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Size and maturity status of the whale shark (Rhincodon typus) at Ningaloo Reef in Western Australia
Fisheries Research 84 (2007) 81–86
Size and maturity status of the whale shark (Rhincodon typus) at Ningaloo Reef in Western Australia Bradley M. Norman a,∗ , John D. Stevens b a
Ecocean, c/o Centre for Fish and Fisheries Research, Murdoch University, South St. Murdoch, Western Australia 6150, Australia b CSIRO Marine and Atmospheric Research, Castray Esplanade Hobart, Tasmania 7000, Australia
Abstract Between 1995 and 1997, 360 observations of whale sharks at Ningaloo Reef revealed that approximately 85% were males (4–12 m TL). Based on the external morphology of claspers, all males <7 m TL were immature. Only 9.3% of males between 7 and 8 m TL were found to be mature, compared to 36.6% of those between 8 and 9 m TL. All but one of the 79 male whale sharks >9 m were considered mature. A logistic equation fitted to the percentage of mature males in each size class predicted a length at first maturity (L50 ) of ∼8.0 m TL, while 95% (L95 ) of males were mature by ∼9.0 m TL. Female whale sharks at Ningaloo Reef during this study were generally smaller and ranged in length from 4 to 8 m TL. The small size and general absence of female whale sharks from Ningaloo Reef suggest that the region may be important for feeding rather than breeding. © 2006 Published by Elsevier B.V. Keywords: Whale shark; Size structure; Ecotourism; Ningaloo Reef
1. Introduction Whale sharks (Rhincodon typus) occur throughout the tropical and sub-tropical regions of the world and are documented from 160 range states (e.g. Allen and Steene, 1988; Last and Stevens, 1994; Taylor, 1994; Clarke and Nelson, 1997; Norman, 2000; Compagno, 2001; Duffy, 2002). While they are currently threatened and listed as Vulnerable by the World Conservation Union (IUCN), seasonal aggregations are known from several areas that include Mexico, Belize, the Coral Sea (off Queensland, Australia), the Australian Commonwealth External Territory of Christmas Island and Ningaloo Reef (Western Australia), each of which apparently coincides with an increase in food availability linked to either cnidarian, crustacean or teleost spawning events (Taylor, 1994; Heyman et al., 2001) or through suitable environmental conditions (Wilson et al., 2001; Duffy, 2002). Annual seasonal aggregations of whale sharks at Ningaloo Reef, Western Australia (see Fig. 1) have been documented since the 1960s (G. King, King Dive, Exmouth, Australia, personal communication) with an associated whale shark ecotourism industry operating since 1993 (Mau et al., 2004). Little is known of the biology of whale sharks, and there is a paucity ∗
Corresponding author. Tel.: +61 414953627; fax: +61 893606303. E-mail address: [email protected] (B.M. Norman).
0165-7836/$ – see front matter © 2006 Published by Elsevier B.V. doi:10.1016/j.fishres.2006.11.015
of information on the size distribution, sex ratio and size at sexual maturity at Ningaloo Reef. Between 1995 and 1997, data recorded by tourist operators and by the senior author at Ningaloo Reef was aimed at addressing these deficiencies. The aims of this study were to determine the size distribution, sex ratio and size at maturity of male R. typus at Ningaloo Reef, Western Australia. 2. Methods 2.1. Length estimates and size at maturity of male whale sharks at Ningaloo Reef Whale shark lengths were estimated to the nearest 0.5 m total length (TL) using a 15 m rope (knotted at 1 m intervals) held underwater alongside the sharks. Some estimates were based on the length of a snorkeller (assumed to be 2 m) swimming alongside the whale shark. All lengths given are TL. The sex of each shark could be determined by diving below the pelvic fins and recording the presence or absence of claspers. Clasper morphology is a reliable and non-invasive means of assessing sexual maturity in male sharks (Joung and Chen, 1995). Claspers are short, soft and smooth in sexually immature individuals, but exhibit accelerated growth and calcification during maturation (McLaughlin and O’Gower, 1971; Bass et al., 1975) and in whale sharks often appear rough and abraded (see
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B.M. Norman, J.D. Stevens / Fisheries Research 84 (2007) 81–86
loo was determined by subjecting the percentage contributions made to each length class by mature animals to logistic regression analysis, using bootstrapping of 1000 random samples (see Smith et al., 2004). 1 1 + e−ln19(L−L50 )/(L95 −L50 ) where PL is the proportion of R. typus with mature, calcified claspers at length interval L, and L50 and L95 are the lengths at which 50 and 95% of the population are mature.
