15
This article was downloaded by: [Michigan State University] On: 27 November 2013, At: 09:11 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 New Zealand Journal of Marine and Freshwater Research Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/tnzm20 Age and growth of New Zealand school shark, Galeorhinus galeus Malcolm P. Francis a & Kevin P. Mulligan b a National Institute of Water & Atmospheric Research Ltd , P.O. Box 14 901, Wellington, New Zealand E-mail: b National Institute of Water & Atmospheric Research Ltd , P.O. Box 14 901, Wellington, New Zealand Published online: 29 Mar 2010. To cite this article: Malcolm P. Francis & Kevin P. Mulligan (1998) Age and growth of New Zealand school shark, Galeorhinus galeus , New Zealand Journal of Marine and Freshwater Research, 32:3, 427-440 To link to this article: http://dx.doi.org/10.1080/00288330.1998.9516835 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 New Zealand school shark,               Galeorhinus galeus

This article was downloaded by: [Michigan State University]On: 27 November 2013, At: 09:11Publisher: Taylor & FrancisInforma Ltd Registered in England and Wales Registered Number: 1072954 Registeredoffice: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK

New Zealand Journal of Marine andFreshwater ResearchPublication details, including instructions for authors andsubscription information:http://www.tandfonline.com/loi/tnzm20

Age and growth of New Zealand schoolshark, Galeorhinus galeusMalcolm P. Francis a & Kevin P. Mulligan ba National Institute of Water & Atmospheric Research Ltd , P.O.Box 14 901, Wellington, New Zealand E-mail:b National Institute of Water & Atmospheric Research Ltd , P.O.Box 14 901, Wellington, New ZealandPublished online: 29 Mar 2010.

To cite this article: Malcolm P. Francis & Kevin P. Mulligan (1998) Age and growth of New Zealandschool shark, Galeorhinus galeus , New Zealand Journal of Marine and Freshwater Research, 32:3,427-440

To link to this article: http://dx.doi.org/10.1080/00288330.1998.9516835

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 tothe accuracy, completeness, or suitability for any purpose of the Content. Any opinionsand 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 Contentshould not be relied upon and should be independently verified with primary sourcesof information. Taylor and Francis shall not be liable for any losses, actions, claims,proceedings, demands, costs, expenses, damages, and other liabilities whatsoeveror howsoever caused arising directly or indirectly in connection with, in relation to orarising out of the use of the Content.

This article may be used for research, teaching, and private study purposes. Anysubstantial 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

Page 2: Age and growth of New Zealand school shark,               Galeorhinus galeus

New Zealand Journal of Marine and Freshwater Research, 1998, Vol. 32: 427-4400028-8330/98/3203-0427 $7.00 © The Royal Society of New Zealand 1998

427

Age and growth of New Zealand school shark,Galeorhinus galeus

MALCOLM P. FRANCISKEVIN P. MULLIGAN

National Institute of Water & AtmosphericResearch Ltd

P.O. Box 14 901Wellington, New Zealandemail: [email protected]

Abstract School shark, Galeorhinus galeus (fam-ily Triakidae), are fished commercially throughoutNew Zealand, and estimates of their growth rate, ageat maturity, and longevity are required for fisherymanagement. We aged school shark from X-rays ofthin vertebral sections, but many sections were un-clear and ageing precision was low. Nevertheless,there was no between-reader bias, and growth curvesderived from length-at-age data appear robust. Agrowth curve was derived independently fromlength-frequency data for juvenile school shark upto 9 years old and 120 cm long, and it agreed wellwith the curve derived from length-at-age data. Forolder sharks, the growth rate is not certain becauseof small sample sizes and lack of validation of theages. Growth rate estimates from tag-recapture datasuggested faster growth for small sharks and slowergrowth for large sharks. Based on length-at-age data,males and females grew at about the same rates.Males matured at about 12-17 years and females atabout 13-15 years. The oldest shark in our sampleswas estimated to be 25 years old, but few large sharkswere available for ageing so the longevity of NewZealand school shark remains uncertain.

