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This article was downloaded by: [The University of Manchester Library] On: 20 October 2014, At: 08:10 Publisher: Taylor & Francis Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK Transactions of the American Fisheries Society Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/utaf20 Age and Growth of the Common Thresher Shark in the Western North Atlantic Ocean Brian J. Gervelis a & Lisa J. Natanson a a National Oceanic and Atmospheric Administration , National Marine Fisheries Service , 28 Tarzwell Drive, Narragansett , Rhode Island , 02882 , USA Published online: 04 Oct 2013. To cite this article: Brian J. Gervelis & Lisa J. Natanson (2013) Age and Growth of the Common Thresher Shark in the Western North Atlantic Ocean, Transactions of the American Fisheries Society, 142:6, 1535-1545, DOI: 10.1080/00028487.2013.815658 To link to this article: http://dx.doi.org/10.1080/00028487.2013.815658 PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http:// www.tandfonline.com/page/terms-and-conditions

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Page 1: Age and Growth of the Common Thresher Shark in the Western North Atlantic Ocean

This article was downloaded by: [The University of Manchester Library]On: 20 October 2014, At: 08:10Publisher: Taylor & FrancisInforma Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House,37-41 Mortimer Street, London W1T 3JH, UK

Transactions of the American Fisheries SocietyPublication details, including instructions for authors and subscription information:http://www.tandfonline.com/loi/utaf20

Age and Growth of the Common Thresher Shark in theWestern North Atlantic OceanBrian J. Gervelis a & Lisa J. Natanson aa National Oceanic and Atmospheric Administration , National Marine Fisheries Service , 28Tarzwell Drive, Narragansett , Rhode Island , 02882 , USAPublished online: 04 Oct 2013.

To cite this article: Brian J. Gervelis & Lisa J. Natanson (2013) Age and Growth of the Common Thresher Shark in the WesternNorth Atlantic Ocean, Transactions of the American Fisheries Society, 142:6, 1535-1545, DOI: 10.1080/00028487.2013.815658

To link to this article: http://dx.doi.org/10.1080/00028487.2013.815658

PLEASE SCROLL DOWN FOR ARTICLE

Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) containedin the publications on our platform. However, Taylor & Francis, our agents, and our licensors make norepresentations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of theContent. Any opinions and views expressed in this publication are the opinions and views of the authors, andare not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon andshould be independently verified with primary sources of information. Taylor and Francis shall not be liable forany losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoeveror howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use ofthe Content.

This article may be used for research, teaching, and private study purposes. Any substantial or systematicreproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in anyform to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http://www.tandfonline.com/page/terms-and-conditions

Page 2: Age and Growth of the Common Thresher Shark in the Western North Atlantic Ocean

Transactions of the American Fisheries Society 142:1535–1545, 2013American Fisheries Society 2013ISSN: 0002-8487 print / 1548-8659 onlineDOI: 10.1080/00028487.2013.815658

ARTICLE

Age and Growth of the Common Thresher Sharkin the Western North Atlantic Ocean

Brian J. Gervelis* and Lisa J. NatansonNational Oceanic and Atmospheric Administration, National Marine Fisheries Service,28 Tarzwell Drive, Narragansett, Rhode Island 02882, USA

AbstractAge and growth estimates were generated for the Common Thresher Shark Alopias vulpinus in the western North

Atlantic (WNA) using vertebral centra from 173 females and 135 males ranging in size from 56 to 264 cm FL.Assuming that vertebral band pairs were deposited annually, we estimated ages up to 22 years (228 cm FL) for malesand 24 years (244 cm FL) for females. The growth of both sexes was similar until approximately age 8 (185 cmFL), after which male growth slowed. The growth of females slowed at a later age (∼age 12) than that of males.Relative goodness of fit for all candidate models supported the separate modeling of sexes. For males, von Bertalanffygrowth parameters generated from the vertebral data using a set size at birth (81 cm FL) provided the best fit forthe band counts (asymptotic length [L∞] = 225.4 cm FL; growth coefficient [k] = 0.17). For females, the standardthree-parameter von Bertalanffy growth model provided the best fit to the band counts (L∞ = 274.5 cm FL; k =0.09; theoretical age at a length of zero [t0] = −4.82). These are the first growth parameters generated for CommonThresher Sharks in the WNA and can be used to make informed decisions for the management of this species.

