Journal of Fish Biology A rare contemporary record of the Critically Endangered Ganges Shark Glyphis gangeticus

Journal of Fish Biology A rare contemporary record of the Critically Endangered Ganges Shark Glyphis gangeticus --Manuscript Draft-- Manuscript Number: MS 18-059R1 Full Title: Short Title: Article Type: Keywords: Corresponding Author: A rare contemporary record of the Critically Endangered Ganges Shark Glyphis gangeticus Critically Endangered Ganges Shark Record Brief Communication enforcement; euryhaline; conservation; protected species; river shark; threatened species Rima W. Jabado, PhD United Arab Emirates University Al Ain, Abu Dhabi UNITED ARAB EMIRATES Corresponding Author Secondary Information: Corresponding Author's Institution: United Arab Emirates University Corresponding Author's Secondary Institution: First Author: Rima W. Jabado, PhD First Author Secondary Information: Order of Authors: Rima W. Jabado, PhD Peter Kyne, PhD Evan Nazareth Dipani Sutaria, PhD Order of Authors Secondary Information: Manuscript Region of Origin: Abstract: INDIA The first record of the Ganges Shark Glyphis gangeticus from anywhere in its range in over a decade is reported from the Arabian Sea. One female specimen was recorded at Sassoon Docks in Mumbai, India in February 2016, measuring 266 cm total length. In light of the Critically Endangered status of this species and its rarity, urgent management actions are needed to determine population size and trends in abundance in combination with fisher education and awareness campaigns. Powered by Editorial Manager and ProduXion Manager from Aries Systems Corporation

Ethics Questionaire Ethics questionnaire for JFB Submitted manuscripts will only be considered if the experimental methods employed are ethically justified. Please answer all questions. If you have answered yes to questions 4 to 7, you should include an Ethics paragraph in the Methods section of your manuscript which justifies your methods used. You should complete this questionnaire based on all fishes used in your experiment. For example, if you used live fishes as prey in predation experiments, this is a lethal endpoint for the prey fish (see Questions 5 & 6). This questionnaire relates to the Editorial published in JFB 68, 1-2, which you have been asked to read. Please read the Editorial published in JFB 68, 1-2, for full information on JFB ethics. PLEASE SUBMIT THE COMPLETED QUESTIONNAIRE WITH YOUR MANUSCRIPT ONLINE THROUGH EDITORIAL MANAGER. Corresponding author s name: Rima W. Jabado Question 1: Were fishes collected as part of faunal surveys? NO If Yes, have the fishes, where feasible, been killed rapidly or returned to the wild after being held in aquaria and have procedures complied with local and or national animal welfare laws, guidelines and policies? If Yes, state these and provide suitable evidence (e.g. for the U.K. a Home Office PPL number is sufficient) that protocols have undergone an ethical review process by an institutional animal care and use (or similar) committee, a local ethics committee Question 2: If you have undertaken experimental work, has the care and use of experimental animals complied with local and or national animal welfare laws, guidelines and policies? Not Applicable If Yes, state these and provide suitable evidence (e.g. for the U.K. a Home Office PPL number is sufficient), both here and in the manuscript, that protocols have undergone an ethical review process by an institutional animal care and use (or similar) committee, a local ethics committee, or by appropriately qualified scientific and lay colleagues. If No, because these laws do not exist in your country, please state this. Alternatively, if you carried out purely observational work so ethical permission was not considered necessary please state this both here and in the manuscript. This was purely observational work and therefore ethical permission was not considered necessary. Question 3: Were fishes killed during or at the end of your experiment (e.g. for tissue sampling)? NO If Yes, what method was used? Please provide details both here and in the manuscript. Question 4: Have you performed surgical procedures? NO If Yes, please give brief details of the surgery here. Full details should be given in the manuscript. If the procedures caused more than slight pain or distress, did you use appropriate sedation, analgesia and anaesthesia, with post-operative care? Please provide full details and

justification both here and within the manuscript including type and concentration of anaesthetic. Question 5: Did you use experimental conditions that severely distressed any fishes involved in your experiments? NO If Yes, state the conditions and how they can be justified. What humane endpoints were used to minimise the effects? Please provide full justification within the methods section of your manuscript. Question 6: Did any of the experimental procedures, particularly those that involve lethal endpoints (e.g. predation studies, toxicity testing), cause lasting harm to sentient fishes? Not applicable If Yes, provide details both here and in the methods section of your manuscript. Normally these procedures will be considered unacceptable by JFB unless any harm caused can be justified against the benefits gained. Question 7: Did any of your procedures involve sentient, un-anaesthetised animals paralysed by chemical agents such as muscle relaxants? NO If Yes, provide details both here and in the methods section of your manuscript. Normally these procedures will be considered unacceptable by JFB.

