Discovery of a pupping site and nursery for critically endangered green sawfish Pristis zijsron

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Journal of Fish Biology (2015) 86, 1658 1663 doi:10.1111/jfb.12668, available online at wileyonlinelibrary.com Discovery of a pupping site and nursery for critically endangered green sawfish Pristis zijsron D. L. Morgan*, M. G. Allen*, B. C. Ebner*, J. M. Whitty* and S. J. Beatty* *Freshwater Fish Group & Fish Health Unit, Centre for Fish & Fisheries Research, School of Veterinary & Life Sciences, Murdoch University, Murdoch, WA 6150, Australia, CSIRO, Land and Water Flagship, Maunds Road, Atherton, Qld 4883, Australia and TropWATER, James Cook University, Townsville, Qld 4811, Australia (Received 17 December 2014, Accepted 16 February 2015) A pilot study targeting sawfishes in the southern Pilbara region of Western Australia, which is undergoing a major expansion in human activity, was conducted using gillnets during April and October 2011 in the Ashburton Estuary and adjacent mangrove creeks. Catch per unit effort was greatest in the Ashburton Estuary in October, due to an influx of green sawfish Pristis zijsron pups, and was orders of magnitude higher than previously reported for any Pristidae; the study sites contained P. zijsron up to almost 3 m total length. This study identified the first pupping site for P. zijsron in Western Australia, and the most southerly known nursery area for the species in Australian waters, and is potentially the most important globally. 2015 The Fisheries Society of the British Isles Key words: Ashburton River; endangered species; fish; fishing; mangrove; Pristidae. The Pristidae is a unique family of batoids that has declined globally, and most species are considered to be extirpated in at least some parts of their former range (Simpfendorfer, 2000; Leeney & Poncelet, 2013; Moore, 2014; Fernandez-Carvalho et al., 2014). All species have now been listed as either endangered or critically endangered by the International Union for the Conservation of Nature (Simpfendorfer, 2013). Unfortunately, Pristidae remain poorly understood, with very little known of their ecology, or even their contemporary distribution and habitat use. This is particularly true for the green sawfish Pristis zijsron Bleeker 1851, which is the least studied and largest extant pristid (maximum size 7 m total length, L T ) (Compagno & Last, 1999). The historical range of P. zijsron once included the Indo-West Pacific from South Africa northwards along the east coast of Africa, through the Red Sea, Persian Gulf, south-east Asia, China and Taiwan to Australia, but there are few reliable contemporary records for the species (Dulvy et al., on-line; Moore, 2014). The species is presumed extirpated from the Pacific coast of eastern Australia and the Australian range is poorly reported Author to whom correspondence should be addressed. Tel.: +61 89360 2813; email: fish@murdoch.edu.au 1658 2015 The Fisheries Society of the British Isles

CRITICALLY ENDANGERED PRISTIS ZIJSRON 1659 (Dulvy et al., on-line). Peverell (2005; unpubl. data) reported on 19 individuals that were captured in the Gulf of Carpentaria (Queensland) off the northern Australian coast. Phillips et al. (2011) demonstrated, based on nucleotide sequence variation in a portion of the mitochondrial control region that was extracted from rostra held in various collections, that the species is genetically sub-divided across northern Australia, with significant structure found between the species in the eastern Indian Ocean coast of the Pilbara and southern Kimberley region of Western Australia and the Gulf of Carpentaria. Morgan et al. (2011) speculated that pupping of P. zijsron may be widespread along this north-western Australian coast, and is probably prevalent in the southern Pilbara region. This supposition was based on numerous small (<30 cm total rostral length) P. zijsron rostra from private collections that originated from this area, and from four small individuals (1000 1110 mm L T ) captured by Stevens et al. (2008) in the northern Pilbara. To elucidate the presence and relative abundance of Pristidae in the southern Pilbara, Western Australia, pristids were surveyed during April and October 2011 near the town of Onslow, within and adjacent to the Ashburton River, which flows into the eastern Indian Ocean (Fig. 1). Sampling at the study sites consisted of setting gillnets (100 or 150 mm monofilament stretched mesh, 60 m length) perpendicular to the bank, although the channel within some sites was narrower than 60 m and thus the length of net deployed varied slightly, as it did with tidal influence affecting channel width. Nets were generally set off sandy shores or within mangroves and fished the entire water column including the extreme shallows. A total of 44 net sets soaked for a total of 128 h pooled across all sites and seasons, including 13, 28 and 22 h in Four Mile Creek, Hooley s Creek and the Ashburton Estuary, respectively, in April (late wet season), and 15, 17 and 32 h in those respective localities in October (late dry season). All pristids captured were measured for L T, sexed and fitted with an identification tag using the methods of Thorburn et al. (2007). A total of 39 P. zijsron were captured during the study, including seven males and three females in April, and 14 males and 15 females in October 2011 (Fig. 2). The L T of P. zijsron ranged from 1122 to 2447 mm in April, and from 767 to 2933 mm in October. Fourteen individuals were recaptured at least once during the study, some in different seasons. Several distinct size classes were observed (767 972, 1350 1526 and >1990 mm) in October, whereas, apart from a group of small individuals, there were no clear cohorts of larger-sized individuals in April (Fig. 2). Uncalcified claspers indicated that all the captured males were sexually immature. Most within the smallest cohort in October (i.e. P. zijsron of 767 972 mm L T ) had open or partly healed yolk-sac wounds, with one possessing the remnants of a yolk sac and rostral teeth that had just begun to emerge from the rostral sheath. In April, however, all yolk-sac scars found on the smallest captured individuals were completely healed. Catch per unit effort (CPUE; mean ± s.e.) of P. zijsron in both Four Mile Creek and Hooley s Creek was higher in April (0 121 ± 0 130 and 0 036 ± 0 028 individuals in 20 m net h 1, respectively) than in October (0 075 ± 0 087 and 0 individuals in 20 m net h 1, respectively). In contrast, CPUE in the Ashburton Estuary was higher in October (0 441 ± 0 191 individuals in 20 m net h 1 ) than in April (0 052 ± 0 029 individuals in 20 m net h 1 ). The high CPUE of P. zijsron in the Ashburton Estuary in October was due to recent pupping presumably at, or in close proximity to, the site, with neonates making up almost half the individuals caught at that time.

