Age and growth of the whale shark (Rhincodon typus)in the north-western Pacific

Hua Hsun HsuA,B,F, Shoou Jeng JoungA,B,E,F, Robert E. HueterC

and Kwang Ming LiuB,D

ADepartment of Environmental Biology and Fisheries Science,National TaiwanOceanUniversity,

2 Pei-Ning Road, Keelung 20224, Taiwan.BGeorge Chen Shark Research Center, National Taiwan Ocean University, 2 Pei-Ning Road,

Keelung 20224, Taiwan.CCenter for Shark Research, Mote Marine Laboratory, 1600 Ken Thompson Parkway, Sarasota,

FL 34236, USA.DInstitute of Marine Affairs and Resource Management, National Taiwan Ocean University,

2 Pei-Ning Road, Keelung 20224, Taiwan.ECorresponding author. Email: f0010@mail.ntou.edu.twFNote: equal contribution of first author and corresponding author.

Abstract. This study estimated age and growth of the largest extant fish, the whale shark (Rhincodon typus) by counting

vertebral band pairs from 92 specimens comprising 43 males (2.68–9.88m total length [TL]), 30 females (1.60–7.02mTL), and 19 unsexed individuals (2.83–6.67mTL) taken byTaiwanese commercial fisheries during 2001–06.Growth bandpairs up to 25 and 42 were counted for a 6.38-m TL female and a 9.88-m TLmale, respectively. Using marginal increment

ratio and centrum edge analysis, band pairs were postulated to be formed twice a year. The two-parameter von Bertalanffygrowth function provided the best fit without significant differences between sexes. Growth parameters were calculatedfor both sexes as LN¼ 16.80m TL, k¼ 0.037 year�1; annual band pair formation would modify these parameters to

LN¼ 15.34m TL, k¼ 0.021 year�1. Using data reported in another study for 50% size at maturity for males (8.1m TL),and the largest immature and smallest mature females (8.7 and 9.6m TL, respectively) in the Indo-Pacific, these TLsconverted to ages at maturity of 17 years for males and 19–22 years for females. The longevity was calculated to be

80.4 years.

Additional keywords: band pair, Taiwan, vertebra, X-ray.

Received 13 December 2013, accepted 14 April 2014, published online 10 October 2014

Introduction

The whale shark (Rhincodon typus (Smith, 1828)), is the largestextant fish in the world. It can grow to at least 12m total length(TL) and may attain lengths of 17–18m TL or even 21.4m TL

(Compagno 2001; Krishna Pillai 2002; Stevens 2007). Thisspecies typically inhabits the epipelagic layers of tropical andsubtropical waters of the world’s oceans (Compagno 2001),

although extreme dives to at least 1928m have been recorded(Hueter et al. 2013). It is one of three filter-feeding sharks thatconsume a wide variety of planktonic and nektonic prey

(Last and Stevens 1994; Colman 1997; Compagno 2001;Stevens 2007; Motta et al. 2010).

Whale sharks have been harvested for their meat, fins andliver oil by fishermen from many Asian countries including

Taiwan (Chen et al. 1997; Norman 2004; Hsu et al. 2012).Conservation and management of the whale shark have beenaddressed by international conservation groups and bodies

such as IUCN (International Union for Conservation of

Nature) and CITES (Convention on International Trade inEndangered Species of Wild Flora and Fauna), which addedthis species to their conservation lists in 1997 and 2002,respectively (Fowler 2000; Norman 2000; CITES 2002).

Additionally, some countries such as the Maldives, Honduras,Thailand, Australia, Mexico, Belise, United States, SouthAfrica and the Philippines have implemented protection of

the species, including regulation of whale shark ecotourism insome areas (Davis et al. 1997; Chen and Phipps 2002; Norman2004). However, much critical information needed to improve

the management of the whale shark, such as biologicalcharacteristics, ecology and behaviour, and accurate popula-tion sizes, is still unknown.

Until 1995, the annual catch of whale sharks in Taiwanese

waters was reported to bemore than 250 individuals (Chen et al.1997). Management measures for whale shark fishing wereimplemented by the Taiwanese Fisheries Agency in 2001, based

on a consensus of members from fisheries, conservation groups,

CSIRO PUBLISHING

Marine and Freshwater Research, 2014, 65, 1145–1154

http://dx.doi.org/10.1071/MF13330

Journal compilation � CSIRO 2014 www.publish.csiro.au/journals/mfr

the scientific community, and government, and eventually this

species was given full protection in Taiwan in November 2007(Hsu et al. 2012).