Revised manuscript with track changes 1 Running headline: Critically Endangered Ganges Shark Record 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 A rare contemporary record of the Critically critically Endangered endangered Ganges Shark shark Glyphis gangeticus R. W. JABADO *, P. M. KYNE, E. NAZARETH, D. N. SUTARIA * Gulf Elasmo Project, P.O. Box 29588, Dubai, United Arab Emirates, Research Institute for the Environment and Livelihoods, Charles Darwin University, Darwin, NT 0909, Australia, Saint Xavier College, Mumbai, P.O. Box 400001, India, College of Marine and Environmental Sciences, James Cook University, Townsville, QLD 4811, Australia * Author to whom correspondence should be addressed. Tel.: +971 50 8885687; email: Commented [A1]: Is the journal format? If not, as the IUCN guidelines, all Category names should be capitalized. Please see: Kyne, P.M. (2016). Extinction risk categories and how to cite them. Mitochondrial DNA 27:508 509. rimajabado@hotmail.com

25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 The first record of the Ganges Shark shark Glyphis gangeticus from anywhere in its range in over a decade is reported from the Arabian Sea. One female specimen was recorded at Sassoon Docks in Mumbai, India in February 2016, measuring 266 cm total length. In light of the Critically critically Endangered endangered status of this species and its rarity, urgent management actions are needed to determine population size and trends in abundance in combination with fisher education and awareness campaigns. Key words: enforcement; euryhaline; conservation; protected species; river shark; threatened species. Commented [A2]: Please see comment at the title regarding capitilization 2

50 51 52 53 54 55 River sharks of the genus Glyphis (Carcharhiniformes: Carcharhinidae) are a group of highly threatened, rare, and elusive sharks. Their distribution and status has been difficult to determine, globally and locally, due to a lack of specimens, taxonomic and nomenclatural issues, and occurrence in often remote, inaccessible or poorly-studied locations. Outside of northern Australia, where intensive research is ongoing (e.g. Kyne, 2012; Feutry et al., 2014; 2017), these species are virtually unknown. 56 57 58 59 60 61 62 63 64 65 66 67 Prior to taxonomic resolution by Li et al. (2015), there were thought to be five species in the genus Glyphis. However, molecular data confirmed that the Borneo River river Shark shark Glyphis fowlerae Compagno, White & Cavanagh, 2010 from the Kinabatangan River, Sabah, Malaysian Borneo, and the Irrawaddy River river Shark shark Glyphis siamensis (Müller & Henle, 1839) from the Irrawaddy River, Myanmar, are junior synonyms of the Ganges Shark shark Glyphis gangeticus (Müller & Henle, 1839). As such, G. gangeticus has a widespread but patchy distribution in the Indo-West Pacific. A further two species, the Speartooth Shark shark Glyphis glyphis (Müller & Henle, 1839) and the Northern River river Shark shark Glyphis garricki Compagno, White & Last, 2008, occur across northern Australia (Pillans et al., 2010), and both were recently rediscovered in Papua New Guinea (White et al., 2015). 68 69 70 71 72 73 74 River sharks are an evolutionarily unique group, specialized to inhabit large rivers and estuaries. They are not however obligate freshwater species, but rather are euryhaline, relying both on riverine and marine environments (Lucifora et al., 2015). Available data from Australia suggests that juvenile Glyphis spp. inhabit tidally-influenced rivers, from low to marine salinities, while adults are generally thought to occur in coastal and marine waters (Pillans et 3