PL =
3. Results
Fig. 1. Location of whale shark observations during 1995, 1996 and 1997 at Ningaloo Reef in Western Australia.
Fig. 3). Thus, using the external morphology of claspers as an indicator of sexual maturity, male whale sharks were designated as ‘immature’ if the claspers were short, smooth and did not extend beyond the pelvic fins, or ‘mature’ if the claspers were elongated and extended beyond the pelvic fins. In many cases, this latter group had claspers that appeared abraded, some to the extent that they had a ‘cauliflowered’ appearance, possibly as a result of previous sexual activity. The dataset collected by the senior author was supplemented by observations on the length of sharks from industry operators. Between 1995 and 1997, all whale sharks at Ningaloo Reef observed by the operators were recorded in the Western Australian Department of Conservation and Land Management (CALM) Whale Shark Operator Logbooks. However, it was often difficult for these operators to collect data on whale shark sex in addition to undertaking their normal tasks. For this reason, these data were not included in this analysis. The total length at which 50% (L50 ) and 95% (L95 ) (including their 95% confidence limits) of R. typus were mature at Ninga-
Information on the size, sex (and for males) maturity state based on length and/or degree of clasper abrasion of R. typus was collected on 360 separate occasions while aboard commercial vessels throughout the 1995, 1996 and 1997 whale shark seasons at Ningaloo Reef. The location of each in-water interaction with whale sharks is shown in Fig. 1. 3.1. Size structure of whale sharks at Ningaloo Reef During 1995, at Ningaloo Reef, the smallest shark recorded in this study was ∼3 m and the largest was ∼12 m (Table 1; Fig. 2); the mean total length was 7.0 m. The results from tour operators indicate that the size of the sharks in 1995 ranged between 2 and 13 m, with a mean total length of 7.2 m. The recorded length range in 1996 was 4.5–12 m, with a mean of 7.6 m. The industry operators recorded a minimum length of 2 m and a maximum length of 14 m (mean 7.7 m) in the same year. In 1997, the length range recorded was 4–10 m, with a mean of 6.7 m, compared with a range of 2–12 m and mean of 7.0 m recorded by the industry. Overall, the mean total length of R. typus at Ningaloo Reef was 7.3 or 7.4 m as recorded during our surveys or by the industry, respectively (Table 1). The modal length class of whale sharks recorded in this study in 1995 and 1996 was 6–7 m, while in 1997, it was 7–8 m (Fig. 2). Overall, modal lengths of 6–7 m were recorded for both male and
Table 1 Estimated mean total length (±S.E.) and sex ratio of Rhincodon typus at Ningaloo Reef from 1995 to 1997 Year
Mean whale shark length (m)
1995 This study Industry records
7.0 ± 0.2 (n = 125) 7.2 ± 0.1 (n = 361)
3–12 2–13
71.7 (n = 113) –
1996 This study Industry records
7.6 ± 0.1 (n = 177) 7.7 ± 0.1 (n = 858)
4.5–12 2–14
91.6 (n = 154) –
1997 This study Industry records
6.7 ± 0.2 (n = 58) 7.0 ± 0.1 (n = 760)
4–10 2–12
91.4 (n = 58) –
Overall (1995–1997) This study Industry records
7.2 ± 0.1 (n = 360) 7.4 ± 0.04 (n = 1979)
3–12 2–14
84.6 (n = 175) –
In 1995 and 1996, 12 and 23 animals, respectively, were unable to be sexed.
Length range (m)
Percentage males
B.M. Norman, J.D. Stevens / Fisheries Research 84 (2007) 81–86
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Fig. 2. Length–frequency histograms of whale sharks sighted by the senior author (personal observations) (A) and by industry operators (industry records) (B) at Ningaloo Reef for each year between 1995 and 1997. The sexes are separated in (A) only. Combined data (1995–1997) for (A) and (B) are also presented.
female whale sharks. The pooled length–frequency distribution data from 1995 to 1997 were very similar when compared with data collected by industry operators during this same period (Fig. 2). Between 1995 and 1997, 84.6% of the 325 individual R. typus that could be sexed at Ningaloo were male. There was however, some interannual variation with 71.7% of sexed sharks being identified as male in 1995, compared to 91.6 and 91.4% in 1996 and 1997, respectively (Table 1). Of those whale sharks sighted that could be sexed, the males ranged in length from 4 to 12 m and all whale sharks recorded >9 m were male (Fig. 2). The length range of males was similar in the different years. For example, in 1995, 1996 and 1997 males ranged in length from 4 to 12, 5 to 11 and 4 to 11 m, respectively.