Keywords age; growth; Galeorhinus galeus;school shark; tagging; length-frequency; GROTAG;MULTIFAN

M97068Received 17 December 1997; accepted 16 March 1998

INTRODUCTION

School shark, Galeorhinus galeus (Linnaeus, 1758)(family Triakidae), are small sharks that inhabit tem-perate and subtropical waters of the Southern Hemi-sphere, and the eastern North Pacific and easternNorth Atlantic Oceans (Compagno 1988). Schoolshark are fished commercially throughout New Zea-land. Commercial landings peaked at 4 800 t in1983-84, but since the introduction of a QuotaManagement System in 1986, they have been re-stricted by Total Allowable Catches to less than3 400 t per year (Annala & Sullivan 1997). Targetlongline and set net fisheries for school shark areseasonally important for small inshore fishing ves-sels in many parts of New Zealand. Annual recrea-tional landings of school shark (estimated from diarysurveys) were less than 2001 in 1991-94 (Annala &Sullivan 1997).

Estimates of school shark growth rate, age atmaturity, and longevity are required in New Zealandfor stock assessment purposes. School shark havebeen aged from vertebral band counts in Brazil(Ferreira & Vooren 1991) and Australia (Moultonet al. 1992). Those two studies used different meth-ods for revealing the vertebral bands (X-rays of sec-tions, and alizarin staining of whole centra,respectively), and they obtained significantly differ-ent results. Ferreira & Vooren (1991) found Brazil-ian school shark to be slow growing and to reach amaximum age of 40 years, whereas Moulton et al.(1992) reported a faster growth rate, and a maximumage of 20 years in Australia. Tagging studies haveshown that Australian school shark live to at least35 years, and probably in excess of 45 years(Moulton et al. 1989). However, using the alizarinmethod on whole centra, Moulton et al. (1992) foundonly 14 bands in the vertebrae of a tagged schoolshark that had been at liberty for over 35 years. Theyacknowledged that their ageing technique seriouslyunderestimated the ages of school shark overc. 130 cm long because of poor resolution of bandscrowded together at the centrum margin. It thereforeappears that the Brazilian X-ray technique may

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428 New Zealand Journal of Marine and Freshwater Research, 1998, Vol. 32

provide more realistic age estimates than the Aus-tralian alizarin technique, though definitive valida-tion is not yet available.

In this study we aged New Zealand school sharkfrom X-rays of thin vertebral sections. We also ob-tained independent growth rate estimates fromlength-frequency and tag-recapture data for compari-son with growth rate estimates derived from length-at-age data.

METHODS

Vertebral ageingVertebrae were obtained from c. 700 school sharkcollected during research trawl surveys throughoutNew Zealand between 1993 and 1995. For eachshark, a block of 3-10 of the largest vertebrae (seeResults) was removed from between the first dorsalfin and the pelvic fins, and frozen. The largest ver-tebrae were used for ageing because it was antici-pated that they would show the greatest band spacingand therefore resolution. This has been confirmed byOfficer et al. (1996) who reported significantlyhigher vertebral counts in the largest (thoracic) ver-tebrae than in the smaller cervical and precaudalvertebrae of both school shark and gummy shark(Mustelus antarcticus).

Vertebral samples were labelled with capture lo-cation, total length (TL, to the centimetre belowactual length), and sex. Subsamples of these verte-brae were selected for processing (Table 1). Most ofthe processed vertebrae came from the west coastSouth Island samples (Fig. 1), which comprised goodnumbers of sharks from a wide size range. Addi-tional vertebrae from large school shark collectedfrom other parts of New Zealand were processed toboost the number of old sharks in the data set (Ta-ble 1, Fig. 1).

In the laboratory, vertebrae were thawed andtrimmed of neural and haemal arches and muscle andconnective tissue. Individual centra were then sepa-rated and immersed in household bleach (42 g litre"1

sodium hypochlorite) until all of the muscle andconnective tissue had been removed (c. 1 h). Exces-sive soaking tended to dissolve the vertebral centra.After overnight soaking in fresh water, vertebraewere air-dried for 1 week.

Vertebrae were individually glued to woodenblocks with quick setting resin (Araldite), and sec-tioned frontally (in the lateral plane) through themiddle of each centrum with an Accutom saw fittedwith a diamond-coated blade. Section thickness av-eraged 450 ± 100 (im. Sections were rinsed of anypaniculate residues, swabbed, and air dried.

Vertebral sections were mounted on quarteredoverhead transparency sheets (149 x 105 mm) usingstrips of double-sided tape. Usually each quarter-sheet held 18 sections (three rows of six sections).The sheets were X-rayed using a Philips 140 kVberyllium industrial X-ray machine and KodakIndustrex grade "R" film. Best exposures wereachieved at 5 mA and 45 kV for 20-27 s. The filmwas processed with standard developer and fixer for9 min each.

