharias do not consume prey
that had direct contact with primary producers and consumers likely to uptake 14 C in a
timely fashion. The assumption was that 14 C dating could not be applied because a mix
of radiocarbon-depleted food sources confounded the comparison of levels measured
in the vertebrae with the 14 C reference levels.
Recently, three additional studies applied 14 C age validation techniques to C. carcharias. Hamady et al. (2014) found 14 C values in vertebrae of four female and four
male C. carcharias from the western North Atlantic Ocean that generated age estimates up to 40 years for the largest female (526 cm LF ) and 73 years for the largest
male (493 cm LF ). These values are considerably higher than those produced by von
Bertalanffy growth parameters from vertebral centra X-radiography.
A re-analysis of Kerr et al.s (2006) data by Andrews & Kerr (2015) suggested that a
re-assignment of the signal phase to older years of formation (a shift in age) produced a
validated life span estimate exceeding 30 years for eastern North Pacific C. carcharias.
This made the data and analyses in both of these papers agree more closely with
those of Hamady et al. (2014) and predicted that C. carcharias live longer (exceeding 30 years) than previously thought. This was interpreted as missing time in the
vertebrae.
Natanson & Skomal (2015) re-assessed band-pair counts in the vertebral centra of 81
specimens of C. carcharias collected between 1963 and 2010 from the western North
Atlantic Ocean. They also re-interpreted the 14 C data of Hamady et al. (2014) and concluded that longevity is more likely to reach c. 44 years (the original 73 year estimate
was only validated to c. 40 years based on the limits of 14 C dating), thus allowing them
to produce a different growth curve.
Natanson & Skomal (2015) also , however, provided evidence that there can be different band-pair counts along the vertebral column in some C. carcharias, thus lending
credence to the somatic growth hypothesis originally used to explain S. californica
vertebral growth. The resulting growth curve has two main phases in it, each reflecting
the knowledge that has been gained from the 14 C analyses and use of several different
growth curve-fitting models. It has been suggested that vertebrae of C. carcharias may
not be a reliable indicator of age because of their nomadic behaviour, feast-and-famine
approach to feeding and the vast habitat changes observed through ontogeny, both
within and among individuals (Andrews & Kerr, 2015).
Other lamniform sharks
Natanson et al. (2002) used vertebral annuli from 578 specimens, along with age
validation using OTC tagrecapture data and known-age porbeagle Lamna nasus
(Bonnaterre 1788) to validate ages up to 11 years. Their extrapolation predicted
longevity of up to 4546 years for an unfished population.
In a related study, Campana et al. (2002) used 14 C analysis in L. nasus from the
western North Atlantic Ocean to show that they live up to 26 years, and possibly
35 years old.
1281
Francis et al. (2007) pointed out that, for L. nasus off New Zealand, ages have been
underestimated by using vertebral centra, especially in the larger, older individuals.
They attributed this to cessation of somatic growth, and therefore vertebrae, in this
relatively long-lived shark species. They did an additional 37 14 C assays from 11 L.
nasus ranging from 163 to 200 cm LF , and found that L. nasus from New Zealand
live twice as long as western North Atlantic L. nasus, and have very different growth
characteristics.
Early studies on sand tiger Carcharias taurus Rafinesque 1810 growth by Branstetter
& Musick (1994), Goldman et al. (2006) and Carlson et al. (2009) provided different
estimates of growth, age at maturity and longevity, with Goldman et al.s (2006) study
providing evidence of annual band-pair deposition from captive OTC injection studies.
No specimen was found to be older than 17 years.
Passerotti et al. (2014) utilized both age estimates from sectioned vertebral centra and
from 14 C values. They found that the C. taurus age estimates up to 12 years old (from
vertebrae used in Goldman et al., 2006) were validated by 14 C, but that this technique
estimated that females reached at least 49 years and males at least 34 years. Thus, ageing using vertebral centrum band patterns underestimated ages in the larger, and older,
individuals, by as much as 1112 years in the western North Atlantic and 1418 years
in the south-western Indian Ocean. They concluded that the traditional ageing methodology does not produce accurate age estimates for fish over 12 years and they termed
this phenomenon missing time. They emphasized that growth-band deposition cannot
be universally assumed to represent annual growth, and strongly recommended age
validation throughout ontogeny in every species.
Other carcharhinids
Andrews et al. (2011) studied the sandbar shark Carcharhinus plumbeus (Nardo
1827) and found that ageing using vertebral band counts was only valid up to
1012 years, but that 14 C estimates of longevity were at least 2026 years, a difference of 511 years based on band counts. Geraghty et al. (2013) studied C. plumbeus
