Please citegrowth ba
ARTICLE IN PRESSG ModelFISH-3621; No. of Pages 13Fisheries Research xxx (2013) xxx xxx
Contents lists available at SciVerse ScienceDirect
jo u r n al homep age: www.elsev ier .com
Age an triHow re cto
Charlie H ,Kate A. La School of Biolb Threatened, P ment c School of Biomd Graduate School of the Environment, Macquarie University, Sydney, New South Wales, Australia
a r t i c l e i n f o
Article history:Received 10 DReceived in reAccepted 23 M
Keywords:ValidationOrectolobusFisheriesVertebral ageiGrowth rate
a b s t r a c t
The determination of age for large, harvested species such as chondrichthyans is important to the estima-
The detechondrichthand other keat-maturityand age de(Cailliet andstock asses
0165-7836/$ http://dx.doi.o this article in press as: Huveneers, C., et al., Age and growth determination of three sympatric wobbegong sharks: How reliable isnd periodicity in Orectolobidae? Fish. Res. (2013), http://dx.doi.org/10.1016/j.shres.2013.03.014
ecember 2012vised form 20 March 2013arch 2013
tion of growth and other key life history parameters such as natural mortality, age-at-maturity, longevity,and recruitment. Vertebrae from 760 wobbegongs (275 Orectolobus ornatus, 232 O. maculatus, and 253O. halei) were collected between June 2003 and December 2007 at seven locations in eastern Australia(Queensland and New South Wales) to estimate growth parameters for these species. A multi-modelinference (MMI) information theoretical approach including four candidate models, with back-calculatedestimates of length in earlier life stages to account for limited numbers of pup and juvenile wobbegongs,was used to determine the most appropriate growth model for each species. The models that combinedobserved and back-calculated lengths-at-age did not provide a better t than the model using observedlengths-at-age data only. Taking into account biologically meaningful estimations of L and k, the mod-els with the best t to the data were the logistic growth function for O. ornatus and O. halei, and thevon Bertalanffy growth model for O. maculatus. Using these models, growth parameters obtained were:999, 1630 and 2128 mm total length for L and 0.19, 0.09 and 0.20 for k, while the maximum numberof growth bands was 20, 22, and 27, for O. ornatus, O. maculatus, and O. halei, respectively. All threespecies were monomorphic, with similar growth rates for males and females. Verication and validationundertaken using edge and marginal increment analyses, as well as chemical marking of captive andwild wobbegongs, suggested that growth band deposition in orectolobids is more likely to be linked tosomatic growth than seasonality. This study is the rst to use chemically marked wild Orectolobiformesto investigate growth band deposition rate. Five orectolobid species have now been shown not to depositgrowth bands following a synchronous annual pattern, in contrast to that inferred for most other chon-drichthyan species. The growth parameters estimated in this study are crucial for stock assessments andfor demographic analyses to assess the sustainability of commercial harvests.
2013 Elsevier B.V. All rights reserved.
rmination of age for large, harvested species such asyans, is essential to the accurate estimation of growthy life history parameters such as natural mortality, age-, longevity, and recruitment (Pauly, 1987). Growth ratestermination are key components of sheries research
Goldman, 2004), and are required for most sheriessments based on age-structured population models
ding author at: School of Biological Sciences, Flinders University,h Australia, Australia. Tel.: +61 8 8207 5302; fax: +61 8 8207 5481.ress: firstname.lastname@example.org (C. Huveneers).
(Pauly, 1987). Recent increases in chondrichthyan exploitationaround the world (Bonl, 1994; Field et al., 2009; Lack and Sant,2006; Stevens et al., 2000) have highlighted the need for life historystudies and especially those focusing on age and growth. Crucially,inaccurate age determination can lead to major errors in stockassessment and poor estimation of resilience to shing pressure,leading to overexploitation (Campana, 2001; Hoenig and Gruber,1990; Hoff and Musick, 1990; Musick, 1999; Ofcer et al., 1996).
Wobbegongs (family: Orectolobidae) are demersal sharks,found in temperate and tropical Western Pacic waters(Compagno, 2001; Last and Stevens, 2009). Twelve species ofwobbegong shark have been identied worldwide, albeit taxo-nomic uncertainties remain. Ten of these species are found inAustralian coastal waters, with three occurring in New South
see front matter 2013 Elsevier B.V. All rights reserved.rg/10.1016/j.shres.2013.03.014d growth determination of three sympaliable is growth band periodicity in Ore
uveneersa,b,, Joanna Steadc, Michael B. Bennettc
eed, Robert G. Harcourtd
ogical Sciences, Flinders University, Adelaide, South Australia, Australiarotected, and Endangered Species Subprogram, South Australian Research and Developedical Sciences, University of Queensland, Brisbane, Queensland, Australia/ locate / f i shres
c wobbegong sharks:lobidae?
