Population Connectivity of the Highly Migratory Shortfin Mako (Isurus oxyrinchus Rafinesque 1810) and Implications for Management in the Southern Hemisphere

Copyright © 2018 Corrigan, Lowther, Beheregaray, Bruce, Cliff, Duffy, Foulis, Francis, Goldsworthy, Hyde, Jabado, Kacev, Marshall, Mucientes, Naylor, Pepperell, Queiroz, White, Wintner and Rogers. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.In this paper we combine analyses of satellite telemetry and molecular data to investigate spatial connectivity and genetic structure among populations of shortfin mako (Isurus oxyrinchus) in and around Australian waters, where this species is taken in recreational and commercial fisheries. Mitochondrial DNA data suggest matrilineal substructure across hemispheres, while nuclear DNA data indicate shortfin mako may constitute a globally panmictic population. There was generally high genetic connectivity within Australian waters. Assessing genetic connectivity across the Indian Ocean basin, as well as the extent that shortfin mako exhibit sex biases in dispersal patterns would benefit from future improved sampling of adult size classes, particularly of individuals from the eastern Indian Ocean. Telemetry data indicated that Australasian mako are indeed highly migratory and frequently make long-distance movements. However, individuals also exhibit fidelity to relatively small geographic areas for extended periods. Together these patterns suggest that shortfin mako populations may be genetically homogenous across large geographical areas as a consequence of few reproductively active migrants, although spatial partitioning exists. Given that connectivity appears to occur at different scales, management at both the national and regional levels seems most appropriate

Isurus paucus

<i>Isurus paucus</i> <p> <i>Fresh material</i>: 1 specimen, ERB 0 935, female, 2540 mm TL, 23 July 2008, 40°24’N, 67°23’W, northwest Atlantic Ocean.</p> <p> <i>Additional illustrations</i>: Compagno (1990, figs. 5L, 6L, 7L).</p>Published as part of <i>Mollen, Frederik H., Wintner, Sabine P., Iglésias, Samuel P., Van, Sean R. & Jagt, John W. M., 2012, Comparative morphology of rostral cartilages in extant mackerel sharks (Chondrichthyes, Lamniformes, Lamnidae) using CT scanning, pp. 29-43 in Zootaxa 3340</i> on page 32, DOI: <a href="http://zenodo.org/record/215285">10.5281/zenodo.215285</a&gt

Lamna ditropis

<i>Lamna ditropis</i> <p> <i>Fresh material</i>: 2 specimens, ERB 0 937, female, 900 mm TL, August 2009, beached south of Monterey Bay near San Luis Obispo and Cambria, northeast Pacific Ocean; ERB 0 854 (= NMFS – AFSC –09SS004), female, 2340 mm TL, 2 October 2009, northeast side of Kodiak Island, northeast Pacific Ocean.</p> <p> <i>Additional illustrations</i>: Matsubara (1955, fig. 15A–C), Compagno (1977, fig. 7Q; 1988, fig. 7.1.A; 1990, figs 5M, 6N, 7M (<i>non</i> fig. 6M, mislabelled), Glikman (1980, fig 1.1–2), and Purdy <i>et al.</i> (2001, fig. 32A).</p>Published as part of <i>Mollen, Frederik H., Wintner, Sabine P., Iglésias, Samuel P., Van, Sean R. & Jagt, John W. M., 2012, Comparative morphology of rostral cartilages in extant mackerel sharks (Chondrichthyes, Lamniformes, Lamnidae) using CT scanning, pp. 29-43 in Zootaxa 3340</i> on page 32, DOI: <a href="http://zenodo.org/record/215285">10.5281/zenodo.215285</a&gt

Carcharodon carcharias

<i>Carcharodon carcharias</i> <p> <i>Fresh material</i>: 1 specimen, ERB 0 932 (= KZNSB –UMT 07015), female, 2120 mm TL, 26 November 2007, protective gill nets off Umtentweni, South Africa, southwest Indian Ocean.</p> <p> <i>Additional material</i>: one set of transverse views through rostrum based on CT scans (unpublished data, courtesy of K. Shimada) of a female, FMNH 38335, c. 2714 mm TL (based on crown height of first anterior teeth, following the method described by Shimada 2003), off southern Florida, USA, Atlantic Ocean, and 2 dried chondrocrania, IRScNB 1385γ, no data, Mediterranean; KZNSB unlabelled, female, c. 3740 mm TL (based on skeleton), date unknown, protective gill nets off KwaZulu-Natal, South Africa, southwest Indian Ocean.</p> <p> <i>Additional illustrations</i>: Haswell (1884, pl. 1, figs. 1–2), Parker [1887, pl. 4, figs. 1, 3; pl. 5, unnumbered fig. (upper part of plate only); <i>non</i> pl. 8, figs. 24–25, misidentified by the author, see Francis (1996) and Mollet <i>et al.</i> (2002)], Compagno (1990, figs. 3G, 5J, 6J, 7J), Gottfried <i>et al.</i> (1996, fig. 5B), Wroe <i>et al.</i> (2008, fig. 1A–B), and Shimada <i>et al.</i> (2009, fig. 2D).</p>Published as part of <i>Mollen, Frederik H., Wintner, Sabine P., Iglésias, Samuel P., Van, Sean R. & Jagt, John W. M., 2012, Comparative morphology of rostral cartilages in extant mackerel sharks (Chondrichthyes, Lamniformes, Lamnidae) using CT scanning, pp. 29-43 in Zootaxa 3340</i> on page 31, DOI: <a href="http://zenodo.org/record/215285">10.5281/zenodo.215285</a&gt

Isurus oxyrinchus

<i>Isurus oxyrinchus</i> <p> <i>Fresh material</i>: 2 specimens, ERB 0 933, female, 1940 mm TL, 20 February 2009, Algeciras fish market, Spain, 29°10’N, 15°20’W, northeast Atlantic Ocean; ERB 0 934, sex unknown (said to be male but unverified), 2300 (+/- 100) mm TL, 26 February 2009, Concarneau fish market, France, northeast Atlantic Ocean.</p> <p> <i>Additional material</i>: 3 dried chondrocrania, IRScNB 1384γ, IRScNB 2190 and IRScNB 2190β, juvenile specimens, no data, Nice, France, Mediterranean.</p> <p> <i>Additional illustrations</i>: Matsubara (1955, fig. 15D–F), Glikman (1967, figs. 8–9, 38; 1980, pls 1–4, fig. 2), Compagno (1990, figs. 5K, 6K, 7K), Muñoz-Chápuli & De Andrés (1995, fig. 1C), Compagno (2001, fig. 12A–C), Wilga (2005, fig. 3D), and Shimada <i>et al.</i> (2009, fig. 2C).</p>Published as part of <i>Mollen, Frederik H., Wintner, Sabine P., Iglésias, Samuel P., Van, Sean R. & Jagt, John W. M., 2012, Comparative morphology of rostral cartilages in extant mackerel sharks (Chondrichthyes, Lamniformes, Lamnidae) using CT scanning, pp. 29-43 in Zootaxa 3340</i> on page 31, DOI: <a href="http://zenodo.org/record/215285">10.5281/zenodo.215285</a&gt

Global population genetic dynamics of a highly migratory, apex predator shark

Knowledge of genetic connectivity dynamics in the world\u27s large-bodied, highly migratory, apex predator sharks across their global ranges is limited. One such species, the tiger shark (Galeocerdo cuvier), occurs worldwide in warm temperate and tropical waters, uses remarkably diverse habitats (nearshore to pelagic) and possesses a generalist diet that can structure marine ecosystems through top-down processes. We investigated the phylogeography and the global population structure of this exploited, phylogenetically enigmatic shark by using 10 nuclear microsatellites (n = 380) and sequences from the mitochondrial control region (CR, n = 340) and cytochrome oxidase I gene (n = 100). All three marker classes showed the genetic differentiation between tiger sharks from the western Atlantic and Indo-Pacific ocean basins (microsatellite FST \u3e 0.129; CR ΦST \u3e 0.497), the presence of North vs. southwestern Atlantic differentiation and the isolation of tiger sharks sampled from Hawaii from other surveyed locations. Furthermore, mitochondrial DNA revealed high levels of intraocean basin matrilineal population structure, suggesting female philopatry and sex-biased gene flow. Coalescent- and genetic distance-based estimates of divergence from CR sequences were largely congruent (dcorr = 0.0015–0.0050), indicating a separation of Indo-Pacific and western Atlantic tiger sharks \u3c1 million years ago. Mitochondrial haplotype relationships suggested that the western South Atlantic Ocean was likely a historical connection for interocean basin linkages via the dispersal around South Africa. Together, the results reveal unexpectedly high levels of population structure in a highly migratory, behaviourally generalist, cosmopolitan ocean predator, calling for management and conservation on smaller-than-anticipated spatial scales

Genepop Input File

Microsatellite allele sizes formatted for Genepop

Dual-plot of individual predator (■) and mean (± SD) δ¹³C and δ¹⁵N values of the PP for each predator ((a), (f), (k), (p); see Table 1).

<p>Standard ellipse areas corrected for sample size (SEA_c) of sharks (solid black) and PP functional prey groups (Crustacean, dashed light gray; Mollusk, dotted light gray; Teleost, dashed dark gray; Elasmobranch, solid dark gray; Mammal solid light gray), and the broader diet (dotted black) following Jackson et al. [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0077567#B29" target="_blank">29</a>]. Note different scales on the x- and y-axes in each species.</p

Laser photogrammetry improves size and demographic estimates for whale sharks

Whale sharks Rhincodon typus are globally threatened, but a lack of biological and demographic information hampers an accurate assessment of their vulnerability to further decline or capacity to recover. We used laser photogrammetry at two aggregation sites to obtain more accurate size estimates of free-swimming whale sharks compared to visual estimates, allowing improved estimates of biological parameters. Individual whale sharks ranged from 432-917 cm total length (TL) (mean +/- SD = 673 +/- 118.8 cm, N = 122) in southern Mozambique and from 420-990 cm TL (mean +/- SD = 641 +/- 133 cm, N = 46) in Tanzania. By combining measurements of stranded individuals with photogrammetry measurements of free-swimming sharks, we calculated length at 50% maturity for males in Mozambique at 916 cm TL. Repeat measurements of individual whale sharks measured over periods from 347-1,068 days yielded implausible growth rates, suggesting that the growth increment over this period was not large enough to be detected using laser photogrammetry, and that the method is best applied to estimating growth rates over longer (decadal) time periods. The sex ratio of both populations was biased towards males (74% in Mozambique, 89% in Tanzania), the majority of which were immature (98% in Mozambique, 94% in Tanzania). The population structure for these two aggregations was similar to most other documented whale shark aggregations around the world. Information on small