The Common Thresher Shark Alopias vulpinus (familyAlopiidae) is a large pelagic species that occurs in temperateand subtropical seas worldwide. In the North Atlantic, Com-mon Thresher Sharks are known to occur from Newfoundland,Canada, to Cuba in the west and from Norway and the BritishIsles to the African coast in the east (Compagno 2001; Castro2011). Off the northeastern USA, they are considered commonin offshore and cold inshore waters during the summer months(Compagno 2001; Castro 2011), and since they are often large,they are frequently contenders in shark fishing tournaments (Na-tional Marine Fisheries Service [NMFS], Apex Predators Inves-tigation, Narragansett, Rhode Island, unpublished data).

Currently, there is no commercial fishery for CommonThresher Sharks on the East Coast of the USA, but they are takenas bycatch on pelagic longlines and in gill nets. Commercial by-catch landings averaged 19,958 kg (44,000 lb; dressed weight)from 2003 to 2011, with landings peaking at 27,801 kg (61,290lb; dressed weight) in 2010 (NMFS 2012). Common ThresherSharks are also highly sought after by recreational sport

*Corresponding author: [email protected] August 22, 2012; accepted June 4, 2013

fishermen throughout the species’ East Coast range, and thosethat are caught are generally landed; the Common ThresherShark is considered one of the better species for human con-sumption (Compagno 2001). Traditionally, the species has beenof low importance at shark tournaments in the northeastern USAin terms of numbers and percentage of the overall catch, but ithas recently become important in both respects. For example,at one major tournament, Common Thresher Shark numbers in-creased steadily from 0.1% to 4.8% of the total catch from 1965to 1995 and jumped to 27.8% of the total catch in 2004 (NMFS,Apex Predators Investigation, unpublished data).

The Common Thresher Shark is the largest of the threealopiid species, yet little is known about this species’ lifehistory throughout its global range (Compagno 2001). Caillietet al. (1983) generated a growth curve for the eastern NorthPacific population and suggested that males and females reacha maximum TL of 650 cm (356 cm FL [FL calculated usingthe equations presented in this paper]) and a maximum age of50 years, with an age at first maturity of between 3 and 8 years.

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1536 GERVELIS AND NATANSON

Cailliet et al. (1983) acknowledged the lack of older, largerindividuals in their study and could only hypothesize the max-imum size and age for the species. Smith et al. (2008) revisedthe growth curve from Cailliet et al. (1983) by incorporatingdata from 175 additional individuals; those authors estimateda maximum TL of 465 cm (256 cm FL [FL calculated usingthe equations presented in this paper]) and a maximum age of25 years. Age at first maturity was approximately 5 years forboth sexes (Smith et al. 2008). Although the Smith et al. (2008)study improved upon previous age estimates and refined ageat maturity for the Common Thresher Shark, it also lacked datafrom larger size-classes. Information on Common ThresherShark reproduction is limited to a single study of the westernNorth Atlantic (WNA) population (Natanson and Gervelis2013, this issue), with estimated lengths at 50% maturity of216 cm FL for females and 188 cm FL for males.

The Common Thresher Shark is currently listed as vulnera-ble on the International Union for the Conservation of Nature’sRed List of Threatened Species, with population declines re-ported globally based on a combination of slow life historycharacteristics that lead to a decreased capacity to recover fromexploitation (Goldman et al. 2009). Accurate age estimates arecrucial for the proper assessment and management of the Com-mon Thresher Shark because they form the basis for growth andmortality rates, estimates of longevity, age at recruitment, andage at maturity (Goldman et al. 2012). Prior to this study, suchdata for Common Thresher Sharks in the WNA were unavail-able. The objective of the present study was to estimate the ageand growth of WNA Common Thresher Sharks, thus providinga basis for management and assessment.

METHODSSampling and processing.—Common Thresher Sharks were

sampled by NMFS personnel between 1965 and 2004. Speci-mens were obtained aboard research, commercial, and recre-ational fishing vessels and at sportfishing tournaments, pri-marily between Cape Fear, North Carolina, and the Gulfof Maine (northeastern coast of the USA). Multiple verte-brae were removed from the area just above the branchialchamber whenever possible. On two occasions, only vertebraefrom above the cloacal region were available. Entire vertebralcolumns were obtained from six fish. Vertebrae were eitherstored frozen or preserved in a 70% solution of ethanol untilprocessing.