75 76 77 78 al., 2010). However, adult specimens of river sharks are rarely encountered, especially in the marine environment. The exception is G. garricki for which adults are regularly recorded in riverine environments (Kyne, unpubl. data), while the first adult G. glyphis were only recorded very recently, being taken from the coast of southern New Guinea (White et al., 2015). 79 80 81 82 83 84 85 86 87 Records of G. gangeticus are patchy, mostly historical, and are often based on jaw material only (Compagno et al., 2010; Li et al., 2015). In the Arabian Sea, the western extent of the species range, there are records based on jaws prior to 2005, but the present status of the species in this region is virtually unknown. The species conservation status is of considerable concern (Compagno, 2007; Jabado et al., 2017). For example, recent targeted surveys in its only known area of occurrence in Borneo, the Kinabatangan River, failed to locate any records (Manjaji-Matsumoto et al., 2017). 88 89 90 91 92 93 94 95 As part of a study investigating shark landings along the northwestern coast of India (Gujarat and Maharashtra states), data on shark landings of sharks were collected at the Sassoon Docks, a major shark landing center located in Mumbai (Maharashtra) (Fig. 1). At this site, sampling was carried out once a week from September 2014 to June 2016, between 6 and 8 am, to investigate landings from gillnet boats, purse-seiners, and trawlers generally operating off the coast of Maharashtra. 96 97 98 On 7 February 7 th 2016, a female G. gangeticus specimen was recorded measuring 266 cm 99 total length (TLLT) (stretched body). Identification was based on the typicalthe following Formatted: Font: Italic Formatted: Subscript 4

100 101 102 103 104 105 106 107 108 109 110 combination of characters: diagnostic features of this species including its broadly rounded short snout, small eyes, the absence of an interdorsal ridge, first dorsal fin origin over rear thirds of pectoral bases, second dorsal- fin height about half of first dorsal- fin height, and an anal fin with deeply notched posterior margins, characteristic upper teeth with high broad serrated triangular hooked cusps, and lower medials moderately large, erect and hookedcusped, narrowly symmetrical with arched roots with weakly serrated cutting edges (Compagno et al., 2010; Ebert et al., 2013). While some photos were taken (Fig. 2), additional information on the origin of the shark, detailed morphometric measurements, and tissue samples for molecular analysis, could not be collected due to rapid processing by fishers and traders at the site. The specimen was presumed most likely to be an adult, based on its large size. 111 112 113 114 115 116 117 118 119 120 121 This G. gangeticus specimen represents the first confirmed record from across the species range in over a decade, the first field observation of a whole large (and most certainly mature) specimen, and the only record from the Arabian Sea outside of Pakistan. The last available accounts of this species are from fishers and jaw traders in Pakistan (M. Harris and G. Naylor, pers. comm.). These include six jaws collected in Karachi in 2001 2002, from sharks estimated to be approximately 180 200 cm LTTL, as well as an additional set of jaws collected from commercial gillnet landings at the Manora Basin in 2005, likely caught in shallow coastal waters south of Karachi and around the Indus River mouth, and estimated to be from a 275 cm LT TL shark (M. Harris, pers. comm.). 122 123 5

124 125 126 127 128 129 130 131 132 133 134 135 136 Information on the fishing location of this record is not available, and it is possible it could have been caught anywhere along the northeast coast of the Arabian Sea. However, even though records of this species are sparse, Glyphis species utilize rivers as nursery areas with female philopatry demonstrated in G. glyphis (Feutry et al., 2017). It could be assumed that the fishing vessel may have traversed north towards the Indus River (adjacent to Karachi, Pakistan), an important site for the species in the northwestern Indian Ocean. However, although the distribution and habitat preferences of adult river sharks remain a critical knowledge gap, studies from Australia and Papua New Guinea indicate that adults can occur outside of rivers in coastal marine environments (Pillans et al., 2010; White et al., 2015). In fact, it is possible that adults may travel long distances with recent molecular data indicating contemporary gene flow between the populations of G. gangeticus in Myanmar (= G. siamensis), Borneo (= G. fowlerae), and those of India and Pakistan, suggesting marine dispersal of several thousand kilometers (Li et al., 2015). 137 138 139 140 141 142 143 144 145 146 147 148 The historical population size of G. gangeticus within the region is unknown, but the population has likely been severely depleted due to a long history of fisheries and other threats in the northern Arabian Sea (Jabado et al., 2017). Over the past three decades, India has ranked as the second or third largest catcher of sharks and rays in the world, contributing up to nine percent of reported global landings (Bineesh et al., 2014; Dent & Clarke, 2015; Kizhakudan et al., 2015), while Pakistan has been considered in the top ten nations contributing to global shark and ray captures (Dent & Clarke, 2015). Landings data, as well as anecdotal information from Indian and Pakistani fishermen, suggest that shark catches, as well as the mean size of sharks landed, has noticeably diminished over the past 15 years with some stocks having already collapsed, especially in nearshore waters (Jabado et al., 2017; Khan, 2012; Kizhakudan 6