Vertebral bands were classified as major (well-defined, hypermineralised bands), uncertain(hypermineralised bands with irregular spacing), orminor (fine check marks) following Officer et al.(1996). The hypermineralised major bands are radio-opaque, and appear light grey or white in X-rays(Ferreira & Vooren 1991; Officer et al. 1996; Fig.2). The major bands were counted directly from theX-ray film under a binocular microscope by tworeaders (Ri and R2). Major bands correspond withoptically translucent bands when viewed under amicroscope using transmitted light (Ferreira &Vooren 1991). They form in winter in Southern

Table 1 School shark (Galeorhinus galeus) vertebral samples used in the estimation of age and growth. Samplingregions are shown in Fig. 1.

Sampling region

West coast North IslandWest coast South IslandWest coast South IslandEast coast South IslandStewart-Snares ShelfStewart-Snares ShelfTotal

Voyage

KAH9410KAH9404KAH9504KAH9406TAN9301TAN9402

Period

Oct 1994Mar-Apr 1994May-Apr 1995May-Jun 1994Feb-Mar 1993Feb-Mar 1994

Males

27327112

12127

Number of sharksFemales

97220165

15137

Total

111454727

727

264

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Francis & Mulligan—Age and growth of school shark

Fig. 1 Map of New Zealandshowing the school shark(Galeorhinus galeus) vertebralcollection regions described inTable 1.

165°E 165°E 175°

429

180°

35°S

40°-

45'

35°S

40°

45°

165°E 165°E 165°E 175°

Hemisphere school shark (Ferreira & Vooren 1991;Officer 1995).

Both readers carried out an initial training exer-cise by counting a subsample of the sections whileknowing the size and sex of the sharks, and thencompared their results. Subsequent counts were car-ried out "blind"; i.e. the readers did not know the sizeor sex of the sharks. The readability of sections wasscored on a scale from 1 (unreadable) to 5 (excep-tionally clear). Vertebral band counts were assessedfor ageing bias and precision using age-bias plots,and plots of the coefficient of variation (CV) againstage, as recommended by Campana et al. (1995).

Vertebral bands are assumed to form annually(see Discussion) and were used to produce age esti-mates for each shark. The theoretical birthday wasdefined as 1 January, based on birth of young dur-ing spring-summer in New Zealand (pers. obs.). Thesame birthday has been used for school shark in

Australia and Brazil (Ferreira & Vooren 1991;Moulton et al. 1992). School shark, like most sharksspecies that give birth to live young, lay down a"birth band" on their vertebrae soon after birth(Ferreira & Vooren 1991; Moulton et al. 1992; pers.obs.). Moulton et al. (1992) used the following al-gorithm to calculate school shark age from bandcounts:

Age = number of bands - 1 for birth band + 1 if theouter perimeter was stained + proportion of the yearfrom 1 January to capture date.

However, the ages of sharks that are caught duringthe second half of the calendar year, and have there-fore deposited an additional winter band, are over-estimated by one year by that algorithm. Wetherefore revised the algorithm as follows:

For sharks caught after 1 January and before theformation of a winter band:

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430 New Zealand Journal of Marine and Freshwater Research, 1998, Vol. 32

Fig. 2 Photomicrographs (transmitted white light) of X-ray plates of frontal sections of school shark (Galeorhinusgaleus) vertebrae from A, 123 cm male, Stewart-Snares Shelf, readability 5, age = 13.2 years (Reader 1 and Reader2); B (opposite), 114 cm male, west coast South Island, readability 2, age = 8.3 years (Reader 1) and 9.3 years (Reader2). (Scale bar = 1 mm.)

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Francis & Mulligan—Age and growth of school shark 431

Fig. 2 (continued)

Age = number of bands - 1 for birth band + propor-tion of the year from 1 January to capture date (1)For sharks caught after the formation of a winterband and up to 31 December:Age = number of bands - 1 for birth band -1 tocorrect for winter band + proportion of the year from1 January to capture date (2)

All but 11 of our school shark were caught during

the first half of the year (Table 1), before the forma-tion of a winter band, and were aged using algorithm(1). The remaining 11 sharks were caught in Octo-ber and were aged using algorithm (2).

Growth curves were fitted to the length-at-agedata using the Von Bertalanffy growth model:

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432 New Zealand Journal of Marine and Freshwater Research, 1998, Vol. 32

where L, is the expected length at age t years, Lx isthe asymptotic maximum length, K is the VonBertalanffy growth constant, and ?0 is the theoreti-cal age at zero length. No attempt was made to de-termine the statistical significance of differencesbetween growth curves because of the low precisionof individual age estimates.