Research on age and growth of the whale shark has been

sparse. Because of the difficulty of collecting samples of thisspecies, most reports have been from observations in aquaria(Chang et al. 1997; Kitafuji and Yamamoto 1998; Uchida et al.

2000; Hsu et al. 2013). Apart from observations in captivity,Wolfson (1983) described seven free-ranging neonate speci-mens (55–93 cm TL), but records of individuals between 93 and

300 cm TL are conspicuously absent in the literature (Colman1997; Martin 2007). Rowat et al. (2008) described someneonatal and very small individuals from northern Indian Oceanwaters and discussed the growth rate immediately following

birth. In addition, the age and growth of a very few matureindividuals have been investigated and only one pregnantfemale, which was caught in the Taiwanese fishery in 1995

and hadmore than 300 embryos in her uteri, has ever been foundand dissected (Joung et al. 1996; Chang et al. 1997). A growthstudy based on 15 samples from a wild population off

South Africa was conducted by Wintner (2000), who providedpreliminary von Bertalanffy parameters based on additionalhypothetical data points.

Current regulations for conservation and protection of thewhale shark in many countries limit the collection of moresamples. This study provides the first estimates of age andgrowth parameters of the whale shark in the north-western

Pacific, based on vertebrae from wild-caught specimens collec-ted in Taiwanese fisheries before the catch of this species wasbanned in 2007. The results derived from this study provide

important and useful information for conservation and manage-ment of this species worldwide.

Materials and methods

Sample collection and preparation

According to Taiwanese fishery records on whale shark catch,429 individuals were landed in Nanfanao and Chengkung fishmarkets, eastern Taiwan, between 2001 and 2006, caught by setnet, harpoon, gill-net, and long-line fishermen operating in

waters off the east coast of Taiwan (Fig. 1). We collected ver-tebral samples from a subset of this catch. Shark sex, TL, weight(W) and maturity stage were recorded for each individual sam-

pled whenever possible. The vertebrae used for aging studieswere typically taken from the region near the branchial chamberand under the first dorsal fin, as these vertebrae are relatively

homogeneous and possess a large radius and clearer growthbands (Cailliet et al. 1983a, 1983b, 1985; Pratt and Casey 1983;Wintner and Cliff 1999). Vertebrae from the region anterior tothe first dorsal fin (18th to 22nd centra) were selected for age

analysis in this study and were removed from fresh specimensand stored frozen. The centrum dorsal diameter (CDD) wasmeasured. Vertebral samples were cleaned, infiltrated and

embedded by using KOH, ethanol, t-butyl alcohol and paraffinto prevent deformations. Using an Isomet low-speed saw, ver-tebraewere sectioned transversely from the intermediate zone or

vertically from the dorsal midline such that the completeness ofthe vertebra or the orientation of sectioning would not influenceband counting and measuring.

Age assignment and validation

Fresh and unprocessed sections were photographed by digitalcamera (Nikon D200, Nikon AF Micro Nikkor 60 mm F2.8D).

Processed vertebrae were sectioned and X-radiographed (IMDMCI-4006 X22). While the sections were X-radiographed, the

28�N

27�N

26�N

25�N

24�N

23�N

22�N

128�E127�E

PacificOcean

Taiwan

Chengkung

Nanfanao

China

126�E125�E124�E123�E122�E121�E120�E119�E

Fig. 1. Sampling area of the whale shark (Rhincodon typus) in the north-western Pacific including eastern

Taiwanese waters. Open circles represent capture localities.

1146 Marine and Freshwater Research H. H. Hsu et al.

distance between the tube and the filmwithout sensitisation casewas 100 cm, tube intensity was set at 40–60KV and 16–32mAs,

and films were exposed 3–5 times. Three methods were used toread and count growth band pairs: (1) from computer screenimages of fresh, unprocessed sections(Fig. 2a), (2) directly on

processed sections (Fig. 2b), and (3) on X-ray films ofsections (Fig. 2c).