Morphometric data were taken on each sample, includingFL (from the tip of the snout to the fork in the tail, over thebody), TL (from the tip of the snout to a point on the horizontalaxis intersecting a perpendicular line extending downward fromthe tip of the upper caudal lobe to form a right angle, over thebody; Kohler et al. 1995), and total weight (WT). All lengthsare reported as FLs unless otherwise noted, and lengths wererecorded in centimeters; WT was generally measured in poundsand then converted to kilograms. Relationships between TL

and FL and between WT and FL were calculated to enablecomparison with previous studies.

One vertebra from each sample was removed and processedby the methods of Natanson et al. (2002). Each centrum was cutthrough the center along the sagittal plane by using a RaytechGem Saw with two diamond blades separated by a 0.6-mmspacer. Resulting sections were stored in individual tissue cap-sules in 70% ethanol. Each section was digitally photographedwith an MTI CCD 72 video camera attached to an SZX9 Olym-pus stereo microscope using reflected light. Magnification var-ied with the size of the section. Band pairs (consisting of oneopaque band and one translucent band; Cailliet et al. 1983)were counted and measured from the images (Figure 1) by us-ing ImagePro 4 (Media Cybernetics, Silver Spring, Maryland).Measurements were made from the focus of the centrum sectionto the opaque growth bands at points along the internal edge ofthe corpus calcareum by using the caliper function in Image Pro.The first band distal to the focus was used as the initial definitionof the birth band (BB). This mark coincided with a slight anglechange in the corpus calcareum. The BB measurements werethen compared with vertebral measurements of late-term em-bryos and young-of-the-year (age-0) fish to verify the identity ofthe BB. The vertebral radius (VR) was measured from the focusto the distal margin of the intermedialia along the same diago-nal as the band measurements. The relationship between the VRand FL was derived based on observed values to determine thebest method for back-calculation of size-at-age data (Goldman2004; Goldman et al. 2012), allowing us to confirm the inter-pretation of the BB (Natanson et al. 2002). Initial scatterplotsof FL and VR indicated that the data were curvilinear, so theVR data were loge transformed in order to fit a linear regression.Potential differences in vertebral growth between the sexes weretested by using ANCOVA. Significance level α was set at 0.05.

FIGURE 1. Vertebral section from a 17-year-old female Common ThresherShark (FL = 239 cm; weight = 230 kg), showing the approximate locations ofthe focus, birth ring, vertebral bands, and vertebral radius (VR).

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COMMON THRESHER SHARK AGE AND GROWTH 1537

Vertebral column interpretation.—Entire vertebral columnswere examined to determine whether band pair counts differedalong the column. Every tenth vertebra was excised, sectioned,and counted, and the band pair counts were plotted againstvertebra number. Presuming that the counts remained the same,any vertebrae obtained could then be used to determine bandpair counts.

Data analysis.—Two age readers independently counted areference set of 96 vertebral sections to ensure quality con-trol and precision for the band pair counts. So as not to biasthe reader, counts and measurements were made without anyknowledge of the length or sex of each shark. Each reader com-pleted two counts of the subsample. Pairwise inter- and intra-reader comparisons were generated for the reference set as wellas for the two counts of the entire sample, which were madeby the primary reader. Bias and precision of band pair countswere examined by using age–bias plots (Campana et al. 1995).Contingency tables and chi-square tests of symmetry (McNe-mar 1947; Bowker 1948; Hoenig et al. 1995; Evans and Hoenig1998) were used to determine whether observed differences be-tween readers were due to systematic bias or random error. Anycounts that differed by more than one band pair in the subsamplewere counted by both readers simultaneously; an age was as-signed after both readers agreed upon a count. This 96-specimensubsample was then used as a reference set for quality control.Assuming that there was no bias, the primary reader then com-pleted two counts of the entire sample, with the first count of thesample being completed before the second count began. Thiswas done to reduce the possibility of reader familiarity with aparticular vertebra. Before each count, the reader verified ag-ing precision by recounting the subsample for quality control.Band pairs were assumed to be annual, although we did not havevalidation (see Discussion).