Length-frequency distributionsSchool shark length-frequency distributions wereobtained from a series of five bottom trawl surveysconducted by the research vessel Kaharoa off thewest coast of South Island between latitudes 40.5 and44° S using a 74 mm mesh cod-end. The surveyswere carried out in March-April between 1990 and1997, and they covered a depth range of 20-400 m.Further details of the surveys were provided byDrummond & Stevenson (1996).

Von Bertalanffy growth curves were fitted to thefive length-frequency distributions using theMULTIFAN model (Fournier et al. 1990). Thismodel simultaneously analyses multiple length-fre-quency distributions using a maximum likelihoodmethod to estimate the proportions of fish in eachage class, and the Von Bertalanffy growth param-eters. The main assumptions of the MULTIFANmodel are: (1) the lengths of the fish in each age classare normally distributed around their mean length;(2) the mean lengths-at-age lie on or near a VonBertalanffy growth curve; and (3) the standard de-viations of the actual lengths about the mean length-at-age are a simple function of the meanlength-at-age (Fournier et al. 1990).

The Von Bertalanffy parameters Lx and K wereestimated by conducting a systematic search acrossa matrix of plausible AT values and age classes. ?Q wasestimated from the equation:

to = h - ax

where tt is the estimated age (in years since the theo-retical birthday), and a\ is the age estimated byMULTIFAN (in years since zero length), of theyoungest age class at the time it first appeared in thelength-frequency samples.

For the identified age classes, MULTIFAN alsoestimates the ratio of the last to first length-stand-ard deviations (5R), and the geometric mean of thefirst and last standard deviations (SA). TheMULTIFAN model was fitted for two differentgrowth hypotheses: (1) constant length standarddeviation for all age classes (fitted by setting 5R = 1and estimating ,SA); a n d (2) variable length standarddeviation across age classes (fitted by estimating

both i*A and SR). Because all five trawl surveys wereconducted at the same time of year, the data containno information on seasonal variability of growth, andno seasonal parameters were fitted.

The constant standard deviation model was fittedto the data first, followed by the addition of the pa-rameter for variable standard deviation. For eachmodel, the maximum log-likelihood (k) was deter-mined. Tests for significant improvement in modelfit were made using likelihood ratio tests. Twice theincrease in X is distributed as a %2 distribution withdegrees of freedom equal to the number of additionalparameters. Following Fournier et al. (1990), a sig-nificance level of 0.10 was used for testing whetherthere was any gain in introducing an additional ageclass in the length-frequency analyses. The test forimprovement resulting from the addition of the pa-rameter for variable standard deviation was carriedout with a significance level of 0.05.

Tag-recapture dataA total of 3,950 school shark were tagged through-out New Zealand between 1985 and 1997. Theywere mainly caught by bottom trawl, and only lively,apparently undamaged, sharks were tagged. Schoolshark were measured (TL) and tagged with loop,dart, or internal tags. Loop tags were inserted throughthe muscle just anterior to the first dorsal fin andclipped or tied together, and dart tags were insertedinto the muscle below the first dorsal fin. Internaltags were inserted into the body cavity, and the tagwound was sutured closed. Each tag was printed witha unique serial number, a return address, and noticeof a reward. Further details of the tagging pro-gramme were given by Hurst et al. (unpubl. data).

Growth rate estimates were obtained from thetagging data using the maximum likelihood methodand computer program GROTAG (Francis 1988).GROTAG estimates ga and gp, the mean annualgrowth offish of lengths a and ft respectively. Thereference lengths a and p were chosen to lie withinthe range of lengths of tagged school shark. Francis(1988) showed that these parameters are betterdescriptors of the growth information in tagging datathan are the more conventional Von Bertalanffygrowth parameters Lx and K. The expected lengthincrement, AL, for a fish of initial length Lx at lib-erty for time AT is given by:

AL =AT

ga-gp

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Francis & Mulligan—Age and growth of school shark 433

I «

5 -

Vertebra number

Fig. 3 Vertebral length measurements from two male(M) and three female (F) school shark (Galeorhinusgaleus) of various total lengths. Vertebrae are numberedfrom anterior (0) to posterior (80).

Also estimated were m and 5 (the mean and stand-ard deviation of the measurement error), v (the co-efficient of variation of growth variability), and p(the proportion of outliers) (Francis 1988). A sea-sonally varying growth function was also tested, anddifferences in growth rate between the two sexeswere investigated.