One band pair comprises one calcified (opaque) and one less

calcified (translucent) band (Cailliet et al. 2006). The firstauthor was the reader and a consensus was determined for thereadings of each section using the following criteria: (1) wherethe first two readings matched, the matching reading was

adopted; (2) where the third reading matched one of the priorreadings, the matching reading was adopted; (3) where noreadings matched but there were two readings that varied by

one band pair, and the fourth reading was adopted whilematching any of the prior three readings. The index of averagepercentage error (IAPE) and the coefficient of variation (CV)

were calculated for each set of first two readings, as described byBeamish and Fournier (1981) and Chang (1982), respectively,and an age bias plot was constructed. Equations used for IAPEand CV were as follows:

IAPE ¼ 1=NX

½1=RX

ðjXij � Xjj=XjÞ� � 100%

CV ¼ 1=NX

ðsi=XjÞ � 100%

where N is the number of sharks aged, R is the number ofreadings,Xij is the count from the jth shark at the ith reading,Xj is

the mean count of the jth shark from i readings, and si is thestandard deviation of i counts from the jth shark.

Periodicity of band pair formation was estimated from mar-ginal increment ratio (MIR) and centrum edge analysis (CEA).

The definition ofMIR followed the description by Conrath et al.(2002): MIR¼MW/PBW, in which MW is the marginal width,and PBW is the previous band pair width. A Kruskal–Wallis test

by ranks was used to test for differences in MIR by month, andOkamura and Semba’s (2009) CEA method was used to statisti-cally verify the timing and frequency of growth-band deposition

on vertebral centra. The modified Akaike’s information criterion(AICc) (Akaike 1973; Burnham and Anderson 2004) was used todetermine which periodicity (or no cycle) of band pair deposition

provided the best fit to edge analysis data.The only pregnant female with full-term embryos was caught

in July (Joung et al. 1996) and thus birthmonth ofwhale sharks inTaiwanese waters was assumed to be July. Opaque band deposi-

tionwas assumed to be restricted in January and July for biannualband pair formation (see Results). With this assumption, eachsample age could be calculated with the following formulae:

Age ¼ BN=2þ ðM � 1Þ=12 ð1oM o 7Þ

Age ¼ BN=2þ ðM � 7Þ=12 ð7oM o 12Þ

Age ¼ BN=2 ðcatch date unknownÞ

where BN is the number of complete band pairs (one opaque andone translucent band) and M is landing month of the sample.

Growth functions

Four growth functions and linear regression were used to fit theobserved TL and age data.When length and weight data of some

(a)

(b)

(c)

Fig. 2. Vertebral photographs showing three methods to read and count

growth band pairs: (a) fresh vertebral section from a 1.6-m TL female;

(b) processed vertebral section from a 4.0-m TLmale; and (c) X-radiograph

of the vertebra from a 1800-kg female. B, birth mark.

Age and growth of the whale shark Marine and Freshwater Research 1147

sharks were incomplete, the precaudal length (PCL), if avail-able, was converted to TL (TL¼ 1.148PCL þ 0.262: Hsu et al.

2012); for individuals without a PCL measurement, W wasconverted to TL (W¼ 12.10TL2.862: Hsu et al. 2012). The vonBertalanffy (VBGF) (von Bertalanffy 1938), modified two-

parameter VBGF (2VBGF: Fabens 1965), Robertson (Robertson1923), and Gompertz (Gompertz 1825) growth functions weredescribed as follows:

Lt ¼ L1f1� exp½�kðt � t0Þ�g ðVBGFÞ

Lt ¼ L1 � ðL1 � L0Þ expð�ktÞ ð2VBGFÞ

Lt ¼ L1=f1þ exp½�kðt � t0Þ�g ðRobertsonÞ

Lt ¼ L1 � expf�exp½�kðt � t0Þ�g ðGompertzÞ

where Lt is predicted length at age t (years from birth), LN is theasymptotic total length, L0 is size at birth (which was 0.64m,adopted from the biggest full-term embryo data of Joung et al.

1996), k is the growth constant (year�1), and t0 is the age at

length zero. Observed length at age data were fitted using thenonlinear regression (PROC NLIN) with SAS software.The AICc was used to determine which model provided the

best fit to length and age data.

Longevity

Theoretical longevity was estimated using two methods. Thesize at which 95% (5(ln2)/k) of LN is attained was determined

following Fabens (1965). Taylor’s (1958) definition of lon-gevity in teleost species as the time to attain 95% of LNwas alsoused. The estimated longevity (age at 95% LN) was calculated

by solving the VBGF for t and replacing Lt with 0.95LN, asfollows:

Longevity ¼ ð1=kÞ lnfðL1 � L0Þ=½L1ð1� xÞ�g

where x¼Lt/LN¼ 0.95 and k, LN, and L0 were parametersfor VBGF.

Results

Sample collection and measurement

Vertebral samples were taken from 92 (43 males, 2.68–9.88mTL; 30 females, 1.60–7.02m TL; 19 unsexed individuals,2.83–6.67m TL) of the 429 individuals caught, 76 of whichwere

used to analyse the cycle of progressive band formation on amonthly basis. In addition, samples from two full-term embryos(61.0-cm TL female and 54.8-cm TLmale) and length data from

another embryo (64 cm TL) in the collection of Joung et al.

(1996) were also included in the study. Length–frequency of thepooled dataset (n¼ 95) indicated that a peak occurred at a size of4–5m TL for both sexes (Fig. 3).

The relationships of CDD (mm) versus TL (m) showed alinear trend and difference between sexes was not significant forthe regression (ANCOVA, P. 0.05) as follows (Fig. 4):

CDD ¼ 10:492TL� 3:850 ðr2 ¼ 0:76; n ¼ 77Þ:

Growth band pair formation

Age bias plot indicates that most samples with 27 or fewer band

pairs were counted consistently (Fig. 5). Although there werehigher variances on vertebral samples with 35 band pairs, lowvalues of 2.37% for IAPE and 3.35% for CV indicated that bandpair counts were highly consistent (Fig. 5). According to the

CDD–TL relationship, the birth size of 0.64m TLwas convertedto birth vertebralCDD as the birthmark. No band pair was foundbefore the birth mark and band pairs were counted to a maxi-

mum of 25 and 42 for a 6.38-m TL female and a 9.88-m TLmale(the only mature individual), respectively.

For verifying the periodicity of growth band pair formation,

Kruskal–Wallis analysis of ranks indicated that mean MIRswere significantly different among January samples versusthose from February, March, April, and May (H¼ 16.24,

d.f.¼ 6, P¼ 0.023). There was one peak in January and anotherpossible one in June; however, sample sizes were low inFebruary (n¼ 3), June (n¼ 4), August (n¼ 2), September(n¼ 3), and November (n¼ 1) (Fig. 6a). In addition, the AICc

value of CEA (no cycle: 106.94; annual: 107.21; biannual:88.79) indicated that the highest probability existed for biannualband pair formation (Fig. 6b). These results indicate that growth

band pairs in these sharks formed biannually.

0

3

6

9

12

15

18

Total length (m)

Num

ber

Male n � 44Female n � 31Sex unknown n � 20

�2 �82–3 3–4 4–5 5–6 6–7 7–8

Fig. 3. Total length–frequency of whale sharks used in this study.

CDD � 10.492 TL � 3.850

r 2 � 0.76

0

20

40

60

80

100

120

140

0 2 4 6 8 10

Total length (m)

Cen

trum

dor

sal d

iam

eter

(m

m)

n � 77

Fig. 4. Linear regression between vertebral centrum dorsal diameter

(CDD) and total length (TL).

1148 Marine and Freshwater Research H. H. Hsu et al.

Growth parameters

The resulting AICc values showed that the 2VBGF best fit maleand sex-combined data (Table 1). Although AICc values for theRobertson function in females were lower than those for the

2VBGF, the asymptotic length of the Robertson function was

6.48m TL (Table 1), much lower than actual observations andliterature reports, and thus 2VBGF was used to describe female

growth. Additionally, the 2VBGF did not significantly differbetween sexes (maximum likelihood ratio test: x2¼ 0.11,P. 0.05) (Kimura 1980). Parameter estimates of the 2VBGF

were LN¼ 16.803m and k¼ 0.037 year�1 based on both sexesand unsexed data (Fig. 7). In addition to the results using themodel of biannual growth band pair formation, parameters

for annual band pair formation also were estimated to beLN¼ 18.023m and k¼ 0.021 year�1 for both sexes (2VBGFalso did not significantly differ between sexes via the maximumlikelihood ratio test, x2¼ 0.14, P. 0.05).

Growth rate and longevity

Growth rates during the first year were estimated to be 0.60myear�1 then declined gradually to 0.29m year�1 by Year 20based on the 2VBGF parameters (Table 2). Longevities were

calculated as 80.4 and 94.2 years using Taylor’s and Fabens’methods, respectively; both values are considerably larger thanthe maximum observed age in this study.

Discussion

Many problems arise when estimating age and growth patternsof fishes, especially large elasmobranchs. For sharks, it is oftendifficult to obtain sufficient numbers of individuals of all sizeand age classes, due to high costs, fishing methods needed, time

involved (Joung et al. 2004) and, in recent decades, conservationconcerns (Hsu et al. 2012). Many countries or regions havebanned fishing for the whale shark and are protecting this spe-

cies (Davis et al. 1997; Norman 2004; Hsu et al. 2012). Strandedspecimens or those that have died in aquaria have providedvertebrae from localities such as South Africa and Japan

(Kitafuji and Yamamoto 1998; Uchida et al. 2000; Wintner2000). Although the sample size used in our study was notoptimal (there were few mature and very small specimens), thisstudy still provides useful age and growth analyses for whale

sharks from the wild population in the north-western Pacific.In many elasmobranch growth studies, the periodicity of

band pair deposition has been discussed and debated. Although

our results showed that a model of two band pairs per year hadthe highest probability, one band pair per year could not becompletely ruled out because our sample size and range were

limited. For some shark species such as the basking shark(Cetorhinus maximus) and the Pacific angel shark (Squatinacalifornica), periodic band pair deposition is related more to

somatic growth than to time (Natanson and Cailliet 1990;Natanson et al. 2008). Natanson et al. (2008) further found thatband counts from different regional vertebrae in larger indivi-dual columns are inconsistent for C. maximus. In our case,

however, counts of vertebral band pairs throughout the columnof the whale shark were consistent.

Biannual band pair deposition has been suggested to occur in

other shark species, including the shortfin mako (Isurus oxy-

rinchus) (Pratt and Casey 1983), the sand tiger (Carchariastaurus) (Branstetter and Musick 1994), and the scalloped

hammerhead (Sphyrna lewini) (Chen et al. 1990; Anislado-Tolentino and Robinson-Mendoza 2001; Kotas et al. 2011).Recently, bomb carbon techniques were used to conclude that

0

5

10

15

20

25

30

35

40

45

0 5 10 15 20 25 30 35 40 45

Reading 1

Rea

ding

2 (

mea

n ±2

s.e.

)

11 4 3

1310

1111107 5 5

2 21

12

1

1

1

IAPE � 2.37%CV � 3.35%

2

Fig. 5. An intrareader age bias plot for the whale shark vertebral growth

band pairs. Numbers above each point represent number of whale sharks,

and dots with vertical bars are themean counts of reading 2 (�2 s.e.) relative

to reading 1. IAPE, index of average percentage error; CV, coefficient of

variation.

0

0.4

0.8

1.2

1.6

2.0(a)

(b)

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

Month

Mea

n m

argi

nal i

ncre

men

t rat

io

6

3

22

10

6

4

5

2

3

6

18

0%

20%

40%

60%

80%

100%

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

Fre

quen

cy

6 3 22 10 6 4 5 2 3 6 1 8

Opaque Translucent

Fig. 6. (a) Monthly marginal increment ratios, and (b) monthly edge

formation, of the vertebrae from 76 individuals. Numbers above each bar

represent sample size. Vertical bars indicate � 2 s.e. Crosses, open circles

and solid triangles denote values predicted by band pair depositionmodels of

no cycle, annual, and biannual, respectively.

Age and growth of the whale shark Marine and Freshwater Research 1149

bands in the shortfin mako are deposited annually (Campanaet al. 2002; Natanson et al. 2006). A sample from recaptured,oxytetracycline (OTC)-injected shortfin mako supported a

deposition of one band pair per year (Natanson et al. 2006),but two band pairs per year in younger makos was also proposedbased on 29 tag–recapture samples (Wells et al. 2013). Goldman

et al. (2006) re-examined age and growth estimates of the sandtiger, and validated annual formation of a single band pair.