In contrast, the female whale sharks typically ranged from 5 to 7 m in total length, with a small number of 4 and 8 m animals recorded (Fig. 2). 3.2. Length at maturity of male whale sharks The clasper morphology of a total of 275 male whale sharks was visually assessed between 1995 and 1997. Enlarged or abraded claspers were not observed in any shark less than 7 m TL (Fig. 4). However, 9.3% of males in the 7–8 m length class possessed enlarged and sometimes abraded claspers, while over 36% of males in the 8–9 m length class were considered mature (Figs. 3 and 4). Of the 79 male sharks >9 m TL, all but one were considered mature (Fig. 4).
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4. Discussion 4.1. Length range and sex ratio
Fig. 3. Clasper morphology of: (A) an immature and (B) a mature male whale shark.
When the logistic function was fitted to the length at maturity data, it was found that the length at which 50% (L50 ) of male whale sharks were mature was ∼8.1 m TL (95% confidence limits = 7.9–8.2 m TL) (Fig. 4). The length at which 95% (L95 ) of male whale sharks had attained maturity was ∼9.1 m (95% confidence limits = 8.9–9.3 m TL).
Results from our observations indicated that the whale sharks at Ningaloo Reef had a mean TL of 7.0 m in 1995, 7.6 m in 1996 and 6.8 m in 1997. Approximately 40–45% of whale sharks at Ningaloo Reef are between 6 and 8 m in length, with ∼40% above this size (see Fig. 2). This agrees with Taylor (1994) who reports that the whale sharks sighted at Ningaloo Reef are usually between 6.0 and 7.5 m in length, and is also consistent with commercial operators in 1993, where a modal length of sharks sighted was 6–8 m (n = 303) (CALM, unpublished). Most species of sharks form groups that are segregated by size and sex (Klimley, 1987; Bres, 1993). A high level of sexual segregation appears to exist at Ningaloo Reef, with most R. typus recorded as male (∼85%) throughout the present study (i.e. ∼72% in 1995, ∼92% in 1996 and ∼91% in 1997). A similar proportion of male whale sharks was reported in 1993, with 86% of sharks (n = 222) identified as male (CALM, unpublished). While age and growth data on whale sharks are limited, it is thought that they are born at ∼50–60 cm TL (Joung et al., 1996). Chang et al. (1997) reported that under captive conditions the TL of a new-born whale shark increased from 60 to 139 cm over a 120-day period. Based on this rapid early growth in captivity, it seems feasible that whale sharks could attain 2 m by the end of their 1st year and that the smallest specimens (2–4 m) observed at Ningaloo Reef may have been in their first few years of life. A captive whale shark in the Osaka aquarium grew from 4 to almost 8 m TL in 8 years (Wintner, 2000). However based on vertebral growth rings, Wintner (2000) found that a whale shark of ∼5 m (precaudal length) would be approximately 20 years of age. As for most sharks, growth may be rapid in the first few years to enable them to grow quickly through the predation window, after which it slows down. The estimation of growth rates requires careful validation and is best not interpreted from captive specimens. Using improved measuring techniques e.g. underwater lasers, stereophotography etc. to accurately determine TL measurements of identified individual whale sharks, in conjunction with whale shark photo-identification and numerous resightings (Arzoumanian et al., 2005), will aid in the determination of the growth of R. typus in their natural environment. 4.2. Maturity in male whale sharks
Fig. 4. Logistic curve (±95% confidence intervals) reflecting the size at maturity of male whale sharks at Ningaloo Reef.
Our results demonstrate that approximately 85% of all whale sharks sexed at Ningaloo Reef were males. Analysis of data for the 275 males, for which clasper observations were available, indicates that the length at which 50% of male R. typus are mature is ∼8.0 m TL. Using the growth curve in Wintner (2000), R. typus of this length are approximately 30 years of age. Beckley et al. (1997) examined the claspers of 13 male whale sharks (3.90–10.26 m TL) from South Africa and only three had calcified claspers, and each was >9 m TL.