Length-at-age estimates based upon band pair counts werefitted to different growth models. We fitted von Bertalanffygrowth functions (VBGFs) to length-at-age data by using theoriginal equation of von Bertalanffy (1938),

Lt = L∞[1 − e−k(t−t0)] ,

where Lt is the predicted length at time t; L∞ is the meanasymptotic FL; k is the growth coefficient (per year); and t0 isthe theoretical age at a length of zero.

Two variations of the VBGF model were used: the customarythree-parameter model as shown above (3-VBGF) and a modi-fied two-parameter model (2-VBGF; von Bertalanffy 1938) thatincorporates a more biologically realistic set size at birth (L0)rather than t0. The L0 was set at 81 cm FL, which was the averagesize of age-0 individuals as estimated during this study.

The Gompertz growth function (GGF) was also fitted, asdescribed by Ricker (1975),

Lt = L0eG[1−e(−kt)],

where G is the instantaneous rate of growth at time t; k deter-mines the rate of decrease in G; and all other parameters aredefined as per the VBGF. Three- and two-parameter versions ofthe GGF model were also calculated using the same size-at-birthvalues as used with the VBGF. A logistic model (modified fromRicker 1979) was also fitted to the data:

Lt = L∞1 + e−g(t−t0)

,

where g is the instantaneous growth coefficient and t0 is theinflection point of the curve.

Parameter estimates for each growth model were obtainedby using nonlinear least-squares regression methods in R (RDevelopment Core Team 2012). Each model’s goodness of fitwas examined using Akaike’s information criterion correctedfor small sample size (AICc; Burnham and Anderson 2002).The AICc difference (�i) of each model i was calculated basedon the lowest observed AICc value (AICc,min) as �i = AICc,i

− AICc,min. Models with �i values less than 2 were deemedto have strong support; models with �i greater than 10 wereconsidered to have little to no support and were eliminated fromfurther analysis (Anderson et al. 2001). To approximate modellikelihood, the Akaike weight (wi) of each model was also cal-culated (Burnham and Anderson 2002). Ninety-five-percent CIswere generated for parameter estimates via bootstrap methodsusing the nlstools package in R (Baty and Delignette-Muller2011). Nested models were constructed to examine differencesbetween sexes in all parameter estimates and were evaluatedbased on AICc values of each model subset. Final model se-lection was based on statistical fit and established biologicalparameters.

Longevity.—The oldest fish aged from the vertebral methodprovides an initial estimate of longevity. However, this valuemay be underestimated in a fished population (Taylor 1958).Longevity estimates for Common Thresher Sharks in the WNAwere based on the time to reach 95% and 99% of L∞ from thebest-fitting growth curve.

RESULTS

Sampling and ProcessingIn total, 308 vertebral samples were collected from Com-

mon Thresher Sharks (173 females; 135 males) ranging in sizefrom 56.3 to 264.4 cm FL (Figure 2). Additional morphometricdata were taken on samples when other biological data wereunavailable, and the data were utilized collectively to establishthe following length and weight conversions:

FL (cm) = 0.5168 × (TL, cm) + 16.466

(n = 173; r2 = 0.84; size range = 150 − 262 cm)

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1538 GERVELIS AND NATANSON

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FIGURE 2. Length frequency for 308 Common Thresher Sharks collected between 1965 and 2004 in the western North Atlantic.

and

WT (kg) = (4.0 × 10−5) · (FL, cm)2.8156

(n = 693; r2 = 0.93; size range = 145 − 263 cm).

Vertebral AgingAnalysis of the six whole vertebral columns showed that

smaller vertebrae at the head and tail were more difficult to ageand that branchial vertebrae provided a better view of growthbands. Counts along the vertebral column never differed by morethan one band pair; therefore, vertebrae from any location alongthe column were suitable for aging. Accordingly, the two verte-bral samples obtained from the cloacal region were included inthe aging sample; only vertebrae from the branchial area wereused for measurement comparisons.