149 150 151 152 153 154 155 156 157 158 159 160 161 162 163 et al., 2015; Mohamed & Veena, 2016; Sutaria, unpubl. data). This raises concerns over the long-term sustainability of these fisheries and the status of G. gangeticus along throughout its known range and its different life-stages. Fishing pressure is intense in India with over 13,400 gillnetters operating off Gujarat, as well as many other types of net gear also deployed in coastal areas (CMFRI, 2010). Furthermore, the reliance of G. gangeticus on riverine and estuarine habitat makes it particularly susceptible to many intensifying threats, including habitat modification and degradation, increased river use, and dams and barrages which alter flow, river productivity, and migration pathways. For example, there are four large dams and 22 barrages on the Indus River, Pakistan, which have fragmented the river habitat, with fragment size declining steadily as more barrages are built (Braulik et al., 2015). The construction of barrages has also led to the collapse of the commercial Hilsa Shad shad (Tenualosa ilisha) (Hamilton, 1822) fishery due to the disruption of their migration (Braulik et al., 2015). Because of habitat overlap, it is possible that this fishery historically took juvenile G. gangeticus as bycatch, while net entanglement would be an ongoing threat in the river if juvenile sharks persist due to ongoing fishing pressure from other sources. 164 165 166 167 168 169 170 171 172 173 While G. gangeticus has been protected since 2001 under Schedule I, Part II A of the Indian Wildlife (Protection) Act, 1972, the effectiveness of this measure is likely limited, with ongoing issues in enforcement and compliance, as well as the accurate identification of protected species in catches. Recent extensive landing site surveys along the western coast of India have failed to record this species (Kizhakudan et al., 2015). Given the consistency of landing surveys, which are increasingly recording new species from Indian waters (Akhilesh et al., 2011; Kizhakudan et al., 2015), the lack of records of G. gangeticus has led to questioning of the occurrence of this species in Indian waters, the possibility of its extinction, 7

174 175 176 177 178 as well as its misidentification in recorded landings (Akhilesh et al., 2014). The lack of specimens suggests that this species might have a very low population size in this region or that it may have been extirpated in some portion of its range. The lack of records likely indicates overexploitation from fishing given the intensity of fishing in the northeastern Arabian Sea (Jabado et al., 2017). 179 180 181 182 183 184 185 186 187 188 189 190 191 192 193 194 195 196 197 Considering the potential rarity of this species, and its Critically critically Endangered endangered status, even low-levels of illegal take likely have negative population-level effects (Kyne & Feutry, 2017). Landings such as this record represent a conservation issue and mitigation measures should be urgently considered in view of the suspected low population sizes. Since river sharks exhibit river-specific female reproductive behaviour, a depleted stock in a river is unlikely to be replenished by other populations (Feutry et al., 2014). Given the localized records of G. gangeticus in the Arabian Sea, and the habitat specificity of species, urgent management actions are needed. These should focus on increased surveys to determine the population size, trends in abundance, and spatial distribution of this species around the Indus River in Pakistan and possibly extending into northwestern India. Importantly, these efforts should be combined with education of fishermen fishers and training in protected species identification as well as increased monitoring and enforcement of regulations. Authors wish to thank the Save Our Seas Foundation for the grant (number 282) provided to undertake this study. We are also thankful to G. J. P. Naylor and M. Harris for providing information on historical records from the Arabian Sea region. PMK was supported by the Commented [A3]: Please see comments above 8

198 199 Marine Biodiversity Hub, a collaborative partnership supported through funding from the Australian Government s National Environmental Science Program (NESP). 200 201 References 202 203 204 205 Akhilesh, K. V., Bineesh, K. K., Gopalakrishnan, A., Jena, J. K., Basheer, V. S., Pillai, N.G.K. (2014). Checklist of chondrichthyans in Indian waters. Journal of the Marine Biological Association of India 56, 109 120. 206 207 208 209 210 Akhilesh, K. V., Ganga, U., Pillai, N. G. K., Vivekanandan, E., Bineesh, K. K., Shanis, C. P. R., Hashim, M. (2011). Deep-sea fishing for chondrichthyan resources and sustainability concerns a case study from southwest coast of India. Indian Journal of Geo-Marine Sciences 40, 347 355. 211 212 213 214 215 Bineesh, K. K., Akhilesh, K. V., Sajeela, K. A., Abdussamad, E. M., Gopalakrishnan, A., Basheer, V. S., Jena, J. K. (2014). DNA barcoding confirms the occurrence of rare elasmobranchs in the Arabian Sea of Indian EEZ. Middle-East Journal of Scientific Research 19,1266 1271. 216 217 218 219 Braulik, G. T., Noureen, U., Arshad, M., Reeves, R. R. (2015). Review of status, threats, and conservation management options for the endangered Indus River blind dolphin. Biological Conservation 192, 30 41. 220 9