B.M. Norman, J.D. Stevens / Fisheries Research 84 (2007) 81–86
4.3. Maturity in female whale sharks It is not possible to determine sexual maturity in females by simple external observation. Pai et al. (1983) and Rao (1986) studied two female whale sharks (7.9 and 8.6 m TL) and found these specimens to have immature ovaries. Beckley et al. (1997) examined seven females (∼4.8–8.7 m TL) from the South African coast, finding that all were immature. The only information on a mature female whale shark is from Joung et al. (1996) who reported that a 10.6 m TL shark had approximately 300 near-term embryos ranging in length from 48–64 cm TL. Based on the above data, it is likely that female whale sharks mature at or above a similar length to that reported for males in this study. Since large females and small new-borns are absent from the Ningaloo region, it is possible that breeding females occur in offshore waters where they are not readily observed. Wolfson (1983) reports on seven juvenile whale sharks (0.55–0.93 m) captured in pelagic tuna purse seine fisheries that were operating in water depths greater than 2600 m. Anecdotal reports from whale sharks sighted at the Galapagos Islands have noted very large females with a distended belly region, which may indicate pregnancy (J. Holmberg, Ecocean, Portland, USA, personal communication). It is interesting to note that small whale sharks have only been recorded from the diets of two species, blue marlin (Makaira nigricans) (A. Goorah, Ministry of Fisheries and Marine Resources, Mauritius, personal communication) and oceanic blue sharks (Prionace glauca) (Kukuyev, 1996), two species that generally occur in areas far from land. Initial rapid growth, combined with difficulty in locating small whale sharks, and/or the possibility that breeding grounds are far from Ningaloo Reef may account for the absence of sightings of this group from the study area. This study has helped to confirm that the whale shark aggregation at Ningaloo Reef is related to feeding rather than reproduction. There is a need to determine the population demographics of other aggregations throughout the world and identify both breeding and nursery grounds for this threatened iconic species. Acknowledgements Special thanks to the members of the whale shark ecotourism industry at Ningaloo Marine Park and Christmas Island, Indian Ocean and the Western Australian Department of Conservation and Land Management (CALM) and Parks Australia North for their assistance in data collection throughout this study. Funding was provided from several sources including the above stakeholders and also the Thyne Reid Education Trust, Murdoch University, Shire of Exmouth, the Commonwealth Department of the Environment and Heritage, the Feilman Foundation, Australian Geographic, the Australian Marine Conservation Society, the former Commonwealth Department of Tourism, WA Lotteries Commission, Skywest Airlines Pty Ltd., Greyhound Coachlines, Sundaze (Oakley), Rip Curl, Sherwood SCUBA, Fishcare WA, and the WA Department of Commerce and Trade.
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Thanks to the many field volunteers, especially Simon Visser and Rhiannon Bennett. The authors are greatly indebted to Dr David Morgan for providing assistance and advice throughout the drafting of this manuscript. The referees are also acknowledged for their useful comments. References Allen, G.R., Steene, R.C., 1988. Fishes of Christmas Island Indian Ocean. Christmas Island Natural History Association, Christmas Island, Indian Ocean. Arzoumanian, Z., Holmberg, J., Norman, B., 2005. An astronomical patternmatching algorithm for computer-aided identification of whale sharks Rhincodon typus. J. Appl. Ecol. 42, 999–1011. Bass, A.J., D’Aubery, J.D., Kistnasamy, N., 1975. Sharks of the east coast of southern Africa. IV. The families Odontaspidae, Scapanorhynchidae, Isuridae, Cetorhinidae, Alopiidae, Orectolobidae and Rhiniodontidae. Investigational Report 39. Oceanographic Research Institute, Durban. Beckley, L.E., Cliff, G., Smale, M.J., Compagno, L.J.V., 1997. Recent strandings and sightings of whale sharks in South Africa. Environ. Biol. Fish. 50, 343–348. Bres, M., 1993. The behaviour of sharks. Rev. Fish Biol. Fish. 3, 133–159. Chang, W.B., Leu, M.Y., Fang, L.S., 1997. Embryos of the whale shark Rhincodon typus: early growth and size distribution. Copeia 2, 444–446. Clarke, E., Nelson, D.R., 1997. Young whale sharks Rhincodon typus feeding on a copepod bloom near La Paz Mexico. Environ. Biol. Fish. 50, 63–73. Compagno, L.J.V., 2001. FAO species catalogue. Sharks of the World. An Annotated and Illustrated Catalogue of Shark Species Known to Date, vol. 2. FAO, Rome. Duffy, C.A.J., 2002. Distribution, seasonality, lengths and feeding behaviour of whale sharks (Rhincodon typus) in New Zealand waters. N.Z. J. Mar. Freshwater Res. 36, 565–570. Heyman, W., Graham, R., Kjerfve, B., Johannes, R.E., 2001. Whale sharks Rhincodon typus aggregate to feed on fish spawn in Belize. Mar. Ecol. Prog. Ser. 215, 275–282. Joung, S.