The approach used was to fit a simple GROTAGmodel with few parameters to the data. The complex-ity of the model was then gradually increased byintroducing additional parameters (for example,parameters to allow seasonal variation in growth).At each stage, new parameter estimates were madeand likelihood ratio tests for significant improvementin model fit were carried out as described above forMULTIFAN models. A significance level of 0.05was used for testing whether there was any gain fromintroducing additional parameters.

RESULTS

Vertebral ageingVertebral length typically increased from behind thechondrocranium to a maximum above the origin ofthe pelvic fins (vertebrae numbers 38-40) (Fig. 3).The same trends occurred in the lateral and dorso-ventral vertebral dimensions. Posterior to the pelvicfin origins, vertebral length declined rapidly, mark-ing the transition from large monospondylous ver-tebrae to small diplospondylous vertebrae.

(0

8,<

LJJCO+1CcoCD

EcoCD>

CDD)

<

• Readability 3-5o Readability 2

10 15 20

Age (RT) (years)

Fig. 4 Comparison of A, actual and B, mean school shark(Galeorhinus galeus) age estimates between Reader 1 (Rj)and Reader 2 (R2). (N= sample size.)

Superimposed on this overall pattern was a "stutterzone" (Springer & Garrick 1964; Compagno 1988)of alternating vertebral lengths around vertebrae42-70 (Fig. 3). Stutter zones were also occasionallyfound in monospondylous vertebrae (Fig. 3). A sur-prising amount of individual variation was observedin vertebral sizes. Occasional school shark displayedsecondary peaks in vertebral size, and maximumvertebral sizes under the first dorsal fin (vertebrae27-32) (Fig. 3). These variations were apparent inall three vertebral dimensions.

In young sharks, the radio-lucent bands werewider than the radio-opaque bands, but the widthdifference declined with increasing age (Fig. 2A). Inthe remainder of this paper, the term "band" refers

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434 New Zealand Journal of Marine and Freshwater Research, 1998, Vol. 32

DC

o

ICO

• I — '

SoO

20

10

0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 '

Age (R^ (years)

Fig. 5 Precision of school shark (Galeorhinus galeus)age estimates made by Reader 2 (R2) relative to the esti-mates made by Reader 1 (R^.

only to the major, narrow radio-opaque bands, whichwere counted to provide age estimates. The third andfourth bands (counted from the centre of the centrum)were often broad and diffuse, and sometimes com-posed of identifiable sub-bands. Bands were clear-est in the intermedialia, but that probably reflectedour particular combination of voltage and exposuretime. In clear centra, bands could also be traced intothe corpus calcareum (Fig. 2A). The banding patternin the corpus calcareum could be enhanced by vary-ing the voltage and exposure time.

Only two vertebral sections were considered un-readable. Of the remaining 264 vertebrae, 80% werescored as poor or moderate (readability 2 or 3; Fig.2B); only 20% were good or exceptionally clear(readability 4 or 5; Fig. 2A).

Age estimates made by R[ and R2 sometimesvaried markedly (Fig. 4A). Some of the larger dif-ferences were for vertebrae that were judged unclear(readability 2) but large differences were also foundfor some of the clearer vertebrae (readability 3-5).Overall, there was no systematic difference in ageestimates between readers (Fig. 4B).

Ageing precision was low, particularly for the 0+-2+ age classes, for which the CV exceeded 30% (Fig.5). The absolute variation for these age classes neverexceeded 1 year for vertebrae with readability scoresgreater than 2 (Fig. 4A). For older sharks the CV ofthe age estimates between readers fluctuated around20%.

The greatest estimated ages (mean of R] and R2)were 23.3,23.7, and 24.8 years, but few sharks weremore than 15 years old (Fig. 6). R] length-at-age dataand fitted R] and R2 Von Bertalanffy growth curvesare shown in Fig. 6A, and Von Bertalanffy growthparameters are given in Table 2. The R] growthcurve differed little from the R2 curve (Fig. 6). Fit-ting of separate growth curves to male and femaledata indicated that there was little difference in thelength-at-age of males and females over the agerange for which adequate samples were available (0-11 years) (Fig. 6B).

The longest male in our data set was 146 cm andthe longest female was 168 cm (with five femaleslonger than 160 cm). The longest reliably measuredschool shark in the New Zealand research trawldatabase were 168 cm and 175 cm males and two168 cm females.

Length-frequency distributionsMost sharks caught during the five west coast SouthIsland trawl surveys were in the length range 35-120 cm TL, and the length-frequency distributionswere polymodal, particularly for sharks less than80 cm long (Fig. 7). All five samples contained re-cently-born 0+ sharks with modal lengths around35-42 cm.