221 222 223 CMFRI (2010). Marine Fisheries Census (2010) Part 1. India, Govt. of India, Ministry of Agriculture, Dept. of Animal Husbandry, Dairying & Fisheries and Central Marine Fisheries Research Institute, Indian Council of Agricultural Research. New Delhi, India. 224 225 226 227 228 Compagno, L. J. V., White, W. T., Cavanagh, R. D. (2010). Glyphis fowlerae sp. nov., a new species of river shark (Carcharhiniformes; Carcharhinidae) from northeastern Borneo. In: Last PR, White WT, Pogonoski JJ (eds) Descriptions of New Sharks and Rays from Borneo. CSIRO Marine and Atmospheric Research Paper 032, 29 44. 229 230 231 Dent, F. & Clarke, S. (2015). State of the global market for shark products. FAO Fisheries and Aquaculture Technical Paper no. 590. pp. 187. FAO, Rome. 232 233 234 Ebert, D., Fowler, S., Compagno, L. (2013). Sharks of the World. Plymouth, United Kingdom: Wild Nature Press. 235 236 237 238 Feutry, P., Kyne, P. M., Pillans, R. D., Chen, X., Naylor, G. J. P., Grewe, P. M. (2014). Mitogenomics of the Speartooth Shark challenges ten years of control region sequencing. BMC Evolutionary Biology 14, 232. 239 240 241 242 243 Feutry, P., Berry, O., Kyne, P. M., Pillans, R. D., Hillary, R. M., Grewe, P. M., Marthick, J. R., Johnson, G., Gunasekera, R. M., Bax, N. J., Bravington, M. (2017). Inferring contemporary and historical genetic connectivity from juveniles. Molecular Ecology 26,444-456. 244 10

245 246 247 248 Jabado, R.W., Kyne, P. M., Pollom, R. A., Ebert, D. A., Simpfendorfer, C. A., Ralph, G. M., Dulvy, N. K. (eds.) (2017). The Conservation Status of Sharks, Rays, and Chimaeras in the Arabian Sea and Adjacent Waters. pp. 236. Environment Agency Abu Dhabi, UAE, and IUCN Species Survival Commission Shark Specialist Group, Vancouver, Canada. 249 250 251 Khan, M. M. (2012). Status report on bycatch of tuna gillnet operations in Pakistan. In IOTC (ed) IOTC-2012- WPEB08-13. Indian Ocean Tuna Commission, Karachi, Pakistan. 252 253 254 255 Kizhakudan, S. J., Zacharia, P. U., Thomas, S., Vivekanandan, E., Muktha, M. (2015). Guidance on National Plan of Action for Sharks in India. CMFRI Marine Fisheries Policy Series, pp. 102. 256 257 258 259 260 261 Kyne, P. M. (2014). Threatened fishes and marine turtles of Kakadu National Park (with notes on marine mammals). In: Winderlich S, Woinarski J (eds) Kakadu National Park Landscape Symposia Series. Symposium 7: Conservation of Threatened Species, 26 27 March 2013, Bowali Visitor Centre, Kakadu National Park. Internal Report 623, Supervising Scientist, Darwin, pp. 58 74. 262 263 264 Kyne, P. M. & Feutry, P. (2017) Recreational fishing impacts on threatened river sharks: a potential conservation issue. Ecological Management and Restoration 18,209 213. 265 266 267 268 Li, C., Corrigan, S., Yang, L., Straube, N., Harris, M., Hofreiter, M., White, W. T., Naylor, G. J. P. (2015). DNA capture reveals transoceanic gene flow in endangered river sharks. Proceeding of the National Academy of Sciences USA 112, 13302 13307. 269 11

270 271 Lucifora, L., de Carvalho, M. R., Kyne, P. M., White, W. T. (2015). Freshwater sharks and rays. Current Biology 25, R965-R979. 272 273 274 275 276 Manjaji-Matsumoto, B. M., