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RESEARCH ARTICLE

Comparing length-measurement methods and estimating growth parameters of free-swimming whale sharks (Rhincodon typus) near the South Ari Atoll, Maldives

Cameron T. Perry orcid.org/0000-0001-5254-581X A B C D , Joana Figueiredo C , Jeremy J. Vaudo A C , James Hancock B , Richard Rees B and Mahmood Shivji A C
+ Author Affiliations
- Author Affiliations

A Guy Harvey Research Institute, Nova Southeastern University, 8000 N Ocean Drive, Dania Beach, FL 33004, USA.

B Maldives Whale Shark Research Programme, Popeshead Court Offices, Peter Lane, York, Yorkshire, Y01 8SU, UK.

C Halmos College of Natural Sciences and Oceanography, Nova Southeastern University, 8000 N Ocean Drive, Dania Beach, FL 33004, USA.

D Corresponding author. Email: cameron@maldiveswhalesharkresearch.org

Marine and Freshwater Research 69(10) 1487-1495 https://doi.org/10.1071/MF17393
Submitted: 22 December 2017  Accepted: 4 April 2018   Published: 9 July 2018

Abstract

Whale sharks (Rhincodon typus) are an endangered species whose growth and reproductive biology are poorly understood. Given their conservation concern, estimating growth parameters, as traditionally derived from vertebral samples of dead animals, is challenging. We used a non-invasive approach to investigate growth parameters of whale sharks frequenting the South Ari Atoll, Maldives, by analysing repeat measurements of free-swimming sharks over a 10-year period. Total lengths of the sharks were estimated by three measurement methods. Visual estimates underestimated the sizes of large sharks, whereas laser and tape measurements yielded results that were similar to one another. The Maldives aggregation consisted of primarily male (91%) juvenile (total length = 3.16–8.00 m) sharks and sharks new to the area were significantly smaller than were returning sharks, which suggests that this site may constitute a secondary nursery ground. Estimates of von Bertalanffy (VBG) growth parameters for combined sexes (L = 19.6 m, k = 0.021 year–1) were calculated from 186 encounters with 44 sharks. For males, VBG parameters (L = 18.1 m, k = 0.023 year–1) were calculated from 177 encounters with 40 sharks and correspond to a male age at maturity of ~25 years and longevity of ~130 years. Differences between these estimates and those from other studies underscore the need for regional studies.

Additional keywords: age estimation, age and growth, elasmobranch, growth rates, laser photogrammetry, von Bertalanffy.


References

Arzoumanian, Z., Holmberg, J., and Norman, B. (2005). An astronomical pattern‐matching algorithm for computer‐aided identification of whale sharks Rhincodon typus. Journal of Applied Ecology 42, 999–1011.
An astronomical pattern‐matching algorithm for computer‐aided identification of whale sharks Rhincodon typus.Crossref | GoogleScholarGoogle Scholar |

Barker, S. M., and Williamson, J. E. (2010). Collaborative photo-identification and monitoring of grey nurse sharks (Carcharias taurus) at key aggregation sites along the eastern coast of Australia. Marine and Freshwater Research 61, 971–979.
Collaborative photo-identification and monitoring of grey nurse sharks (Carcharias taurus) at key aggregation sites along the eastern coast of Australia.Crossref | GoogleScholarGoogle Scholar |

Bass, A. (1978). Problems in studies of sharks in the southwest Indian Ocean. In ‘Sensory Biology of Sharks, Skates, and Rays’. (Eds E. Hodgson and R. Mathewson.) pp. 545–594. (Department of the Navy, Office of Naval Research: Arlington, VA, USA.)

Borrell, A., Aguilar, A., Gazo, M., Kumarran, R., and Cardona, L. (2011). Stable isotope profiles in whale shark (Rhincodon typus) suggest segregation and dissimilarities in the diet depending on sex and size. Environmental Biology of Fishes 92, 559–567.
Stable isotope profiles in whale shark (Rhincodon typus) suggest segregation and dissimilarities in the diet depending on sex and size.Crossref | GoogleScholarGoogle Scholar |

Brooks, K., Rowat, D., Pierce, S. J., Jouannet, D., and Vely, M. (2010). Seeing spots: photo-identification as a regional tool for whale shark identification. Western Indian Ocean Journal of Marine Science 9, 185–194.

Brunnschweiler, J. M., and Baensch, H. (2011). Seasonal and long-term changes in relative abundance of bull sharks from a tourist shark feeding site in Fiji. PLoS One 6, e16597.
Seasonal and long-term changes in relative abundance of bull sharks from a tourist shark feeding site in Fiji.Crossref | GoogleScholarGoogle Scholar |

Cagua, E. F., Collins, N., Hancock, J., and Rees, R. (2014). Whale shark economics: a valuation of wildlife tourism in South Ari Atoll, Maldives. PeerJ 2, e515.
Whale shark economics: a valuation of wildlife tourism in South Ari Atoll, Maldives.Crossref | GoogleScholarGoogle Scholar |

Chang, W. B., Leu, M. Y., and Fang, L. J. (1997). Embryos of the whale shark, Rhincodon typus: early growth and size distribution. Copeia 1997, 444–446.
Embryos of the whale shark, Rhincodon typus: early growth and size distribution.Crossref | GoogleScholarGoogle Scholar |

Chen, C. T., Liu, K. M., and Joung, S. J. (1997). Preliminary report on Taiwan’s whale shark fishery. Traffic Bulletin 17, 1–5.

Deakos, M. H. (2010). Paired-laser photogrammetry as a simple and accurate system for measuring the body size of free-ranging manta rays Manta alfredi. Aquatic Biology 10, 1–10.
Paired-laser photogrammetry as a simple and accurate system for measuring the body size of free-ranging manta rays Manta alfredi.Crossref | GoogleScholarGoogle Scholar |

Delacy, C. R., Olsen, A., Howey, L. A., Chapman, D. D., Brooks, E. J., and Bond, M. E. (2017). Affordable and accurate stereo-video system for measuring dimensions underwater: a case study using oceanic whitetip sharks Carcharhinus longimanus. Marine Ecology Progress Series 574, 75–84.
Affordable and accurate stereo-video system for measuring dimensions underwater: a case study using oceanic whitetip sharks Carcharhinus longimanus.Crossref | GoogleScholarGoogle Scholar |

Domeier, M. L., and Nasby-Lucas, N. (2007). Annual re-sightings of photographically identified white sharks (Carcharodon carcharias) at an eastern Pacific aggregation site (Guadalupe Island, Mexico). Marine Biology 150, 977–984.
Annual re-sightings of photographically identified white sharks (Carcharodon carcharias) at an eastern Pacific aggregation site (Guadalupe Island, Mexico).Crossref | GoogleScholarGoogle Scholar |

Dudgeon, C. L., Noad, M. J., and Lanyon, J. M. (2008). Abundance and demography of a seasonal aggregation of zebra sharks Stegostoma fasciatum. Marine Ecology Progress Series 368, 269–281.
Abundance and demography of a seasonal aggregation of zebra sharks Stegostoma fasciatum.Crossref | GoogleScholarGoogle Scholar |

Fox, S., Foisy, I., De La Parra Venegas, R., Galván Pastoriza, B., Graham, R., Hoffmayer, E., Holmberg, J., and Pierce, S. (2013). Population structure and residency of whale sharks Rhincodon typus at Utila, Bay Islands, Honduras. Journal of Fish Biology 83, 574–587.
Population structure and residency of whale sharks Rhincodon typus at Utila, Bay Islands, Honduras.Crossref | GoogleScholarGoogle Scholar |

Gallucci, V. F., Taylor, I. G., and Erzini, K. (2006). Conservation and management of exploited shark populations based on reproductive value. Canadian Journal of Fisheries and Aquatic Sciences 63, 931–942.
Conservation and management of exploited shark populations based on reproductive value.Crossref | GoogleScholarGoogle Scholar |

Goldman, K. J., Cailliet, G. M., Andrews, A. H., and Natanson, L. J. (2012). Assessing the age and growth of chondrichthyan fishes. In ‘Biology of Sharks and their Relatives’. (Eds J. Carrier, J. Musick, and M. Heithaus) pp. 423–448. (CRC Press: Boca Raton, FL, USA.)