Several other studies on the age and growth of S. lewini alsofound an annual growth band pair cycle (Schwartz 1983;Branstetter 1987; Piercy et al. 2007). Biannual band pair

formation on scales and otoliths in several teleosts has beendocumented for the threadfin bream (Nemipterus japonicas) andtilapia (Oreochromis niloticus) (Rao and Rao 1986; Admassu

and Casselman 2000; Bwanika et al. 2007).One whale shark maintained in the Okinawa Churaumi

Aquarium, Japan, was fed food containing OTC and later

analysis of this shark’s vertebrae supported a model of one bandpair per year (Cailliet et al. cited in Colman 1997). However,MIR analysis of our vertebrae showed that one obvious peak andalso another uncertain peak was present, based on the limited

sample size. In addition, the CEA showed a higher probabilityfor biannual band pair formation. Although only one matureshark was sampled in our study, two growth band pairs per year

appear more responsible for juvenile whale shark vertebrae, ashas been concluded for juvenile shortfin makos off California(Wells et al. 2013). The mechanism behind vertebral band

formation is still under study by elasmobranch biologists.Ribot-Carballal et al. (2005) suggested that temperature influ-ences band formation for the shortfin mako, but no effect of

Table 1. Parameters of growth functions

Estimates of growth parameters and goodness of fit for linear regression and four growthmodels fitted to observed size-at-age data for the whale shark. VBGF,

von Bertalanffy growth function; 2VBGF, modified 2-parameter VBGF with L0 – 64 cm; AICc, modified Akaike’s information criterion. AICc values are

based on absolute differences between models, where a lower value indicates the better model

Growth model Parameter Male (n¼ 44) Female (n¼ 31) Sex combined (n¼ 95)

Estimate AICc value Estimate AICc value Estimate AICc value

Based on annual band pair formation

Linear – – 112.1 – 63.93 – 214.43

VBGF LN 18.072 113.8 12.559 65.49 14.558 209.96

k 0.017 – 0.030 – 0.023 –

t0 �2.113 – �0.683 – �1.576 –

2VBGF LN 18.023 110.4 15.821 62.43 15.338 206.93

k 0.017 – 0.021 – 0.021 –

Robertson LN 10.042 116.3 6.406 62.39 8.590 218.66

k 0.100 – 0.229 – 0.125 –

t0 16.789 – 10.283 – 13.652 –

Gompertz LN 11.126 115.0 6.978 62.79 9.457 213.36

k 0.061 – 0.143 – 0.078 –

t0 12.996 – 8.302 – 10.539 –

Based on biannual band pairs formation

Linear – – 111.3 – 63.43 – 213.33

VBGF LN 19.207 113.1 14.740 65.59 15.607 209.96

k 0.031 – 0.047 – 0.042 –

t0 �1.015 – �0.380 – �0.782 –

2VBGF LN 19.704 109.7 20.500 62.53 16.803 207.03

k 0.030 – 0.029 – 0.037 –

Robertson LN 10.105 115.5 6.477 62.49 8.707 217.86

k 0.198 – 0.446 – 0.243 –

t0 8.728 – 5.465 – 7.202 –

Gompertz LN 11.248 114.1 7.097 62.99 9.620 212.86

k 0.120 – 0.276 – 0.151 –

t0 6.840 – 4.469 – 5.622 –

0

2

4

6

8

10

0 5 10 15 20 25 30 35 40 45 50

Age (years)

Tot

al le

ngth

(m

)

Observed data for biannual band pairs

Observed data for annual band pair2VBGF for biannual band pairs

2VBGF for annual band pair

Annual: Lt � 15.34 – 14.70 e�0.021t

Biannual: Lt � 16.80 – 16.16 e�0.037t

Fig. 7. Modified two-parameter von Bertalanffy growth function

(2VBGF) for the whale shark in the north-western Pacific.

1150 Marine and Freshwater Research H. H. Hsu et al.

temperature on band deposition was apparent for little skates(Raja erinacea) (Natanson 1993). For whale sharks, watertemperature, plankton blooms, light, duration in coastal or

pelagic life stages, and long-distance migrations might affectthe pattern of band formation. Further research is needed onthese relationships.

The 0.64m TL size at birth of R. typus appears to be much

smaller than that of other large shark species such asC. maximus(1.5–1.7m TL: Compagno 2001) and white shark (Carcharodoncarcharias) (1.07–1.65m TL: Compagno 2001). Small size at

birth, filter-feeding habits, and slower swimming speed (Hsuet al. 2007) may expose juvenile R. typus to a higher naturalmortality rate, which may be offset by its larger litter size and

higher neonatal growth rate (Joung et al. 1996; Chang et al.

1997). Further research related to the evolutionary meaning ofthe relationship between size at birth and litter size is needed.