-J., Chen, C.-T., 1995. Reproduction in the sandbar shark, Carcharhinus plumbeus, in the waters of northeastern Taiwan. Copeia 3, 659– 665. Joung, S.-J., Chen, C.-T., Clarke, E., Uchida, S., Huang, W.Y.P., 1996. The whale shark Rhincodon typus is a livebearer: 300 embryos found in one ‘megamamma’ supreme. Environ. Biol. Fish. 46, 219–223. Klimley, A.P., 1987. The determinants of sexual segregation in the scalloped hammerhead shark, Sphyrna lewini. Environ. Biol. Fish. 18, 27–40. Kukuyev, E.I., 1996. The new finds in recently born individuals of the whale shark Rhiniodon typus (Rhiniodontidae) in the Atlantic Ocean. J. Icthyol. 36, 203–205. Last, P.R., Stevens, J.D., 1994. Sharks and Rays of Australia. CSIRO, Hobart, Australia. Mau, R., Fitzpatrick, B., Chindemi, M., 2004. Whale shark interaction management: Progress Report 2004. Progress Report for the Department of Conservation and Land Management Wildlife Management Program No. 27. Perth. McLaughlin, R.H., O’Gower, A.K., 1971. Life history and underwater studies of a heterodont shark. Ecol. Monogr. 41, 271–289. Norman, B.M., 2000. In: Hilton-Taylor, C. (Ed.), IUCN Red List of Threatened Species. IUCN, Gland and Cambridge. Pai, M.V., Nandakumar, G., Telang, K.Y., 1983. On a whale shark, Rhincodon typus Smith landed off Karwar, Karnataka. Ind. J. Fish. 30, 157– 160. Rao, G.S., 1986. Note on the occurrence of the whale shark off Veraval coast. In: Marine Fisheries Information Service, T and E Series No. 66. CMFRI, Cochin. Smith, K.D., Hall, N.G., de Lestang, S., Potter, I.C., 2004. Potential bias in estimates of the size of maturity of crabs derived from trap samples. ICES J. Mar. Sci. 61, 906–912.
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Taylor, G., 1994. Whale Sharks. Angus and Robertson Publishers, Sydney. Wilson, S.G., Taylor, J.G., Pearce, A.F., 2001. The seasonal aggregation of whale sharks at Ningaloo Reef, Western Australia: currents, migrations and El Nino/Southern Oscillation. Environ. Biol. Fish. 61, 1– 11.
Wintner, S.P., 2000. Preliminary study of vertebral growth rings in the whale shark, Rhincodon typus, from the east coast of South Africa. Environ. Biol. Fish. 59, 441–451. Wolfson, F.H., 1983. Records of seven juveniles of the whale shark, Rhincodon typus. J. Fish. Biol. 22, 647–655.
Size and maturity status of the whale shark (Rhincodon typus) at Ningaloo Reef in Western Australia Bradley M. Norman a,∗ , John D. Stevens b a
Ecocean, c/o Centre for Fish and Fisheries Research, Murdoch University, South St. Murdoch, Western Australia 6150, Australia b CSIRO Marine and Atmospheric Research, Castray Esplanade Hobart, Tasmania 7000, Australia
Abstract Between 1995 and 1997, 360 observations of whale sharks at Ningaloo Reef revealed that approximately 85% were males (4–12 m TL). Based on the external morphology of claspers, all males <7 m TL were immature. Only 9.3% of males between 7 and 8 m TL were found to be mature, compared to 36.6% of those between 8 and 9 m TL. All but one of the 79 male whale sharks >9 m were considered mature. A logistic equation fitted to the percentage of mature males in each size class predicted a length at first maturity (L50 ) of ∼8.0 m TL, while 95% (L95 ) of males were mature by ∼9.0 m TL. Female whale sharks at Ningaloo Reef during this study were generally smaller and ranged in length from 4 to 8 m TL. The small size and general absence of female whale sharks from Ningaloo Reef suggest that the region may be important for feeding rather than breeding. © 2006 Published by Elsevier B.V. Keywords: Whale shark; Size structure; Ecotourism; Ningaloo Reef
1. Introduction Whale sharks (Rhincodon typus) occur throughout the tropical and sub-tropical regions of the world and are documented from 160 range states (e.g. Allen and Steene, 1988; Last and Stevens, 1994; Taylor, 1994; Clarke and Nelson, 1997; Norman, 2000; Compagno, 2001; Duffy, 2002). While they are currently threatened and listed as Vulnerable by the World Conservation Union (IUCN), seasonal aggregations are known from several areas that include Mexico, Belize, the Coral Sea (off Queensland, Australia), the Australian Commonwealth External Territory of Christmas Island and Ningaloo Reef (Western Australia), each of which apparently coincides with an increase in food availability linked to either cnidarian, crustacean or teleost spawning events (Taylor, 1994; Heyman et al., 2001) or through suitable environmental conditions (Wilson et al., 2001; Duffy, 2002). Annual seasonal aggregations of whale sharks at Ningaloo Reef, Western Australia (see Fig. 1) have been documented since the 1960s (G. King, King Dive, Exmouth, Australia, personal communication) with an associated whale shark ecotourism industry operating since 1993 (Mau et al., 2004). Little is known of the biology of whale sharks, and there is a paucity ∗
Corresponding author. Tel.: +61 414953627; fax: +61 893606303. E-mail address: [email protected] (B.M. Norman).