Harry, A. V. (2018). Evidence for systemic age underestimation in shark and ray ageing studies. Fish and Fisheries 19, 185–200.
Evidence for systemic age underestimation in shark and ray ageing studies.Crossref | GoogleScholarGoogle Scholar |

Hart, D. R., and Chute, A. S. (2009). Estimating von Bertalanffy growth parameters from growth increment data using a linear mixed-effects model, with an application to the sea scallop Placopecten magellanicus. ICES Journal of Marine Science 66, 2165–2175.
Estimating von Bertalanffy growth parameters from growth increment data using a linear mixed-effects model, with an application to the sea scallop Placopecten magellanicus.Crossref | GoogleScholarGoogle Scholar |

Heupel, M. R., Carlson, J. K., and Simpfendorfer, C. A. (2007). Shark nursery areas: concepts, definition, characterization and assumptions. Marine Ecology Progress Series 337, 287–297.
Shark nursery areas: concepts, definition, characterization and assumptions.Crossref | GoogleScholarGoogle Scholar |

Holmberg, J., Norman, B., and Arzoumanian, Z. (2009). Estimating population size, structure, and residency time for whale sharks Rhincodon typus through collaborative photo-identification. Endangered Species Research 7, 39–53.
Estimating population size, structure, and residency time for whale sharks Rhincodon typus through collaborative photo-identification.Crossref | GoogleScholarGoogle Scholar |

Hsu, H., Joung, S., and Liu, K. (2012). Fisheries, management and conservation of the whale shark Rhincodon typus in Taiwan. Journal of Fish Biology 80, 1595–1607.
Fisheries, management and conservation of the whale shark Rhincodon typus in Taiwan.Crossref | GoogleScholarGoogle Scholar |

Hsu, H. H., Leu, M. Y., Wang, W. H., Hsieh, T. C., and Joung, S. J. (2013). Tagging and release of a captive whale shark after eight years in Taiwan’s aquarium: a case study. Taiwan Shuichanxue Hui Kan 40, 143–151.

Hsu, H. H., Joung, S. J., Hueter, R. E., and Liu, K. M. (2014). Age and growth of the whale shark (Rhincodon typus) in the north-western Pacific. Marine and Freshwater Research 65, 1145–1154.
Age and growth of the whale shark (Rhincodon typus) in the north-western Pacific.Crossref | GoogleScholarGoogle Scholar |

Huveneers, C., Stead, J., Bennett, M. B., Lee, K. A., and Harcourt, R. G. (2013). Age and growth determination of three sympatric wobbegong sharks: how reliable is growth band periodicity in Orectolobidae? Fisheries Research 147, 413–425.
Age and growth determination of three sympatric wobbegong sharks: how reliable is growth band periodicity in Orectolobidae?Crossref | GoogleScholarGoogle Scholar |

Jeffreys, G., Rowat, D., Marshall, H., and Brooks, K. (2013). The development of robust morphometric indices from accurate and precise measurements of free-swimming whale sharks using laser photogrammetry. Journal of the Marine Biological Association of the United Kingdom 93, 309–320.
The development of robust morphometric indices from accurate and precise measurements of free-swimming whale sharks using laser photogrammetry.Crossref | GoogleScholarGoogle Scholar |

Joung, S.-J., Chen, C.-T., Clark, E., Uchida, S., and Huang, W. Y. (1996). The whale shark, Rhincodon typus, is a livebearer: 300 embryos found in one ‘megamamma’ supreme. Environmental Biology of Fishes 46, 219–223.
The whale shark, Rhincodon typus, is a livebearer: 300 embryos found in one ‘megamamma’ supreme.Crossref | GoogleScholarGoogle Scholar |

Ketchum, J. T., Galván-Magaña, F., and Klimley, A. P. (2013). Segregation and foraging ecology of whale sharks, Rhincodon typus, in the southwestern Gulf of California. Environmental Biology of Fishes 96, 779–795.
Segregation and foraging ecology of whale sharks, Rhincodon typus, in the southwestern Gulf of California.Crossref | GoogleScholarGoogle Scholar |

Kinney, M. J., and Simpfendorfer, C. A. (2009). Reassessing the value of nursery areas to shark conservation and management. Conservation Letters 2, 53–60.
Reassessing the value of nursery areas to shark conservation and management.Crossref | GoogleScholarGoogle Scholar |

Kitafuji, M., and Yamamoto, K. (1998). Rearing of the whale shark, Rhincodon typus, in the Osaka aquarium ‘Kaiyukan’. Journal of Japanese Association of Zoological Gardens and Aquariums 39, 47–54.

Marshall, A., and Pierce, S. (2012). The use and abuse of photographic identification in sharks and rays. Journal of Fish Biology 80, 1361–1379.
The use and abuse of photographic identification in sharks and rays.Crossref | GoogleScholarGoogle Scholar |

McClain, C. R., Balk, M. A., Benfield, M. C., Branch, T. A., Chen, C., Cosgrove, J., Dove, A. D., Gaskins, L. C., Helm, R. R., and Hochberg, F. G. (2015). Sizing ocean giants: patterns of intraspecific size variation in marine megafauna. PeerJ 3, e715.
Sizing ocean giants: patterns of intraspecific size variation in marine megafauna.Crossref | GoogleScholarGoogle Scholar |

McGuinness, K. A. (2002). Of rowing boats, ocean liners and tests of the ANOVA homogeneity of variance assumption. Austral Ecology 27, 681–688.
Of rowing boats, ocean liners and tests of the ANOVA homogeneity of variance assumption.Crossref | GoogleScholarGoogle Scholar |

Mohan, P. J., Clark, S. T., and Schmid, T. H. (2004). Age and growth of captive sharks. In ‘The Elasmobranch Husbandry Manual: Captive Care of Sharks, Rays and their Relatives’. (Eds M. Smith, D. Warmolts, D. Thoney, and R. Hueter.) pp. 201–226. (Ohio Biological Survey: Columbus, OH, USA.)

Natanson, L. J., Wintner, S. P., Johansson, F., Piercy, A., Campbell, P., De Maddalena, A., Gulak, S. J., Human, B., Fulgosi, F. C., and Ebert, D. A. (2008). Ontogenetic vertebral growth patterns in the basking shark Cetorhinus maximus. Marine Ecology Progress Series 361, 267–278.
Ontogenetic vertebral growth patterns in the basking shark Cetorhinus maximus.Crossref | GoogleScholarGoogle Scholar |

Norman, B. M., and Morgan, D. L. (2016). The return of ‘Stumpy’ the whale shark: two decades and counting. Frontiers in Ecology and the Environment 14, 449–450.
The return of ‘Stumpy’ the whale shark: two decades and counting.Crossref | GoogleScholarGoogle Scholar |

Norman, B. M., and Stevens, J. D. (2007). Size and maturity status of the whale shark (Rhincodon typus) at Ningaloo Reef in Western Australia. Fisheries Research 84, 81–86.
Size and maturity status of the whale shark (Rhincodon typus) at Ningaloo Reef in Western Australia.Crossref | GoogleScholarGoogle Scholar |

Norman, B. M., Holmberg, J. A., Arzoumanian, Z., Reynolds, S. D., Wilson, R. P., Rob, D., Pierce, S. J., Gleiss, A. C., de la Parra, R., Galvan, B., Ramírez-Macias, D., Robinson, D., Fox, S., Graham, R., Rowat, D., Potenski, M., Levine, M., McKinney, J. A., Hoffmayer, E., Dove, A. D. M., Hueter, R., Ponzo, A., Araujo, G., Aca, E., David, D., Rees, R., Duncan, A., Rohner, C. A., Prebble, C. E. M., Hearn, A., Acuna, D., Berumen, M. L., Vázquez, A., Green, J., Bach, S. S., Schmidt, J. V., Beatty, S. J., and Morgan, D. L. (2017). Undersea constellations: the global biology of an endangered marine megavertebrate further informed through citizen science. Bioscience 67, 1029–1043.
Undersea constellations: the global biology of an endangered marine megavertebrate further informed through citizen science.Crossref | GoogleScholarGoogle Scholar |

Pierce, S. J., and Norman, B. (2016). Rhincodon typus. In ‘The IUCN Red List of Threatened Species 2016’, e.T19488A2365291. Available at http://www.iucnredlist.org/details/19488/0 [Verified 16 May 2018].

Pravin, P. (2000). Whale shark in the Indian coast-need for conservation. Current Science 79, 310–315.

Quinn, T. J., and Deriso, R. B. (1999). ‘Quantitative Fish Dynamics.’ (Oxford University Press: New York, NY, USA.)