1660 D. L. MORGANET AL. Western Australia Indian Ocean Hooley s Creek Four Mile Creek Onslow Ashburton Estuary Ashburton River 0 4 5 9 18 km Fig. 1. Sample sites for Pristidae on the southern Pilbara coast of Western Australia near the town of Onslow, including the Ashburton Estuary and two tidal mangrove creeks. This study is the first to confirm that the remote southern Pilbara region of the Australian continent houses a globally threatened pristid, with previous distribution reports being either speculative and based on patchy distributional data (Dulvy et al., on-line), from the location of origin of rostra in private collections (Morgan et al., 2011; Phillips et al., 2011), or from deeper waters as by-catch in commercial fisheries (P. Stephenson & J. Chidlow, unpubl. data). The captures represent the majority (58%) of all published records of whole specimens of P. zijsron from the eastern Indian Ocean coast of Australia (Morgan et al., 2011). Heupel et al. (2007) defined an elasmobranch nursery area as: (1) an area in which sharks (used in a general sense) are more common than in surrounding areas,

CRITICALLY ENDANGERED PRISTIS ZIJSRON 1661 10 (a) 8 6 4 2 Number 0 10 (b) 8 6 4 2 0 0 200 400 600 800 1000 1200 1400 L T (mm) 1600 1800 2000 2200 2400 2600 2800 3000 Fig. 2. Total length (L T )-frequency histograms of the Pristis zijsron captured in the study region during (a) April and (b) October 2011. (2) an area in which sharks remain or frequently visit and (3) an area that is used during successive years. Following Heupel et al. s (2007) definition, the presence of immature P. zijsron in the Ashburton Estuary and the surrounding tidal mangrove creeks suggests that these habitats act as a nursery for the species. In April, the size classes were less distinct, with the individuals measuring from 1122 to at least 1317 mm L T probably being older representatives of the 0+ year age class (S. C. Peverell, unpubl. data). The largest individual recorded during the study was a 2933 mm L T immature male. Pristis zijsron is thought to mature at c. 3000 mm L T (Last & Stevens, 2009), but there are no data to substantiate this claim. This study therefore suggests that the Ashburton Estuary houses all early life-history stages of P. zijsron, from neonates to sub-adults. Although the juvenile nursery habitats in Western Australia are not subjected to commercial fishing, sub-adults and adults that move into deeper waters of the Pilbara are captured in the Pilbara fish trawl fishery with records indicating that 4 t of the species were caught in 2001 (P. Stephenson & J. Chidlow, unpubl. data). Similarly, in