0165-7836/$ – see front matter © 2006 Published by Elsevier B.V. doi:10.1016/j.fishres.2006.11.015
of information on the size distribution, sex ratio and size at sexual maturity at Ningaloo Reef. Between 1995 and 1997, data recorded by tourist operators and by the senior author at Ningaloo Reef was aimed at addressing these deficiencies. The aims of this study were to determine the size distribution, sex ratio and size at maturity of male R. typus at Ningaloo Reef, Western Australia. 2. Methods 2.1. Length estimates and size at maturity of male whale sharks at Ningaloo Reef Whale shark lengths were estimated to the nearest 0.5 m total length (TL) using a 15 m rope (knotted at 1 m intervals) held underwater alongside the sharks. Some estimates were based on the length of a snorkeller (assumed to be 2 m) swimming alongside the whale shark. All lengths given are TL. The sex of each shark could be determined by diving below the pelvic fins and recording the presence or absence of claspers. Clasper morphology is a reliable and non-invasive means of assessing sexual maturity in male sharks (Joung and Chen, 1995). Claspers are short, soft and smooth in sexually immature individuals, but exhibit accelerated growth and calcification during maturation (McLaughlin and O’Gower, 1971; Bass et al., 1975) and in whale sharks often appear rough and abraded (see
82
B.M. Norman, J.D. Stevens / Fisheries Research 84 (2007) 81–86
loo was determined by subjecting the percentage contributions made to each length class by mature animals to logistic regression analysis, using bootstrapping of 1000 random samples (see Smith et al., 2004). 1 1 + e−ln19(L−L50 )/(L95 −L50 ) where PL is the proportion of R. typus with mature, calcified claspers at length interval L, and L50 and L95 are the lengths at which 50 and 95% of the population are mature.
PL =
3. Results
Fig. 1. Location of whale shark observations during 1995, 1996 and 1997 at Ningaloo Reef in Western Australia.
Fig. 3). Thus, using the external morphology of claspers as an indicator of sexual maturity, male whale sharks were designated as ‘immature’ if the claspers were short, smooth and did not extend beyond the pelvic fins, or ‘mature’ if the claspers were elongated and extended beyond the pelvic fins. In many cases, this latter group had claspers that appeared abraded, some to the extent that they had a ‘cauliflowered’ appearance, possibly as a result of previous sexual activity. The dataset collected by the senior author was supplemented by observations on the length of sharks from industry operators. Between 1995 and 1997, all whale sharks at Ningaloo Reef observed by the operators were recorded in the Western Australian Department of Conservation and Land Management (CALM) Whale Shark Operator Logbooks. However, it was often difficult for these operators to collect data on whale shark sex in addition to undertaking their normal tasks. For this reason, these data were not included in this analysis. The total length at which 50% (L50 ) and 95% (L95 ) (including their 95% confidence limits) of R. typus were mature at Ninga-
Information on the size, sex (and for males) maturity state based on length and/or degree of clasper abrasion of R. typus was collected on 360 separate occasions while aboard commercial vessels throughout the 1995, 1996 and 1997 whale shark seasons at Ningaloo Reef. The location of each in-water interaction with whale sharks is shown in Fig. 1. 