Institute, Adelaide, South Australia, Australia
Please cite nation of three sympatric wobbegong sharks: How reliable isgrowth ba 1016/j.shres.2013.03.014
ARTICLE IN PRESSG ModelFISH-3621; No. of Pages 132 C. Huveneers et al. / Fisheries Research xxx (2013) xxx xxx
Wales (NSW): Orectolobus ornatus, O. maculatus, and O. halei, andan additional two in Queensland (Qld) Eucrossorhinus dasypogonand O. wardi (Corrigan et al., 2008; Huveneers, 2006; Last et al.,2010; Last and Stevens, 2009). In NSW, wobbegongs have beencommerciasince 1991the catch representinGrinberg, 1stable at arannual catccatch resullimits the mshers to siseem to hamented, thremains in nominationas a threatBiodiversityof wobbegomanagemewhich accurequired.
Concenttebral cent(Ridewood,to report grestimates fO. ornatus)(Chidlow, 2attempted vthe periodinot supporrates matchassumed foof band depjaponicus) sspring, but of the verteboth of theband formadation in w
In the pspecies of wto length-atGrowth parand three bent growthof growth bses, physicaof captive a
Vertebrahalei caughtnets while the period JNSW (MoreTerrigal, Sy
One to fo(vertebral n
ap ofere co
r to ecaued t
esencas mis, 20
with. 10 mi (cae it facerae w
or leC freero
growechnthodchniqd fornd thca, 19sed d waParsimproved the clarity of growth bands. Thus, vertebrae were
prepared as follows.r to embedding in clear polyester casting resin cleanedrae were oven dried at 55 C. A thin layer of resin was pouredsilicon mould and left to partially cure for ca. 3060 min. Anual centrum was subsequently placed on the tacky surfacether resin was then poured into the mould until the centrummpletely covered. Blocks were left at room temperature for1 h and were then placed in an oven at 55 C until poly-tion of the resin was complete. Sagittal sections were madedicular to the greatest centrum diameter, using a Gemmastay saw tted with a diamond-impregnated blade. Up to ves of ca. 350 m thick were taken, ensuring that the focus
centrum was included. The two best sections were rinsed inand cleaned with alcohol prior to mounting onto a glass slide, this article in press as: Huveneers, C., et al., Age and growth determind periodicity in Orectolobidae? Fish. Res. (2013), http://dx.doi.org/10.
lly targeted within the Ocean Trap and Line Fishery, to be sold as ake. From 1990/1991 to 2000/2001,reduced from 150 tonnes to 65 tonnes per year,g a decrease of more than 50% in a decade (Pease and995; NSW DPI, 2006). Since then, catches remainedound 60 tonnes per year until 2008/2009, when theh fell to 20 tonnes per year. This latter reduction ofted from shing legislation introduced in 2007 thataximum bag number of wobbegongs for commercial
x per day (Rowling et al., 2010). Although the catchesve stabilized since the new regulations were imple-e ability of wobbegongs to withstand shing pressurequestion. This uncertainty is exemplied by the recent
of the spotted wobbegong (O. maculatus) for listingened species under the Environment Protection and
Conservation Act 1999 (the EPBC Act). An assessmentng resilience to shing pressure is necessary to informnt decisions such as the proposed EPBC listing, forrate determination of age and growth parameters is
ric growth bands have been documented in the ver-ra of most chondrichthyans for nearly a century
1921), and are often used for ageing. The only studyowth parameters for Australian wobbegongs providedor Orectolobus hutchinsi and O. halei (misidentied as
collected from waters off Perth, Western Australia003; Chidlow et al., 2007). Chidlow et al. (2007)alidation using captive wobbegongs, and reported that
city of vertebral band formation in captive animals didt a synchronous annual pattern. Yet, captive growthed those predicted when an annual band pattern wasr wild caught individuals. Similarly, the periodicityosition in captive Japanese wobbegongs (Orectolobushowed that a growth band usually formed annually inthat the formation time sometimes varied with growthbral centrum rather than with time (Tanaka, 1990). Inse studies, validation of the periodicity of the growthtion was undertaken on captive sharks only and vali-ild sharks remains un-assessed.resent study, growth parameters of three sympatricobbegongs were estimated by tting growth models-age data obtained using thin cut sections of vertebrae.ameters are compared using observed lengths-at-ageack-calculated equations, and applied to four differ-
models. Validation and verication of the periodicityand deposition was also attempted using edge analy-l measurement of captive sharks, and chemical markingnd wild specimens.