1662 D. L. MORGANET AL. the northern Pilbara, it was estimated that between 2000 and 2004, P. zijsron as trawl fishery by-catch ranged from 5 3 to9 6 t (McAuley et al., 2005). The location of pupping grounds and nursery habitats of nearshore elasmobranch species is a crucial knowledge gap hindering effective conservation planning, especially in areas that are heavily affected by anthropogenic disturbances. Kinney & Simpfendorfer (2009) suggest, however, that in the absence of management of older juveniles and mature individuals that typically live outside of such nursery areas, a well-managed and well-protected nursery area may have little direct benefit to the overall conservation of the species. Therefore, further exploration of the wider region should be conducted to identify key adult habitats as well as other nurseries for the species in order to better inform conservation planning and management. This project was funded by Chevron Australia Pty Ltd. Technical and logistical support was provided by URS. We express gratitude for the tremendous assistance given to the project by J. Keleher (Murdoch University), M. Fraser and T. Hurley (URS), G. Young, T. Rouphael, N. Page, S. Moore and C. Morgan (Chevron) and G. Herbert and A. Slater (Scubaroo Dive). This work was conducted under permits from the Department of Fisheries, Department of Environment and Conservation, the Department of Transport and the Murdoch University Animal Ethics Committee. References Compagno, L. J. V. & Last, P. R. (1999). Pristidae. Sawfishes. In FAO Identification Guide for Fishery Purposes. The Living Marine Resources of the Western Central Pacific (Carpenter, K. E. & Niem, V., eds), pp. 1410 1417. Rome: FAO. Dulvy, N. K., Davidson, L. N. K., Kyne, P. M., Simpfendorfer, C. A., Harrison, L. R., Carlson, J. K. & Fordham, S. V. (On-line). Ghosts of the coast: global extinction risk and conservation of sawfishes. Aquatic Conservation: Marine and Freshwater Ecosystems. doi: 10.1002/aqc.2525. Fernandez-Carvalho, J., Imhoff, J. L., Faria, V. V., Carlson, J. K. & Burgess, G. H. (2014). Status and the potential for extinction of the largetooth sawfish Pristis pristis in the Atlantic Ocean. Aquatic Conservation: Marine and Freshwater Ecosystems 24,478 497. doi: 10.1002/aqc.2394. Heupel, M. R., Carlson, J. K. & Simpfendorfer, C. A. (2007). Shark nursery areas: concepts, definition, characterization and assumptions. Marine Ecology Progress Series 337, 287 297. Kinney, M. J. & Simpfendorfer, C. A. (2009). Reassessing the value of nursery areas to shark conservation and management. Conservation Letters 2, 53 60. Last, P. R. & Stevens, J. D. (2009). Sharks and Rays of Australia. Collingwood: CSIRO Publishing. Leeney, R. H. & Poncelet, P. (2013). Using fishers ecological knowledge to assess the status and cultural importance of sawfish in Guinea-Bissau. Aquatic Conservation: Marine and Freshwater Ecosystems. 10.1002/aqc.2419. Moore, A. B. M. (2014). A review of sawfishes (Pristidae) in the Arabian region: diversity, distribution, and functional extinction of large and historically abundant marine vertebrates. Aquatic Conservation: Marine and Freshwater Ecosystems. doi: 10.1002/aqc.2441 Morgan, D. L., Whitty, J. M., Phillips, N. M., Thorburn, D. C., Chaplin, J. A. & McAuley, R. (2011). North-western Australia as a hotspot for endangered elasmobranchs, with particular reference to sawfishes and the Northern River Shark. Journal of the Royal Society of Western Australia 94, 345 358. Peverell, S. C. (2005). Distribution of sawfishes (Pristidae) in the Queensland Gulf of Carpentatria, Australia, with notes on sawfish ecology. Environmental Biology of Fishes 73, 391 402. Phillips, N. M., Chaplin, J. A., Morgan, D. L. & Peverell, S. C. (2011). Population genetic structure and genetic diversity of three critically endangered Pristis sawfishes in Australian waters. Marine Biology 158, 903 915.

CRITICALLY ENDANGERED PRISTIS ZIJSRON 1663 Simpfendorfer, C. A. (2000). Predicting population recovery rates for endangered western Atlantic sawfishes using demographic analysis. Environmental Biology of Fishes 58, 371 377. Thorburn, D. C., Morgan, D. L., Rowland, A. J. & Gill, H. S. (2007). Freshwater Sawfish Pristis microdon Latham, 1794 (Chondrichthyes : Pristidae) in the Kimberley region of Western Australia. Zootaxa 1471, 27 41. Electronic References McAuley, R., Lenanton, R., Chidlow, J., Allison, R. & Heist, E. (2005). Biology and stock assessment of the thickskin (sandbar) shark, Carcharhinus plumbeus, in Western Australia and further refinement of the dusky shark, Carcharhinus obscurus, stock assessment, Final FRDC Report Project 2000/134. Fisheries Research Report No. 151. Available at http://www.fisheries.wa.gov.au/documents/research_reports/frr151.pdf/ Simpfendorfer, C. (2013). Pristis zijsron. The IUCN Red List of Threatened Species. Version 2014.3. Available at http://www.iucnredlist.org/details/39393/0 (accessed on 20 December 2014). Stevens, J. D., McAuley, R. B., Simpfendorfer, C. A. & Pillans, R. D. (2008). Spatial Distribution and Habitat Utilisation of Sawfish (Pristis spp) in Relation to Fishing in Northern Australia. A Report to the Department of the Environment, Water, Heritage and the Arts. CSIRO and Western Australia Department of Fisheries. Available at http://www.environment.gov.au/coasts/publications/pubs/sawfish-report.pdf/