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Grant Kyne Categorising Use Patterns of Non https://link.springer.com/article/10.1007%2Fs11160-019-09576-w POSTPRINT or read published version online https://rdcu.be/bRuYx provided by the Springer Nature SharedIt content-sharing initiative. 1 Running Title: 2 Non-marine elasmobranchs review 3 4 Categorising use patterns of non-marine environments by elasmobranchs and a review of their 5 extinction risk 6 7 Michael I. Grant1*, Peter M. Kyne2, Colin A. Simpfendorfer1, William T. White3,4 and 8 Andrew Chin1 9 10 1Centre for Sustainable Tropical Fisheries and Aquaculture and College of Science and 11 Engineering, James Cook University, 1 James Cook Drive, Townsville, Qld 4811, Australia. 12 2Research Institute for the Environment and Livelihoods, Charles Darwin University, 13 Ellengowan Drive, Darwin 0909, Northern Territory, Australia. 14 3CSIRO Oceans and Atmosphere, 3–4 Castray Esplanade, Hobart, Tas. 7004, Australia. 15 4 Australian National Fish Collection, CSIRO National Research Collections Australia, 16 Hobart, Tas. 7004, Australia. 17 *Corresponding author: [email protected] 18 19 Acknowledgements: 20 The authors wish to extend their thanks to Stacy Beirwagon for valuable assistance with 21 producing maps for this manuscript. We also thank the Save Our Seas Foundation for their 22 ongoing support of our research. MIG was supported by an Australian Post Graduate Award, 23 and PMK was supported by the Shark Conservation Fund, and the Marine Biodiversity Hub, a 24 collaborative partnership supported through funding from the Australian Government's 25 National Environmental Science Program. Finally, we thank three anonymous reviewers for 26 their helpful comments on this MS. 27 https://www.nespmarine.edu.au/document/categorising-use-patterns-non- 1 marine-environments-elasmobranchs-and-review-their-extinction https://link.springer.com/article/10.1007%2Fs11160-019-09576-w POSTPRINT or read published version online https://rdcu.be/bRuYx provided by the Springer Nature SharedIt content-sharing initiative. 28 Abstract 29 As the state of non-marine aquatic environments (freshwater and estuarine 30 environments with salinities ≤ 30 ppt) continues to decline globally, there is increasing concern 31 for elasmobranchs (sharks and rays) that use them at critical stages of their life history. Due to 32 a range of impediments including unresolved taxonomy, lack of fisheries data, and poor public 33 perception, our knowledge of elasmobranchs in non-marine environments has lagged behind 34 marine species. Here, we refine previous categorisations of elasmobranchs that occur in non- 35 marine environments by reviewing the timing and duration of freshwater (≤ 5ppt) and/or 36 estuarine (>5 to ≤ 30 ppt) habitat use throughout each species’ life history. We identified five 37 categories describing elasmobranchs in non-marine environments: 1) freshwater obligates (43 38 spp.); 2) euryhaline generalists (10 spp.); 3) estuarine generalists (19 spp.); 4) non-marine 39 transients; 5) non-marine vagrants. Criteria for species inclusion is provided for all categories, 40 and species lists are presented for categories 1–3. Euryhaline and estuarine generalists had the 41 highest number of species that are threatened with extinction on the IUCN Red List of 42 Threatened Species (50% and 65%, respectively), and freshwater obligate species have a very 43 high portion of Data Deficient and Not Evaluated species (77%). The refinement of non-marine 44 elasmobranch categories will aid in our understanding of elasmobranchs that occur in non- 45 marine environments, helping facilitate more strategic conservation and management 46 initiatives. Research on the biology of elasmobranchs and their human interactions in non- 47 marine environments are suggested, as this will lead to better availability of information for 48 conservation and management. 49 50 Key words: Conservation; Elasmobranchs; Estuaries; Euryhaline; Freshwater; Management 51 52 53 54 https://www.nespmarine.edu.au/document/categorising-use-patterns-non- 2 marine-environments-elasmobranchs-and-review-their-extinction https://link.springer.com/article/10.1007%2Fs11160-019-09576-w POSTPRINT or read published version online https://rdcu.be/bRuYx provided by the Springer Nature SharedIt content-sharing initiative. 55 56 Introduction 57 Elasmobranchs (sharks and rays) that use non-marine environments (salinities < 30 ppt, 58 McLusky 1993) during critical stages of their life history are one of the most poorly understood 59 and threatened groups of vertebrates (Compagno and Cook 1995; Dulvy et al. 2014). 