The best fit MULTIFAN model consisted of vari-able length standard deviation (SR = 1.71, SA =3.90 cm) with nine age classes. The parameters ofthe MULTIFAN Von Bertalanffy growth curve aregiven in Table 2. The age of the 0+ sharks at the timethey first appeared in the length-frequency samples(/]) was 0.25 years (the time elapsed between thetheoretical birthday (1 January) and the samplingdate midpoint (1 April)). The estimated age in yearssince zero length of the 0+ age class at the time itfirst appeared in the length-frequency samples (a{)was 2.16 years, producing a t0 estimate of-1.91years.

The MULTIFAN growth curve (Fig. 8) has beentruncated at 9 years (the number of age classes de-tected by MULTIFAN), and should not be extrapo-lated beyond that point because the length-frequencydata represent mostly small, immature school shark.The MULTIFAN growth curve was very similar tothe growth curve based on vertebral ages (Fig. 8).

Tag-recapture dataSeventy-nine recaptured school shark had sufficientinformation (lengths at tagging and recapture, daysat liberty) to be used in the growth analysis. InitialGROTAG model fits identified two sharks as

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Francis & Mulligan—Age and growth of school shark 435

Fig. 6 School shark (Galeo-rhinus galeus) length-at-age data(Reader 1, R,), with fitted VonBertalanffy growth curves for A,all samples and both sexes com-bined (Reader 1 and Reader 2, Rj),and B, all samples and males andfemales separately (R,). See Table2 for Von Bertalanffy parameters.(N= sample size.)

10 15

Age (years)

Table 2 Von Bertalanffy growth curve parameters based on school shark (Caleorhinus galeus)length-at-age and length-frequency data. Standard error estimates for the MULTIFAN parametersare considered unreliable (Francis & Francis 1992) and are not shown. (SE, standard error; R bReader 1; R2, Reader 2; M, male; F, female.)

Vertebralreader Sex

Samplesize (cm) (years"1) (years)

Length-at-age data (vertebrae)R, M + F 264 165.8 ±6.0 0.104 ±0.009 -2.37 ± 0.26R2 M + F 264 180.4 ±6.0 0.086 + 0.006 -2.48 + 0.20R, F 137 179.2 ±9.5 0.086±0.011 -2.68 ±0.38Ri M 127 142.9±6.0 0.154±0.019 -1.64±0.31

Length-frequency data (MULTIFAN)M + F 2344 154.9 0.131 -1.91

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436 New Zealand Journal of Marine and Freshwater Research, 1998, Vol. 32

6

4 -

o _

020 -

10 -

0

& 3 0

0 20-

p 100

20

10

0

15 -

10 -

5 -

0

1990KAH9006A/=156

1992KAH9204N =522

i i

1994KAH9404N = 6491 @ 165 cm not shown

I i

1995KAH9504N =566

1997KAH9701/V=451

20 40 60 80 100

Total length (cm)

120 140 160

Fig. 7 School shark (Galeorhinus galeus) length-frequency distributions (both sexes combined) obtained from fivetrawl surveys off the west coast of South Island in March-April 1990-97. (N = sample size.)

outliers (sharks having absolute standardisedresiduals greater than 3.0). These outliers probablyresulted from measurement errors, and were deletedfrom the data set, leaving 77 sharks.

Most of the school shark were between 60 and150 cm long at tagging, with males being slightlylarger on average than females (Fig. 9). The

GROTAG reference lengths a and P were set at70 cm and 140 cm respectively. Periods at libertyranged from 1 to 3 505 days (0-9.6 years), but mostsharks were at liberty for less than 5 years (Fig. 10).

A simple model, with two growth rate parametersand parameters for growth variability and measure-ment variability (Table 3, Model 1) produced

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Page 12: Age and growth of New Zealand school shark,               Galeorhinus galeus

Francis & Mulligan—Age and growth of school shark 437

NZ, vertebraeNZ, length-frequencyAustraliaBrazil, females

60

Age (years)

Fig. 8 Comparison of growth curves derived from NewZealand length-at-age data (Reader 1, vertebrae), andMULTIFAN analysis of length-frequency data. Alsoshown are growth curves derived for school shark(Galeorhinus galeus) from Brazil (Ferreira & Vooren1991) and Australia (Moulton et al. 1992).