in eastern temperate Australia and got similar longevities, using MIA as validation.
Chin et al. (2013) found similar results for blacktip reef sharks Carcharhinus
melanopterus (Quoy & Gaimard 1824), which possibly stops depositing vertebral
growth zones as determined by a tagrecapture study. A similar situation was documented for dusky sharks Carcharhinus obscurus (Lesueur 1818) (Natanson et al.,
2014). The original growth curves using just vertebral band counts from sharks in
the western North Atlantic and western Australia (Natanson et al., 1995; Natanson
& Kohler, 1996; Simpfendorfer et al., 2002; Geraghty et al., 2013) produced age
estimates that were relatively high and similar. Bomb radiocarbon analyses showed
that annual band pairs in vertebrae were valid up to c. 11 years of age, but that vertebral
band counts underestimated true age, which reached at least 42 years of age (Natanson
et al., 2014).
DEMOGRAPHIC ANALYSES
Demographic analyses have been carried out for only a few species, mainly those for
which ages have been either fully or partially validated and age-specific mortality and
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G. M. CAILLIET
reproductive output have been reasonably estimated (Cailliet & Ebert, 2014). With elasmobranch age validation, age-structured models, such as life-history tables and matrix
population models, can be utilized appropriately for analysing population dynamics
through various fishery models (Corts, 1998). Gedamke et al. (2007) reviewed the
pros and cons of using demographic models to determine intrinsic rates of increase
and other parameters to help guide sustainable fishery management policies.
Demographic analyses have helped manage some of those species for which ages
have been validated. For example, when life-history demographic analyses were performed on T. semifasciata from California waters (Cailliet, 1992; Kusher et al., 1992),
the results produced an intrinsic rate of population increase (r) of 0067, in the absence
of fishing pressure, and the implication was that when fishing mortality is included,
these population parameters can be significantly reduced, influencing the need for management procedures such as size and bag limits.
The demographic analysis carried out for S. californica (Cailliet et al., 1992) was not
based on age-validated life-history parameters, but rather on tagrecapture analysis
that produced von Bertalanffy growth curves. With additional size-specific reproductive output data, a reasonable demographic analysis was accomplished. This has been
used in fishery management policies for this species in California.
For D. dipterura (Smith et al., 2008), ages were indeterminately validated using CEA
and MIA and demographic parameters were produced using several methods. It is presumed that these will prove useful for fishery management purposes in Mexico.
For I. oxyrinchus, there has been one attempt to analyse their demography (Tsai et al.,
2014). Due to the inconsistency among the validation attempts in the studies discussed
earlier, they chose to use a two-sex, stage-based matrix to model the most likely population parameters for population growth. The uncertainty regarding age at maturity
and longevity was found to be relatively minor, but uncertainty related to survival rate
and fecundity was more important in deriving population growth rate estimates. They
proposed size-limit management policies for this species throughout its range.
The demography of the C. carcharias was modelled in a study using life-history
tables, Leslie matrices and several stage-based matrix models to evaluate four species
chosen to represent different life histories: (1) the pelagic stingray Pteroplatytrygon
violacea (Bonaparte 1832), (2) C. taurus, (3) the pelagic thresher shark Alopias pelagicus Nakamura 1935 and (4) C. carcharias (Mollet & Cailliet, 2002). For C. carcharias,
the original growth parameters of Cailliet et al. (1985) and Wintner & Cliff (1999)
were used. This, of course, will eventually be influenced by the final interpretation
of C. carcharias growth, as additional age validation results come in. But, this initial study serves as a baseline for such a demographic analysis. Indeed, Burgess et al.
(2014) used these demographic parameters to estimate the population size of the C.
carcharias population off central California.
Brewster-Geisz & Miller (2000) undertook a stage-based demographic analysis
for C. plumbeus but this also is a preliminary analysis given the uncertainty in its
life-history parameters.
For skates, recent demographic analyses have been carried out, even though the age,
growth and longevity parameters have not been validated. Barnett et al. (2013) performed demographic analyses for five species of skates in the genus Bathyraja. These
analyses provided estimates of demographic parameters that indicated these populations had low growth coefficients, thus influencing their fisheries management policies
(Corts, 2002, 2007).
1283
THE ROLE OF ELASMOBRANCH LIFE-HISTORY STUDIES