3.1. Size structure of whale sharks at Ningaloo Reef During 1995, at Ningaloo Reef, the smallest shark recorded in this study was ∼3 m and the largest was ∼12 m (Table 1; Fig. 2); the mean total length was 7.0 m. The results from tour operators indicate that the size of the sharks in 1995 ranged between 2 and 13 m, with a mean total length of 7.2 m. The recorded length range in 1996 was 4.5–12 m, with a mean of 7.6 m. The industry operators recorded a minimum length of 2 m and a maximum length of 14 m (mean 7.7 m) in the same year. In 1997, the length range recorded was 4–10 m, with a mean of 6.7 m, compared with a range of 2–12 m and mean of 7.0 m recorded by the industry. Overall, the mean total length of R. typus at Ningaloo Reef was 7.3 or 7.4 m as recorded during our surveys or by the industry, respectively (Table 1). The modal length class of whale sharks recorded in this study in 1995 and 1996 was 6–7 m, while in 1997, it was 7–8 m (Fig. 2). Overall, modal lengths of 6–7 m were recorded for both male and
Table 1 Estimated mean total length (±S.E.) and sex ratio of Rhincodon typus at Ningaloo Reef from 1995 to 1997 Year
Mean whale shark length (m)
1995 This study Industry records
7.0 ± 0.2 (n = 125) 7.2 ± 0.1 (n = 361)
3–12 2–13
71.7 (n = 113) –
1996 This study Industry records
7.6 ± 0.1 (n = 177) 7.7 ± 0.1 (n = 858)
4.5–12 2–14
91.6 (n = 154) –
1997 This study Industry records
6.7 ± 0.2 (n = 58) 7.0 ± 0.1 (n = 760)
4–10 2–12
91.4 (n = 58) –
Overall (1995–1997) This study Industry records
7.2 ± 0.1 (n = 360) 7.4 ± 0.04 (n = 1979)
3–12 2–14
84.6 (n = 175) –
In 1995 and 1996, 12 and 23 animals, respectively, were unable to be sexed.
Length range (m)
Percentage males
B.M. Norman, J.D. Stevens / Fisheries Research 84 (2007) 81–86
83
Fig. 2. Length–frequency histograms of whale sharks sighted by the senior author (personal observations) (A) and by industry operators (industry records) (B) at Ningaloo Reef for each year between 1995 and 1997. The sexes are separated in (A) only. Combined data (1995–1997) for (A) and (B) are also presented.
female whale sharks. The pooled length–frequency distribution data from 1995 to 1997 were very similar when compared with data collected by industry operators during this same period (Fig. 2). Between 1995 and 1997, 84.6% of the 325 individual R. typus that could be sexed at Ningaloo were male. There was however, some interannual variation with 71.7% of sexed sharks being identified as male in 1995, compared to 91.6 and 91.4% in 1996 and 1997, respectively (Table 1). Of those whale sharks sighted that could be sexed, the males ranged in length from 4 to 12 m and all whale sharks recorded >9 m were male (Fig. 2). The length range of males was similar in the different years. For example, in 1995, 1996 and 1997 males ranged in length from 4 to 12, 5 to 11 and 4 to 11 m, respectively.
In contrast, the female whale sharks typically ranged from 5 to 7 m in total length, with a small number of 4 and 8 m animals recorded (Fig. 2). 3.2. Length at maturity of male whale sharks The clasper morphology of a total of 275 male whale sharks was visually assessed between 1995 and 1997. Enlarged or abraded claspers were not observed in any shark less than 7 m TL (Fig. 4). However, 9.3% of males in the 7–8 m length class possessed enlarged and sometimes abraded claspers, while over 36% of males in the 8–9 m length class were considered mature (Figs. 3 and 4). Of the 79 male sharks >9 m TL, all but one were considered mature (Fig. 4).
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4. Discussion 4.1. Length range and sex ratio
Fig. 3. Clasper morphology of: (A) an immature and (B) a mature male whale shark.
When the logistic function was fitted to the length at maturity data, it was found that the length at which 50% (L50 ) of male whale sharks were mature was ∼8.1 m TL (95% confidence limits = 7.9–8.2 m TL) (Fig. 4). The length at which 95% (L95 ) of male whale sharks had attained maturity was ∼9.1 m (95% confidence limits = 8.9–9.3 m TL).