50 60 70 80 90 100 110 120 130 140 150 160

Total length (cm)

Fig. 9 Length-frequency distributions (at tagging) oftagged and recaptured school shark (Galeorhinus galeus)used in the GROTAG analysis of growth rates. (N= sam-ple size.)

estimates of growth rate of 12.46 cm yr 1 at 70 cmand 0.91 cm y r 1 at 140 cm. However the growthvariability parameter (v) was estimated to be zero,indicating that the data contained insufficient

^ 50 -

_o, 40 -

c

CD

<D

30 -

20 -

10 -

0

-10 -

-20

Males (N = 36)Females {N = 41)

1 Q -

0 1000 2000 3000 4000

Days at libertyFig. 10 Relationship between growth increment andperiod at liberty for tagged school shark (Galeorhinusgaleus). ( N = sample size.)

information for GROTAG to distinguish growthvariability from measurement variability.

The addition of parameters for outlier contami-nation, measurement bias, and seasonal growth didnot significantly improve the log-likelihood (Table3, Models 2-4), and nor did subdivision of the databy sex (Table 3). However, sample sizes were small,statistical power was low, and only large seasonalvariation, or large growth differences between thesexes, could have been detected.

The best GROTAG model (Table 3, Model 1) hadno apparent pattern or trend in the residuals.GROTAG was run in simulation mode (Francis1988) using parameter estimates from Model 1 todetermine the accuracy and precision of the growthrate estimate. The mean annual growth rates wereestimated to be 12.61 cmyH at 70 cm, and 0.88 cmyr 1 at 140 cm (Table 4).

DISCUSSION

X-ray images of school shark vertebral sections wereoften unclear and difficult to count, leading to lowcounting precision. Officer et al. (1996) concludedthat experienced school shark vertebral readers pro-duced more precise age estimates than inexperiencedreaders. In our study, the two readers were experi-enced in reading teleost otoliths, but not in readingshark vertebrae. The ability of readers to distinguishmajor bands from uncertain and minor bands (Of-ficer et al. 1996) depends on the clarity of the X-rays,and the contrast and discreteness of the radio-opaquebands. When major bands are difficult to

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Page 13: Age and growth of New Zealand school shark,               Galeorhinus galeus

438 New Zealand Journal of Marine and Freshwater Research, 1998, Vol. 32

discriminate, a reader's experience of their shape andappearance in other sections proves useful. We agreewith Officer et al. (1996) that ageing school sharkfrom their vertebrae involves a learning process, andthat inevitably the interpretation of banding patternswill be somewhat subjective, but should improvewith experience.

School shark vertebral ageing has not yet beenvalidated, although marginal zone analysis doessupport annual deposition of bands (Ferreira &Vooren 1991). Ageing validation studies are cur-rently underway in Australia (R. Officer, Marine andFreshwater Resources Institute, Victoria, Australiapers. comm.), and until they are completed only in-direct means are available for verifying the currentageing techniques. Analysis of length-frequency dataproduced a growth curve and estimated annualgrowth increments that were remarkably close tothose derived from length-at-age data (Fig. 8, Table4) over the age range 0-9 years, providing strongsupport for our interpretation of the major vertebralbands as annual. Length increment data from taggedschool shark suggested more extreme growth ratesthan those estimated from the other two sources (i.e.,faster growth of smaller sharks and slower growthof larger sharks; Table 4).

Lack of precision means that vertebral ageing isunlikely to be useful when accurate school sharkages are required (e.g., in the estimation of year classstrength from an age-frequency distribution), at leastwithout increased reader experience. Nevertheless,the growth curves generated by both readers werenearly identical for sharks up to 15 years old (Fig.6A), suggesting that the length-at-age growth param-eters reported in Table 2 are relatively robust.

In our analyses, we pooled the length-at-age andtag-recapture data from different parts of New Zea-land. Movement of tagged school shark around NewZealand is considerable, and a significant proportionof tagged animals has crossed the Tasman Sea be-tween New Zealand and Australia (Hurst et al.unpubl. data). The degree of mixing around the NewZealand coast suggests that there is unlikely to bemajor regional variation in growth rates, and thatdata pooling is valid. However, young juveniles (0+and 1+) apparently have much lower mobility, andthere is some evidence from length-frequency datathat their growth rates may differ regionally (L. J.Paul, NIWA pers. comm.).

Previous studies have found little difference be-tween the growth rates of male and female schoolshark (Ferreira & Vooren 1991; Moulton et al. 1992),

Table 3 Parameter estimates from GROTAG growth models for school shark (Galeorhinus galeus) (N - 11).Seasonal phase is given in years since 1 January. (M, male; F, female; SD, standard deviation; -, parameter notestimated.)