IN FISHERIES MANAGEMENT
When life histories are compared across taxa (Hoenig & Gruber, 1990; Corts,
1998, 2002), it is immediately apparent that many sharks and rays are among the
latest-maturing and slowest-reproducing of vertebrates. This, and the relatively close
relationship between parent stock and subsequent recruitment from their live-borne or
egg-borne early development, contrasts markedly with most teleosts, which support
most fisheries (Musick, 1999; Musick et al., 2000; Stevens et al., 2000, 2005). Shark
and ray life histories, however, vary considerably among taxa and locations, leading
to variation in their vulnerability to exploitation.
A relatively recent analytical technique, the IRP (Au & Smith, 1997; Smith et al.,
1998, and refined into an even simpler calculation model by Au et al., 2015), requires
less basic life-history information and may prove very useful in early management
efforts on newly developing shark and ray fisheries. Their method incorporates that
density dependence as the intrinsic rate of increase (r) depends on the level of fishing
mortality and the resulting decrease in population size. In their model, productivity is
strongly affected by age at maturity and little affected by maximum age.
Sharks with the highest IRP values tend to be smaller, early-maturing, relatively
short-lived, inshore coastal species such as smoothhounds Mustelus spp., the sharpnose
shark Rhizoprionodon terraenovae (Richardson 1836) (Corts, 1995; Simpfendorfer,
1999) and the bonnethead shark Sphyrna tiburo (L. 1758) (Corts & Parsons,
1996). Those with the lowest IRP values tended to be larger-sized, slow-growing,
late-maturing and long-lived coastal sharks such as C. obscurus, C. plumbeus and
C. taurus, along with the scalloped hammerhead shark Sphyrna lewini (Griffith &
Smith 1834). Smaller-sized species such as S. acanthias and S. suckleyi and the tope
Galeorhinus galeus (L. 1758) appear to also be in this group (Smith et al., 1998).
As mentioned earlier, Simpfendorfer & Kyne (2009) have added many deep-sea
chondrichthyans to these IRP curves and they tended to fit with the slow-growing, late
maturing and long-lived elasmobranchs mentioned above.
Many studies have looked for other life-history traits that might be correlated with
response to exploitation, such as body size, with larger species possibly having lower
replacement rates than smaller species (Walker & Hislop, 1998; Dulvy et al., 2000,
2005, 2008, 2014; Dulvy & Reynolds, 2002; Dulvy & Forrest, 2010). This trend,
however, has not been shown to be widespread nor does there appear to be a body
size correlation with Smith et al.s (1998) IRP (Stevens et al., 2000; Corts, 2002).
Many relatively small deep-water species are among the most unproductive, long-lived
and consequently most vulnerable elasmobranch species (Smith et al., 1998; Kyne &
Simpfendorfer, 2010; Garca et al., 2008; Winton et al., 2014). To determine which
species are potentially vulnerable to exploitation information on growth rate, age at
maturity, fecundity and longevity is required, often in conjunction with each other. All
of these rely on adequate age validation to be maximally useful.
Stock assessments are only as good as the data used in their production. Accurate
life-history parameters will produce more reliable management strategies. In addition,
because latitudinal variation in growth rates is often reported in marine species, populations from higher latitude seas generally attain greater maximum ages and ages at
maturity (Cailliet & Ebert, 2014). Thus, it is important to obtain life-history information and conduct demographic analyses in all regions of a species range, particularly
1284
G. M. CAILLIET
in areas where the population is subject to exploitation (Lombardi-Carlson et al., 2003;