ls and methods
ion of samples
e were collected from O. ornatus, O. maculatus, and O. by hook and line shing vessels, or captured using handscuba diving or free diving. Sharks were collected overune 2003December 2007, at seven locations in Qld andton Bay, Nambucca Heads, Port Stephens, Newcastle,dney and Eden) (Fig. 1).ur vertebrae were taken from the post-cranium regionumbers 14) of each specimen. Removal of vertebrae
Fig. 1. Mbidae) w
anteriodone bidentithe pr(TL) w(Francbefore
Verual cenhypochvariedtus (caO. halebecausing surVerteb30 mina 20
Numity of each tthe meeral temethobrae aLaMarwere umetho1997; pencil instead
Priovertebinto a individand furwas coabout merizaperpenlapidarsectionof the water (a) Australia and (b) locations where wobbegongs (family: Orectolo-llected.
the rst dorsal n (i.e. the largest vertebrae) was notse it lowers the carcass market value. Each shark waso species (Huveneers, 2006) and sex was determined bye of claspers in males. Before dissection, total lengtheasured using straight-line stretched measurements06) to the nearest 1 mm. Vertebrae were stored on iceg placed in a freezer at 20 C until further analysis.
e were thawed, excess tissue was removed, and individ-eparated using a knife before immersion in 5% sodiume solution to remove any remaining esh. Soaking time
vertebral size and ranged from 30 min for adult O. orna-m in diameter) to two immersions of 1 h each for adult. 25 mm in diameter). Excessive soaking was avoidedtends to dissolve the centra and makes the articulat-s brittle and crumbly (Francis and Maolagin, 2000).ere then placed in fresh running tap water for at leastft soaking overnight. Cleaned vertebrae were stored inezer until sectioned for age determination.us techniques have been used to enhance the visibil-th bands in chondrichthyan vertebrae. The success ofique is species-dependent and slight modications of
can enhance results (Goldman, 2005). Therefore, sev-ues were tested on wobbegong vertebrae to identify a
elucidating the clearest growth bands on whole verte-in cut sections. Alizarin red (Gruber and Stout, 1983;66) and crystal violet (Johnson, 1979; Schwartz, 1983)to stain whole and sectioned vertebrae, and a pencils also tested on whole vertebrae (Carlson and Parsons,ons, 1983, 1985). Neither staining nor the use of the
Please cite natiogrowth ba 1016
ARTICLE IN PRESSG ModelFISH-3621; No. of Pages 13C. Huveneers et al. / Fisheries Research xxx (2013) xxx xxx 3
with a cover-slip placed over the section to avoid damage duringhandling and storage.
2.3. Reading of growth bands
Thin sec(Olympus S(DFW-X700Cupertino, CSoftware, Ltransmittedcent band.
Growth readers on out knowlenotches alocounts by pThe angle cbetween faand Ebert, 1as growth bdened as a
Each pro16 based oment of thewith readabanalysis. Anmore than trienced reawas assigneestimates thestimates w2011). If therandomly a
The radicareum alonthe Optimaet al., 2006)TL and teste
Count rreader variaage percenet al., 1995)Chang, 1982of band cou
Twenty-lected, werepost-craniabrae were cvertebrae, lcounts frompre-caudal throughout
A multcal approagrowth moKatsanevak
2009). An a priori set of four candidate models were tted to thelength-at-age data. The candidate set consisted of: the traditionalthree-parameter von Bertalanffy growth model (VBGM vonBertalanffy, 1938); a two-parameter modied form of the VBGF
through the length-at-birth (L0) (2P VBGM Fabens, 1965),2P VBGM, L0 was estimated using the largest near-termo in Huveneers et al. (2011); the two-parameter Gompertz
to talculthreeas des-at--calo the
comk-caldologis, 19ds w
biol dats m
d (Fd (Fon weses
del s regusinsampIC +
imateize, S/n odelrisonted f eacIC = A
is td suerablo sung thculat
R is termwas and f
eral m of ges, grive a this article in press as: Huveneers, C., et al., Age and growth determind periodicity in Orectolobidae? Fish. Res. (2013), http://dx.doi.org/10.
tions were viewed under a dissecting microscopeZH) with a 0.75 lens connected to a Sony camera). Images were visualized on an iMac computer (Apple,A, USA) using the BTVPro software Version 5.4.1 (Ben
ondon, England). Thin sections were illuminated with light. A growth band was dened as a narrow, translu-
bands of each section were counted, by two differenttwo occasions, after being chosen at random and with-dge of the size or sex of the specimen. When present,ng the outside edge of the corpus calcareum helpedroviding an additional ageing feature (Goldman, 2005).hange on the centrum face, a result of the differencest intra-uterine and slower post-natal growth (Walter991), was considered as the birth mark and assignedand 0. Any band observed before this birth mark was
pre-birth mark (Allen and Wintner, 2002).cessed vertebra was assigned a readabil...