Ramírez-Macías, D., Queiroz, N., Pierce, S. J., Humphries, N. E., Sims, D. W., and Brunnschweiler, J. M. (2017). Oceanic adults, coastal juveniles: tracking the habitat use of whale sharks off the Pacific coast of Mexico. PeerJ 5, e3271.
Oceanic adults, coastal juveniles: tracking the habitat use of whale sharks off the Pacific coast of Mexico.Crossref | GoogleScholarGoogle Scholar |

Riley, M. J., Hale, M. S., Harman, A., and Rees, R. G. (2010). Analysis of whale shark Rhincodon typus aggregations near South Ari atoll, Maldives Archipelago. Aquatic Biology 8, 145–150.
Analysis of whale shark Rhincodon typus aggregations near South Ari atoll, Maldives Archipelago.Crossref | GoogleScholarGoogle Scholar |

Rogers, T. D., Cambiè, G., and Kaiser, M. J. (2017). Determination of size, sex and maturity stage of free swimming catsharks using laser photogrammetry. Marine Biology 164, 213.
Determination of size, sex and maturity stage of free swimming catsharks using laser photogrammetry.Crossref | GoogleScholarGoogle Scholar |

Rohner, C. A., Richardson, A., Marshall, A., Weeks, S., and Pierce, S. (2011). How large is the world’s largest fish? Measuring whale sharks Rhincodon typus with laser photogrammetry. Journal of Fish Biology 78, 378–385.
How large is the world’s largest fish? Measuring whale sharks Rhincodon typus with laser photogrammetry.Crossref | GoogleScholarGoogle Scholar |

Rohner, C. A., Couturier, L. I., Richardson, A. J., Pierce, S. J., Prebble, C. E., Gibbons, M. J., and Nichols, P. D. (2013). Diet of whale sharks Rhincodon typus inferred from stomach content and signature fatty acid analyses. Marine Ecology Progress Series 493, 219–235.
Diet of whale sharks Rhincodon typus inferred from stomach content and signature fatty acid analyses.Crossref | GoogleScholarGoogle Scholar |

Rohner, C. A., Richardson, A. J., Prebble, C. E., Marshall, A. D., Bennett, M. B., Weeks, S. J., Cliff, G., Wintner, S. P., and Pierce, S. J. (2015). Laser photogrammetry improves size and demographic estimates for whale sharks. PeerJ 3, e886.
Laser photogrammetry improves size and demographic estimates for whale sharks.Crossref | GoogleScholarGoogle Scholar |

Rowat, D., and Brooks, K. (2012). A review of the biology, fisheries and conservation of the whale shark Rhincodon typus. Journal of Fish Biology 80, 1019–1056.
A review of the biology, fisheries and conservation of the whale shark Rhincodon typus.Crossref | GoogleScholarGoogle Scholar |

Sequeira, A. M., Thums, M., Brooks, K., and Meekan, M. G. (2016). Error and bias in size estimates of whale sharks: implications for understanding demography. Royal Society Open Science 3, 150668.
Error and bias in size estimates of whale sharks: implications for understanding demography.Crossref | GoogleScholarGoogle Scholar |

Shortis, M. (2015). Calibration techniques for accurate measurements by underwater camera systems. Sensors 15, 30810–30826.
Calibration techniques for accurate measurements by underwater camera systems.Crossref | GoogleScholarGoogle Scholar |

Taylor, C. C. (1958). Cod growth and temperature. ICES Journal of Marine Science 23, 366–370.
Cod growth and temperature.Crossref | GoogleScholarGoogle Scholar |

Uchida, S., Toda, M., Kamei, Y., and Teruya, H. (2000). The husbandry of 16 whale sharks Rhincodon typus, from 1980 to 1998 at the Okinawa expo aquarium. In ‘Abstracts of the American Elasmobranch Society 16th Annual Meeting’, La Paz, Mexico, 14–20 June 2000. p. 359. (American Elasmobranch Society: La Paz, Mexico.)

Van Tienhoven, A., Den Hartog, J., Reijns, R., and Peddemors, V. (2007). A computer‐aided program for pattern‐matching of natural marks on the spotted raggedtooth shark Carcharias taurus. Journal of Applied Ecology 44, 273–280.
A computer‐aided program for pattern‐matching of natural marks on the spotted raggedtooth shark Carcharias taurus.Crossref | GoogleScholarGoogle Scholar |

Wintner, S. P. (2000). Preliminary study of vertebral growth rings in the whale shark, Rhincodon typus, from the east coast of South Africa. Environmental Biology of Fishes 59, 441–451.
Preliminary study of vertebral growth rings in the whale shark, Rhincodon typus, from the east coast of South Africa.Crossref | GoogleScholarGoogle Scholar |

Zar, J. (1984). ‘Biostatistical Analyses’, 2nd edn. (Prentice-Hall: Englewood Cliffs, NJ, USA.)