Because only onemature and few very small specimens wereused in our study, the derived growth function was based onmostly immature individuals and combined-sex data. Whencomparing our results with Wintner’s (2000) theoretical growth

curves, LN and k values differ slightly (this study: LN¼ 16.80mTL, k¼ 0.037 year�1; Wintner: LN¼ 14.96–19.66m TL,k¼ 0.021–0.032 year�1), likely due to annual versus biannual

band pair formation or regional differences. If more samples areacquired in the future, our growth curve will be revised andseparated by sex.

The maximum sizes of 16.0 and 17.3m TL calculated fromthe length–weight equation of Hsu et al. (2012) for whalesharks weighing 34 000 kg (Chen et al. 1997) and 42 000 kg(S. J. Joung’s personal observation), respectively, are close to

the present LN values of 15.3 or 16.8m. The LN is smaller thanCompagno’s (2001) suggestion of 21.4m and Eckert andStewart’s (2001) record of 18m, but neither of these directly

measured individual whale sharks at such sizes.A male whale shark maintained in Okinawa Churaumi

Aquarium for more than 17 years attained sexual maturity at8.5m TL (Matsumoto et al. 2013). Colman (1997) indicated that

the whale sharks of both sexes at Ningaloo Reef mature at morethan 9m TL; the age for this size converts to 19.8 years based onour biannual 2VBGF. Norman and Stevens (2007) observed a

large number of specimens underwater in the same region andestimated that 50% and 95% size atmaturity formales was 8.1mTL and 9.1m TL, respectively; these sizes represent ages of

16.8 and 20.1 years respectively, using our results. The largestimmature female recorded in South Africa was 8.7m TL

(Beckley et al. 1997), which converts to 18.8 years. In Taiwa-

nese waters, the only pregnant female observed to date was10.6m TL (Joung et al. 1996), corresponding to 26.0 years. Theage of 9.6m TL and 11.9m TLmature females caught off easternTaiwan (H. H. Hsu, unpubl. data) are calculated to be 22.0 and

32.3 years, respectively. From these various reports and con-versions, we estimate that male whale sharks in the Indo-Pacificbegin maturing at ,17 years, and females mature between 19

and 22 years. In the Atlantic there is some preliminary evidencethat female whale sharks may mature at a length as small as7.5m TL (Hueter et al. 2013); this would correspond to an age of

,15 years if growth rates in theAtlantic are identical to thosewehave found in the north-western Pacific, which they may not beas Indo-Pacific and Atlantic whale sharks appear to representgenetically different populations (Castro et al. 2007). Age at

Table 2. Calculated growth rates for the whale shark

Growth rates (m year�1) calculated using a two-parameter von Bertalanffy growth function based on observed length-at-age values

Annual Biannual

Age (year) TL Growth rate Age (year) TL Growth rate Age (year) TL Growth rate

(m) (m year�1) (m) (m year�1) (m) (m year�1)

0 0.64 20 5.739 0 0.64

1 0.95 0.28 21 5.941 0.197 1 1.224 0.603

2 1.253 0.275 22 6.139 0.194 2 1.787 0.58

3 1.55 0.27 23 6.333 0.191 3 2.329 0.558

4 1.84 0.265 24 6.523 0.187 4 2.852 0.537

5 2.125 0.261 25 6.708 0.184 5 3.356 0.516

6 2.403 0.256 26 6.89 0.181 6 3.842 0.497

7 2.676 0.252 27 7.068 0.178 7 4.31 0.478

8 2.943 0.248 28 7.243 0.175 8 4.762 0.46

9 3.204 0.243 29 7.413 0.172 9 5.197 0.443

10 3.46 0.239 30 7.58 0.169 10 5.616 0.426

11 3.71 0.235 31 7.744 0.166 11 6.02 0.41

12 3.955 0.231 32 7.904 0.163 12 6.41 0.394

13 4.195 0.227 33 8.061 0.16 13 6.785 0.379

14 4.43 0.223 34 8.214 0.158 14 7.147 0.365

15 4.66 0.219 35 8.364 0.155 15 7.496 0.351

16 4.885 0.215 36 8.511 0.152 16 7.832 0.338

17 5.105 0.212 37 8.655 0.15 17 8.157 0.325

18 5.321 0.208 38 8.796 0.147 18 8.469 0.313

19 5.532 0.204 39 8.934 0.144 19 8.77 0.301

20 5.739 0.201 40 9.069 0.142 20 9.06 0.289

Age and growth of the whale shark Marine and Freshwater Research 1151

maturity on a population scale is critical to assess demographyfor this threatened species (Bradshaw et al. 2007).