The relationship between FL and VR was best describedusing a curvilinear regression (r2 = 0.90; Figure 3). There wasa significant difference between the intercepts for males andfemales (ANCOVA: P < 0.05); thus, the relationships werecalculated separately. The positive proportional growth betweenthe FL and the centra throughout life shows that vertebrae are

a suitable aging structure for this species (Lagler 1952). Thelinearized forms of the FL–VR regressions can be defined as

FLmale = −152.96 · loge(VR) + 127.99 (r2 = 0.86; n = 129),

and

FLfemale = −176.57 · loge(VR) + 138.84

× (r2 = 0.76; n = 169).

Since the regression did not pass through the origin, the linearmodified Dahl–Lee method with the loge transformed VR wasconsidered the best method for back-calculation (Goldman et al.2012).

The location of the BB was confirmed by comparing the BBwith the VR of near-term embryos and age-0 fish. The BB was6.21 ± 0.41 mm (mean ± SD; n = 297) from the focus of thevertebrae; this translates to a FL of 81 cm at birth. This, alongwith VR measurements from late-term embryos (mean VR ±SD = 5.92 ± 0.61 mm; FL = 67.4 ± 7.4 cm; n = 11) andage-0 fish (VR = 7.59 ± 0.68 mm; FL = 100.3 ± 12.7 cm; n =18), confirmed the correct identification of the BB. No pre-birthmarks were evident in any of the vertebrae.

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COMMON THRESHER SHARK AGE AND GROWTH 1539

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Male embryos

Mean radius of birth mark (n = 308)(6.2 mm)

(n = 135)

(n = 173)

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FL = 136.06Ln(VR) -170.72

R2 = 0.8978

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5202510150

Vertebral Radius (mm)

Female embryos

Average size at birth (81 cm FL)

(n = 4)

FIGURE 3. Plot of FL versus vertebral radius (VR) for 308 Common Thresher Sharks collected between 1965 and 2004 in the western North Atlantic. The meanradius of the birth band (vertical dotted line), the mean size at birth (horizontal dotted line), and the line of best fit (solid curve) are shown.

Data AnalysisAll of the vertebral samples in the reference set were deemed

readable by both readers. Percent agreement (to within twobands or fewer) between the two readers on the reference setwas 86.2%. The age–bias plots on the reference set indicatedthat the primary reader overestimated the ages produced by thesecondary reader on the four largest samples (Figure 4a). Thisdifference in counts (one, two, and five band pairs) on the largerfish was expected given that larger fish tend to be more difficultto read due to compression of the band pairs as the sharksgrow older. Chi-square tests of symmetry gave no indicationthat differences between counts were systematic rather than dueto random error (Bowker [1948] test: χ2 = 37.6, df = 37, P =0.44, n = 96; McNemar [1947] test: χ2 = 3.06, df = 3, P =0.38, n = 96; Evans and Hoenig [1998] test: χ2 = 0.05, df = 1,P = 0.82, n = 96). Within the reference set, those vertebrae that

produced conflicting age estimates were assigned an age afterconsultation between the two readers.

The age–bias plot indicated high agreement and no system-atic bias between the primary reader’s two counts of the entiresample (Figure 4b). Percent agreement (to within two bands orfewer) was 97.4%. Chi-square tests of symmetry gave no indi-cation that differences between the primary reader’s two countswere systematic rather than due to random error (Bowker [1948]test: χ2 = 54.0, df = 40, P = 0.07, n = 304; McNemar [1947]test: χ2 = 5.67, df = 3, P = 0.13, n = 304; Evans and Hoenig[1998] test: χ2 = 1.95, df = 1, P = 0.16, n = 304). Finalband counts were taken from the second read conducted by theprimary reader.

Incorporating separate parameter estimates for each sex im-proved the model fit for all growth curves, as indicated by AICc

values (Table 1); therefore, sex was included as a factor for final

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1540 GERVELIS AND NATANSON

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FIGURE 4. Age–bias plots of pairwise age comparisons between the primary and secondary readers (upper panel) and between the first and second counts madeby the primary reader (lower panel) based on examination of Common Thresher Shark vertebrae. The mean coefficient of variation (CV), the 95% CI about themean count, the 1:1 equivalence line, and the sample sizes at each age are shown.