Results from our observations indicated that the whale sharks at Ningaloo Reef had a mean TL of 7.0 m in 1995, 7.6 m in 1996 and 6.8 m in 1997. Approximately 40–45% of whale sharks at Ningaloo Reef are between 6 and 8 m in length, with ∼40% above this size (see Fig. 2). This agrees with Taylor (1994) who reports that the whale sharks sighted at Ningaloo Reef are usually between 6.0 and 7.5 m in length, and is also consistent with commercial operators in 1993, where a modal length of sharks sighted was 6–8 m (n = 303) (CALM, unpublished). Most species of sharks form groups that are segregated by size and sex (Klimley, 1987; Bres, 1993). A high level of sexual segregation appears to exist at Ningaloo Reef, with most R. typus recorded as male (∼85%) throughout the present study (i.e. ∼72% in 1995, ∼92% in 1996 and ∼91% in 1997). A similar proportion of male whale sharks was reported in 1993, with 86% of sharks (n = 222) identified as male (CALM, unpublished). While age and growth data on whale sharks are limited, it is thought that they are born at ∼50–60 cm TL (Joung et al., 1996). Chang et al. (1997) reported that under captive conditions the TL of a new-born whale shark increased from 60 to 139 cm over a 120-day period. Based on this rapid early growth in captivity, it seems feasible that whale sharks could attain 2 m by the end of their 1st year and that the smallest specimens (2–4 m) observed at Ningaloo Reef may have been in their first few years of life. A captive whale shark in the Osaka aquarium grew from 4 to almost 8 m TL in 8 years (Wintner, 2000). However based on vertebral growth rings, Wintner (2000) found that a whale shark of ∼5 m (precaudal length) would be approximately 20 years of age. As for most sharks, growth may be rapid in the first few years to enable them to grow quickly through the predation window, after which it slows down. The estimation of growth rates requires careful validation and is best not interpreted from captive specimens. Using improved measuring techniques e.g. underwater lasers, stereophotography etc. to accurately determine TL measurements of identified individual whale sharks, in conjunction with whale shark photo-identification and numerous resightings (Arzoumanian et al., 2005), will aid in the determination of the growth of R. typus in their natural environment. 4.2. Maturity in male whale sharks
Fig. 4. Logistic curve (±95% confidence intervals) reflecting the size at maturity of male whale sharks at Ningaloo Reef.
Our results demonstrate that approximately 85% of all whale sharks sexed at Ningaloo Reef were males. Analysis of data for the 275 males, for which clasper observations were available, indicates that the length at which 50% of male R. typus are mature is ∼8.0 m TL. Using the growth curve in Wintner (2000), R. typus of this length are approximately 30 years of age. Beckley et al. (1997) examined the claspers of 13 male whale sharks (3.90–10.26 m TL) from South Africa and only three had calcified claspers, and each was >9 m TL.
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4.3. Maturity in female whale sharks It is not possible to determine sexual maturity in females by simple external observation. Pai et al. (1983) and Rao (1986) studied two female whale sharks (7.9 and 8.6 m TL) and found these specimens to have immature ovaries. Beckley et al. (1997) examined seven females (∼4.8–8.7 m TL) from the South African coast, finding that all were immature. The only information on a mature female whale shark is from Joung et al. (1996) who reported that a 10.6 m TL shark had approximately 300 near-term embryos ranging in length from 48–64 cm TL. Based on the above data, it is likely that female whale sharks mature at or above a similar length to that reported for males in this study. Since large females and small new-borns are absent from the Ningaloo region, it is possible that breeding females occur in offshore waters where they are not readily observed. Wolfson (1983) reports on seven juvenile whale sharks (0.55–0.93 m) captured in pelagic tuna purse seine fisheries that were operating in water depths greater than 2600 m. Anecdotal reports from whale sharks sighted at the Galapagos Islands have noted very large females with a distended belly region, which may indicate pregnancy (J. Holmberg, Ecocean, Portland, USA, personal communication). It is interesting to note that small whale sharks have only been recorded from the diets of two species, blue marlin (Makaira nigricans) (A. Goorah, Ministry of Fisheries and Marine Resources, Mauritius, personal communication) and oceanic blue sharks (Prionace glauca) (Kukuyev, 1996), two species that generally occur in areas far from land. Initial rapid growth, combined with difficulty in locating small whale sharks, and/or the possibility that breeding grounds are far from Ningaloo Reef may account for the absence of sightings of this group from the study area. This study has helped to confirm that the whale shark aggregation at Ningaloo Reef is related to feeding rather than reproduction. There is a need to determine the population demographics of other aggregations throughout the world and identify both breeding and nursery grounds for this threatened iconic species. Acknowledgements Special thanks to the members of the whale shark ecotourism industry at Ningaloo Marine Park and Christmas Island, Indian Ocean and the Western Australian Department of Conservation and Land Management (CALM) and Parks Australia North for their assistance in data collection throughout this study. Funding was provided from several sources including the above stakeholders and also the Thyne Reid Education Trust, Murdoch University, Shire of Exmouth, the Commonwealth Department of the Environment and Heritage, the Feilman Foundation, Australian Geographic, the Australian Marine Conservation Society, the former Commonwealth Department of Tourism, WA Lotteries Commission, Skywest Airlines Pty Ltd., Greyhound Coachlines, Sundaze (Oakley), Rip Curl, Sherwood SCUBA, Fishcare WA, and the WA Department of Commerce and Trade.
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