60 Elasmobranchs occurring in these environments may be obligate freshwater species or 61 euryhaline species (Lucifora et al. 2015). Approximately 56 (~5%) of all elasmobranch species 62 are known to regularly occur in low salinity environments (Lucifora et al. 2015). Most of these 63 species are rays from the families Potamotrygonidae (neotropical stingrays) and Dasyatidae 64 (stingrays) that reside exclusively in freshwater throughout their entire life history. Meanwhile, 65 only a few elasmobranchs are euryhaline, able to transition between marine and freshwater 66 environments for prolonged periods e.g. bull shark (Carcharhinus leucas) and largetooth 67 sawfish (Pristis pristis). Almost all freshwater and euryhaline elasmobranchs occur across 68 tropical latitudes with a few species also extending marginally into temperate zones such as C. 69 leucas and green sawfish (Pristis zijsron), while the Maugean skate (Zearaja maugeana) occurs 70 exclusively in temperate waters of Tasmania, Southeastern Australia (Compagno 2002; 71 Compagno and Cook 1995). 72 73 With most elasmobranchs that use non-marine environments occurring in tropical latitudes, 74 they have been exposed to a range of anthropogenic pressures associated with the higher levels 75 of human population growth in tropical regions (Collen et al. 2014; Smith 2003). Fisheries 76 pressure (mostly commercial but also artisanal and recreational) is the primary threat to 77 elasmobranchs in freshwater and estuarine environments (Kyne and Feutry 2017; Lucifora et 78 al. 2015; Lucifora et al. 2017). River engineering, habitat destruction, and pollution also pose 79 considerably greater threat to elasmobranchs in non-marine environments, compared to species 80 that use only marine environments (Compagno and Cook 1995; Dulvy et al. 2014; Lucifora et 81 al. 2016; White and Kyne 2010). Elasmobranchs are inherently susceptible to population https://www.nespmarine.edu.au/document/categorising-use-patterns-non- 3 marine-environments-elasmobranchs-and-review-their-extinction https://link.springer.com/article/10.1007%2Fs11160-019-09576-w POSTPRINT or read published version online https://rdcu.be/bRuYx provided by the Springer Nature SharedIt content-sharing initiative. 82 decline due to low productivity, which includes slow growth, late age-at-maturity, longevity, 83 low fecundity, low natural mortality, and often protracted breeding cycles (Cortés 2000). These 84 ‘slow’ life history traits are particularly unfavourable in spatially-confined freshwater and 85 estuarine environments, where population size is inherently constrained (Ballantyne and 86 Robinson 2010). 87 88 Temporally, freshwater and estuarine environments are much more variable in their physical 89 parameters (e.g. temperature, salinity, turbidity, dissolved oxygen, water flow) compared to 90 marine environments (McLusky 1993; Pinto and Marques 2015). Furthermore, it is likely that 91 fluctuations in these physical parameters will become more frequent and severe with climate 92 change (Lennox et al. 2019). Unlike their marine counterparts, elasmobranchs in freshwater 93 and estuarine environments cannot always readily escape unfavourable environmental and 94 anthropogenic pressures (Compagno and Cook 1995). Nor have they evolved strategies such 95 as rapid growth, short life cycles or the ability to aestivate or breath air in order to outlast 96 unfavourable environmental conditions like some teleost fishes (Compagno 2002). 97 98 In recent decades, significant concern has been raised about the status of freshwater and 99 euryhaline elasmobranch populations (Dulvy et al. 2014; Lucifora et al. 2015). Many species 100 have become increasingly threatened and rapid local extinctions have been observed in regions 101 of dense human population (Dulvy et al. 2014; Dulvy et al. 2016; Moore 2017). Of the 33 102 freshwater species identified in Dulvy et al. (2014) (a grouping which includes obligate 103 freshwater and euryhaline species), 12 are listed as threatened with extinction on the 104 International Union for the Conservation of Nature (IUCN) Red List of Threatened Species 105 (‘the Red List’) (IUCN 2018). The conservation status of euryhaline elasmobranchs indicates 106 they have the highest susceptibility to negative anthropogenic pressures. This likely because 107 they move between freshwater and marine environments during their life history, thereby 108 increasing potential for exposure across a range of environments (Compagno and Cook 1995). https://www.nespmarine.edu.au/document/categorising-use-patterns-non- 4 marine-environments-elasmobranchs-and-review-their-extinction https://link.springer.com/article/10.1007%2Fs11160-019-09576-w POSTPRINT or read published version online https://rdcu.be/bRuYx provided by the Springer Nature SharedIt content-sharing initiative. 109 Sawfishes (Pristidae) for example, are one of the most threatened marine vertebrate families 110 with all five species assessed as either Critically Endangered
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