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COMMON THRESHER SHARK AGE AND GROWTH 1541

TABLE 1. Relative goodness of fit (based on Akaike’s information criterioncorrected for small-sample bias [AICc]) of candidate growth models for Com-mon Thresher Shark specimens from the western North Atlantic (2-VBGF =two-parameter von Bertalanffy growth function; 3-VBGF = three-parameterVBGF; GGF = Gompertz growth function; and logistic = logistic growth func-tion). Models with common parameter estimates for both sexes or with separateparameter estimates for each sex are ranked from best fitting to worst fitting. Inall cases, the use of separate parameter estimates improved the model fit.

AICc

Model Sexes combined Sexes separate

3-VBGF 2,403.58 2,374.80GGF 2,409.94 2,380.122-VBGF 2,410.56 2,380.25Logistic 2,418.10 2,386.84

growth curve analyses. For females, the 3-VBGF was stronglysupported (�i < 2); values of wi did not indicate substantial evi-dence for a single model (wi < 0.90 for all growth curves). The 2-VBGF and 3-VBGF models were strongly supported for the datadescribing males (�i < 2); again, the wi values did not indicatesubstantial evidence for a single model (wi < 0.90 for all growthcurves). Based on both statistical fit and the resulting realisticbiological parameters, the 3-VBGF was considered the bestdescription of growth for females, while the 2-VBGF was con-sidered the best description of growth for males (Tables 2, 3).

TABLE 2. Relative goodness of fit for each candidate growth model for fe-male and male Common Thresher Sharks from the western North Atlantic(models are defined in Table 1). All four models incorporated separate param-eter estimates for each sex. Models are ranked from best fitting to worst fitting(parameters = total number of regression parameters; LL = log-likelihood;AICc = Akaike’s information criterion corrected for small-sample bias; �i =Akaike difference; wi = Akaike weight).

Model Parameters LL AICc �i wi

Females3-VBGF 4 −664.67 1,337.59 0.00 0.78GGF 4 −666.33 1,340.90 3.31 0.152-VBGF 3 −668.48 1,343.11 5.52 0.05Logistic 4 −668.37 1,344.98 7.39 0.02

Males2-VBGF 3 −516.51 1,039.22 0.00 0.413-VBGF 4 −515.46 1,039.24 0.02 0.41GGF 4 −516.47 1,041.26 2.05 0.15Logistic 4 −517.80 1,043.92 4.70 0.04

Males and females exhibited similar growth until the onsetof maturity in males (188 cm FL, age 8; Natanson and Gervelis2013), after which the growth of males slowed (Figure 5).Female growth then slowed at a later age corresponding to theonset of maturity (216 cm FL, age 12; Natanson and Gervelis

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FIGURE 5. Von Bertalanffy growth curves for male (two-parameter von Bertalanffy growth function [VBGF]) and female (three-parameter VBGF) CommonThresher Sharks in the western North Atlantic, plotted with the observed (obs.) length-at-age data. Maturity information is from Natanson and Gervelis (2013).

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1542 GERVELIS AND NATANSON

2013). Overall, females grew at a slower rate than males, yetthey obtained a larger maximum size and greater maximum agethan males.

LongevityThe oldest Common Thresher Sharks based on ages from the

vertebral samples were a 24-year-old female (244 cm FL) anda 22-year-old male (228 cm FL). Using 95% and 99% of L∞from the respective growth models, longevity ranged from 28 to46 years for females and from 15 to 25 years for males.

DISCUSSIONThis is the first comprehensive study of age and growth for

Common Thresher Sharks in the WNA. Initial growth curvesproduced by Cailliet et al. (1983) for the West Coast populationof Common Thresher Sharks lacked older, larger individualsin the sample and thus produced high estimates of asymptoticlength (Figure 6). Smith et al. (2008) added larger individuals tothe samples from the previous study and then remodeled growthfor the species. The growth parameters generated for the WNApopulation differed slightly from those generated for the West

Coast population by Smith et al. (2008; Table 3). Males fromthe current study grew to a similar size (225.4 cm FL) but at aslower rate (k = 0.17) than males in the Pacific (230 cm FL;k = 0.19). Females from the WNA grew to a slightly larger size(274.5 cm FL) and at a slower rate (k = 0.09) than females inthe Pacific (254 cm FL; k = 0.12; Figure 6). Although thesestudies provide the only growth estimates generated for Com-mon Thresher Sharks, results suggest that growth rates of thisspecies may be similar in different regions. The difference ingrowth rate for Common Thresher Sharks in the current studyis reflected in higher ages at maturity (males: 188.4 cm FL,8 years; females: 215.8 cm FL, 12 years) relative to previousworks (Gubanov 1972; Smith et al. 2008).