Some shark species have a k value lower than 0.1 year�1; forexample, the shortfin mako (0.05 year�1: Ribot-Carballal et al.2005), the dusky shark (Carcharhinus obscurus) (0.04 year�1:

Natanson et al. 1995), and the white shark (0.065 year�1:Wintner and Cliff 1999). These species, like the whale shark,are all large migratory elasmobranchs for which energy may be

used more for movement than growth, thus the lower k values.However, blue sharks (Prionace glauca) migrate long distances(Kohler et al. 2002) and yet have been estimated to have a veryhigh k value of 0.16 or 0.25 year�1 (Cailliet et al. 1983a; Lessa

et al. 2004). Further research on feeding habits, migratorybehaviour, energy transformation and k values is needed toclarify these relationships.

Chang et al. (1997) reported growth rates of ,8.1–22.3 cmmonth�1 in the first months after birth for whale shark speci-mens in aquariums, and a 0.7m TL male (one of the specimens

studied by Joung et al. 1996) raised in the Oita Aquarium, Japan,grew 1.3m in the first year, and 2.99m in 25months (Young andHorike 1998). One captive male whale shark raised in Taiwan’saquarium grew from 2.3m to 7.2m TL in eight years (61.3 cm

year�1: Hsu et al. 2013). These results for growth rate weremuch higher than our derived 0.6m year�1 in the first year afterbirth for wild sharks. Whale sharks maintained in Japanese

aquaria have shown average annual growth of 21.6–50.0 cm(Kitafuji andYamamoto 1998; Uchida et al. 2000). InWintner’s(2000) study, growth rates of the first year after birth were

estimated to be 0.45 and 0.40m based on two assumed VBGFs.It is not uncommon for sharks to exhibit significantly highergrowth rates in captivity than in the wild, due to lower energy

demands, constant temperature, consistent availability of high-energy food, and other factors in aquaria (Mohan et al. 2004).

A longevity of at least 80 years in whale sharks is longerthan those estimated for most other shark species (Cailliet and

Goldman 2004; Garcıa et al. 2008). The lifespans of thesandbar (C. plumbeus) and dusky sharks have been estimatedto be more than 30 years (Garcıa et al. 2008; Andrews et al.

2011). The longnose velvet dogfish (Centroscymnus crepida-ter) was estimated to be 54 years (Irvine et al. 2006). The whiteshark and leafscale gulper shark (Centrophorus squamosus)

might live more than 70 years (Clarke et al. 2002; Garcıa et al.2008; Hamady et al. 2014). Longevity data are important forassessing population dynamics of whale sharks (Bradshawet al. 2007), and the relationship among high longevity, huge

body size and other evolutionarily significant factors in fishesrequires further study.

Slow growth (k¼ 0.037 year�1) and high longevity (80.4

years) make the whale shark very sensitive to fisheries exploita-tion and environmental change (Pauly 2002). Prior to Taiwan’sban of fishing for the whale shark in 2007, Taiwanese commer-

cial fishermen landed between 80 and 270 individuals everyyear (Hsu et al. 2012). The ban now in place should be strictlyenforced and incidental catch or by-catch should be monitored

to ensure the long-term sustainability of the whale sharkpopulation in the north-western Pacific. In addition, interna-tional management and cooperation on this highly migratoryand vulnerable species are important. Further studies on

region-specific age validation, stock assessment, ecology, and

behaviour of the whale shark also are needed to help manage theburgeoning exploitation of this species in ecotourism operations

around the world.

Acknowledgements

We thank L. F. Chen and C. Y. Joung, processors of sharks in the Nanfanao

fish market, W. J. Chen, the consignee of shark sales in the Chengkung fish

market, and W. C. Chiang and J. H. Tien, Eastern Marine Biology Research

Center, for collecting vertebral samples. We also thank the Georgia

Aquarium for supporting ourR. typus research. This studywas funded by the

Fisheries Agency, Taiwan, R. O. C. (grants Nos FA90-145-F1-15, FA91-

251-F1-23, FA92-911-F1-5, FA93-911-F1-12, FA94-1411-F1-11, and

FA95-1411-F2-2).

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