Frisk & Miller, 2006; Frisk, 2010).
THE FUTURE OF ELASMOBRANCH AGE AND GROWTH STUDIES

Several decades ago, Cailliet & Tanaka (1990) provided recommendations for future
research to better understand the life histories of elasmobranchs. They emphasized
the need for better verification and validation studies, more tagging studies (especially
with markers such as OTC), larger sample sizes, acceptance of individual variation
and higher precision and accuracy to increase the likelihood that age and growth studies would produce good growth models. While they did not mention CEA and MIA,
these indirect validation approaches have been emphasized in later reviews and discussed here.
Of the six methods of age determination and verification promoted by Cailliet &
Tanaka (1990), several have worked, but others have not. Improved image analysis and
computer-aided ageing is now available and electron microprobe elemental analysis
has been attempted (Cailliet & Radtke, 1987) but not used extensively or effectively.
Radiometric dating was tried by Welden et al. (1987) but did not succeed in elasmobranch vertebrae due to violation of assumptions, but might be useful in spines (Irvine
et al., 2006a). The analysis of stable isotopes, tissue protein concentrations (fatty acids)
and calcium physiology have been attempted, but little progress has been made with
these approaches leading to better growth estimates of elasmobranchs.
While not an ageing or age validation technique, the recent use of near infrared spectroscopy (NIRS; Rigby et al., 2014; Rigby & Simpfendorfer, 2015) might become a
useful analytical technique for elasmobranch age and growth studies. Unfortunately,
the actual mechanism that NIRS uses in age and growth studies is still unclear, so it
remains untested.
The use of 14 C analysis, on the other hand, has increased substantially and has shed
light on various aspects of elasmobranch growth and physiology, but often with mixed
results, as seen earlier in this paper. This approach deserves more attention, but its
use is limited by the timing of the bomb tests and the requirement that specimens
were old enough to have been exposed to 14 C through time before, during and after
the nuclear tests in the 1950s and 1960s. Perhaps, the radiation coming from Japans
earthquake-damaged Fukushima nuclear power plant could provide a similar tool. It
is known that Cesium-134 and Cesium-137 have been produced and detected in the
Pacific Ocean (Pacchioli, 2013). Even though these radioisotopes have relatively short
half lives, they might be useful for assessing annual band-pair deposition in fishes that
live near the source in Japan, or at more distant sites as they progress across the North
Pacific Ocean.
Undoubtedly, scientists will come up with additional ageing and age validation
approaches that will help more clearly describe the life histories of sharks and rays.
As a result, better fisheries management will be possible.
I thank D. Sims for inviting me to prepare this paper and to speak at the July 2015 meeting of
the Fisheries Society of the British Isles. I very much appreciate the travel funding I received
from FSBI and the Marine Biological Association of the United Kingdom. I have received
much good advice from discussions with A. Andrews (NMFS, Honolulu, Hawaii), G. Burgess
(University of Florida, Gainesville, Florida), S. Campana (Senior Scientist, Canadian Shark
1285
Research Laboratory, Bedford Institute of Oceanography, Dartmouth, Nova Scotia), E. Corts

(NMFS Panama City Laboratory, Florida), D. Ebert (Pacific Shark Research Center, Moss
Landing Marine Laboratories), M. Francis (National Institute of Water and Atmospheric
Research, Wellington, New Zealand), K. Goldman (Alaska Department of Fish and Wildlife),
J. Musick (Virginia Institute of Marine Sciences), L. Natanson (NOAA Fisheries Service,
Northeast Fisheries Science Center), M. Passerotti (NMFS Panama City Laboratory, Florida),
C. Simpfendorfer (James Cook University, Australia), S. E. Smith (NMFS, SWFSC, retired)
and J. Stevens (CSIRO, Hobart, Tasmania, retired). All provided invaluable assistance on various portions of this study, with three individuals, including M. Francis, J. Ellis (CEFAS) and
an anonymous reviewer, providing constructive comments for the revision of this manuscript.
Funding for this paper and the results it summarizes was provided by NOAA/NMFS to the
National Shark Research Consortium and Pacific Shark Research Center at Moss Landing
Marine Laboratories, the David and Lucile Packard Foundation and the North Pacific Research
Board.
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Journal of Fish Biology (2015) 87, 12711292

doi:10.1111/jfb.12829, available online at wileyonlinelibrary.com

Perspectives on elasmobranch life-history studies: a focus on

Key words: ageing; demography; growth; longevity; rays; sharks.

EARLY APPROACHES AND STRUCTURES USED IN ELASMOBRANCH

MORE RECENT APPROACHES AND STRUCTURES IN ELASMOBRANCH

VERIFICATION AND VALIDATION OF GROWTH ZONES

periodicity of band-pair formation. A good example of a study in which both CEA

VALIDATION STUDIES FOR SELECTED SPECIES

Of the elasmobranch species studied, several have proven difficult or impossible to

THE ROLE OF ELASMOBRANCH LIFE-HISTORY STUDIES

in areas where the population is subject to exploitation (Lombardi-Carlson et al., 2003;

THE FUTURE OF ELASMOBRANCH AGE AND GROWTH STUDIES

Research Laboratory, Bedford Institute of Oceanography, Dartmouth, Nova Scotia), E. Corts

Lombardi-Carlson, L. A., Corts, E., Parsons, G. R. & Manire, C. A. (2003). Latitudinal

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