The extended period (i.e., 40 years) over which vertebralsamples were collected may have introduced some variabilityinto the length-at-age data described in this study. Extendedperiods of overexploitation have been shown to elicit density-dependent changes in life history parameters for many species(Rose et al. 2001). These responses to population reduction arepoorly understood for elasmobranchs (Walker 1998; Gedamkeet al. 2005; Cortes 2007), although several studies have shown

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This study female Cailliet et al. (1983) female Smith et al. (2008) female

FIGURE 6. Growth curves generated for the western North Atlantic Common Thresher Shark population (this study), along with the growth curves from Caillietet al. (1983) and Smith et al. (2008) for the eastern North Pacific population.

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TABLE 3. Growth model parameters for Common Thresher Sharks from the western North Atlantic based on age estimates from vertebral sections. Models aredefined in Table 1 (L∞ = asymptotic FL; k = growth coefficient [VBGF] or rate parameter [GGF]; t0 = theoretical age at a length of zero [VBGF] or inflectionpoint of the curve [logistic growth function]; L0 = length at birth; g = instantaneous growth coefficient; G = instantaneous rate of growth [GGF]). All lengths arepresented as FLs (cm). Bootstrap 95% CIs for each parameter are indicated in parentheses when relevant. An asterisk indicates that the parameter was set prior tomodel fitting. The 95% and 99% longevity estimates (years) are reported for the final growth models. Parameter estimates for Common Thresher Sharks in theNorth Pacific are also provided for comparison. The plus symbol indicates an alternative method for calculating longevity (see the corresponding reference fordetails).

Growth Longevitymodel 95%/99%or reference Sex L∞ L0 k t0 g G (years)

Western North Atlantic population3-VBGF F 274.46

(260.88–294.31)97.75

(86.81–108.30)0.09

(0.07–0.11)−4.82

(−6.30–3.74)28.0/45.6

M 227.92(218.49–239.48)

87.21(78.74–96.30)

0.16(0.13–0.189)

−3.08(−3.90–2.45)

2-VBGF F 263.73(253.63–275.87)

81* 0.11(0.10–0.13)

M 225.40(216.88–236.19)

81* 0.17(0.14–0.20)

15.1/25.0

GGF F 262.80(219.51–316.58)

102.76(92.89–113.02)

0.13(0.11–0.15)

0.94(0.86–1.03)

M 223.16(188.62–264.31)

90.34(82.25–98.21)

0.21(0.18–0.24)

0.90(0.83–0.99)

Logistic F 256.46(247.38–268.05)

107.36(98.00–117.10)

1.96(1.32–2.58)

0.17(0.14–0.20)

M 219.86(213.11–228.85)

92.80(85.52–99.89)

1.21(0.70–1.67)

0.26(0.22–0.30)

Eastern North Pacific populationCailliet et al.

(1983)F 340.35 0.16 −1.02 50+

M 268.19 0.22 −1.42Smith et al.

(2008)F 253.90 0.12 −3.35 25+

M 229.66 0.19 −2.08

varying degrees of density-dependent changes in fished elas-mobranch populations (Sminkey and Musick 1995; Carlsonand Baremore 2003; Cassoff et al. 2007; Taylor and Gallucci2009). The Common Thresher Shark is not a commerciallytargeted species in the WNA (Castro 2011) and has only re-cently become popular with recreational fishermen (Natansonand Gervelis 2013). Given the low exploitation of this species inthe WNA, density-dependent shifts in growth are not expected,and thus the protracted time span of the data collection shouldnot present a problem.

This study would have benefited from the inclusion of addi-tional younger, smaller individuals in the sample. The majorityof fish were collected from sportfishing tournaments, wherelarger individuals that occur offshore are targeted (Natansonand Gervelis 2013). Smaller individuals tend to occur closer in-shore and are occasionally caught as bycatch in the inshore trawland gill-net fisheries along the East Coast (J. Mello, Northeast

Fisheries Observer Program, Woods Hole, Massachusetts, per-sonal communication). The lack of smaller fish in our analysisproduced high estimates of birth size for the growth models usedhere and most likely contributed to improved statistical fit of the2-VBGF for males.