Parameter

Log likelihoodMean growth rates

Growth variabilitySD measurement errorMeasurement biasOutlier contaminationSeasonal amplitudeSeasonal phase

2Xg?0 (cm yr1

gi4o (cm y rV

s (cm)m (cm)Puw(yr)

1

261.08) 12.461) 0.91

0.007.19

----

Both sexes combined2

261.0812.460.910.007.18

_0.00

--

3

261.0812.470.910.007.180.00

_--

4

261.0712.480.910.067.18

--

0.520.04

Separate sexesM F

261.0312.39 12.480.96 1.010.007.18

----

Table 4 Comparison of school shark (Galeorhinus galeus) annual growthincrements at two reference lengths (70 and 140 cm) based on length-at-age(Rl), length-frequency and tag-recapture data.

Total length Annual growth increment (cm ± standard error)(cm) Length-at-age Length-frequency Tag-recapture

70140

9.362.54

10.53 12.61 ±0.120.88 + 0.05

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Page 14: Age and growth of New Zealand school shark,               Galeorhinus galeus

Francis & Mulligan—Age and growth of school shark 439

and our results support that conclusion. In Australia,the greatest reported lengths were 171 cm and174 cm for males and females respectively (Moultonet al. 1992), and the greatest reliably measured NewZealand school shark were 175 cm (males) and168 cm (females). In most shark species, femalesreach a greater maximum length than males, butschool shark are an exception to this rule.

In New Zealand, most male school shark matureat 125-135 cm and most females mature at 135-140 cm (NIWA unpubl. data). These are similar tothe lengths at maturity reported for Australian schoolshark (Olsen 1984). Based on the length-at-agegrowth curves given in Table 2, age at maturity inNew Zealand is estimated to be 12-17 years formales and 13-15 years for females. However, fewsharks in our samples were over 15 years old, andtherefore the growth curves are not well definedabove that age. More female sharks from around thelength at maturity are required to properly estimatethe age at maturity. For similar reasons, we are un-able to estimate the longevity of school shark fromour data.

The growth curves for New Zealand school sharkderived in the present study fall in between those forAustralian and Brazilian sharks (Fig. 8). There isgood evidence from the estimated ages at recaptureof tagged and released school shark that the Austral-ian technique of alizarin staining whole vertebraeseriously underestimates the ages of school sharkover c. 130 cm (Moulton et al. 1992). It probably alsounderestimates the ages of smaller sharks to a lesserdegree. Conversely, the Brazilian X-ray techniquethat we used provides age estimates that are consist-ent with the long periods at liberty (more than 35years) observed for tagged sharks (Moulton et al.1989; Ferreira & Vooren 1991). We conclude thatNew Zealand school shark grow at rates similar tothose of Australian school shark, and that the differ-ences observed in the growth curves (Fig. 8) areattributable to age underestimation by Moulton et al.(1992). New Zealand school shark appear to growsomewhat faster than Brazilian school shark.

The above conclusions must be treated with somecaution. It is possible that we also underestimatedthe ages of the larger New Zealand school sharkbecause of band crowding near the vertebral margin.Evidence pointing to this possibility includes: (1) thelow maximum age estimate in our study (c. 25 years)despite the inclusion in our samples of a few sharksnear the maximum known length; and (2) the factthat the growth rate estimate for large sharks ob-tained from the tag-recapture data was lower than

that obtained from the length-at-age data (Table 4).If our ageing method did result in an underestima-tion of the ages of older sharks, then our age-basedestimates of growth rates will be too high.

In summary, the growth rate of school shark upto about 120 cm and 9 years of age has been deter-mined from length-at-age, length-frequency and tag-recapture data, which are all in reasonableagreement. For larger sharks, growth rates have beenestimated from length-at-age data, but these are pro-visional because of small sample sizes and lack ofvalidation of the age data. Our estimates of age atmaturity are probably reasonable, but we were un-able to determine the longevity of New Zealandschool shark.

ACKNOWLEDGMENTS

We thank our NIWA colleagues for helping to collectschool shark vertebrae. Stuart Hanchetmade useful com-ments on an earlier draft of this paper. This research wascarried out by NIWA under contract to the New ZealandMinistry of Fisheries (Project P1AG01).

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Drummond, K. L.; Stevenson, M. L. 1996: Inshore trawlsurvey of the west coast South Island and Tasmanand Golden Bays, March-April 1995 (KAH9504).New Zealand fisheries data report 74. 59 p.

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