Although there have been numerous age and growth studiesof elasmobranchs, the determination of band pair periodicity re-mains problematic (Goldman et al. 2012). Validation of age esti-mates is a crucial component of any age study, particularly thoseused to inform management decisions (Goldman et al. 2012).Historically, annual band pair periodicity was a major assump-tion of age and growth studies (Cailliet 1990). Annual band pairdeposition has been documented in two pelagic shark species inthe WNA by using bomb radiocarbon-analyzed, oxytetracycline(OTC)-injected, and known-age (age-0) individuals (Campanaet al. 2002; Natanson et al. 2002; Ardizzone et al. 2006) as wellas in the Tiger Shark Galeocerdo cuvier (Kneebone et al. 2008)

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1544 GERVELIS AND NATANSON

and Great Hammerhead Sphyrna mokarran (Passerotti et al.2010), showing that this is a reasonable assumption. To the con-trary, recent studies have demonstrated that validation may bedifficult or impossible and that band pair deposition may notremain constant throughout life in some species (Kalish andJohnston 2001; Kerr et al. 2006; Francis et al. 2007; Andrewset al. 2011). Age and growth studies of alopiid sharks have beenlimited to a few studies conducted in the Pacific Ocean (Cail-liet et al. 1983; Liu et al. 1998, 1999; Smith et al. 2008) andone in the eastern North Atlantic (Fernandez-Carvalho et al.2011). These studies also assumed annual band pair periodic-ity. Because we were unable to capture a suitable number ofindividuals for an OTC injection tag–recapture study or to ob-tain a suitable number of specimens with the appropriate sizeand age for bomb radiocarbon analysis, we could not determineband pair deposition frequency for Common Thresher Sharksand we therefore assumed that it was annual. Despite the lackof validation, these data represent the only age estimates forCommon Thresher Sharks in the WNA, but they should be usedwith caution pending validation.

Longevity estimates can be calculated using several differ-ent relationships, but there is no evidence that suggests thatone method provides a better estimate than another. The equa-tion developed by Ricker (1979) was used because it is a com-mon method of estimating longevity. Published longevity esti-mates for the Common Thresher Shark vary from 25 to 50 years(Cailliet et al. 1983; Smith et al. 2008). Estimates from our studyare near this range at 15–25 years for males and 28–46 years forfemales. The oldest individuals represent a small proportion ofthe population, which makes the probability of catching themquite low (Hoenig 1983). Compagno (2001) reported that themaximum size for the Common Thresher Shark worldwide wasat least 573 cm TL (312 cm FL [FL calculated using the equa-tions presented in this paper]). The largest Common ThresherShark used in our study was a 264-cm-FL female, which wasthe largest recorded individual from the WNA at the time ofcollection (NMFS, Apex Predators Investigation, unpublisheddata). It is possible that larger, older individuals are present inthe population; therefore, the longevity estimates produced inthis study are deemed reasonable for the region.

The present study provides the first age and growth estimatesfor Common Thresher Sharks in the WNA. Validation is es-sential if these estimates are to inform stock assessments andmanagement decisions for this species. With the increasing pop-ularity of Common Thresher Sharks in the recreational sector,overexploitation of this species could become a concern. Accu-rate life history data are vital for proper management of sustain-ability for the WNA Common Thresher Shark population.

ACKNOWLEDGMENTSThis study would not have been possible without the staff

of the NMFS Apex Predators Program (Narragansett, RhodeIsland), including Nancy Kohler, Pat Turner, Ruth Briggs, Cami

McCandless, Dave McElroy, Jeff Kneebone, Bryan DeAngelis,and Karen Tougas. We also thank Greg Skomal, John Carlson,Chris Jensen, and Steve McCandless for collecting samples.We are indebted to the thousands of tournament fishermen whovoluntarily provided samples from shark tournaments and whotagged and returned sharks for the NMFS Cooperative SharkTagging Program. This study was partially funded by a grantfrom the Lerner–Gray Foundation. Reference to trade namesdoes not imply endorsement by the National Marine FisheriesService.

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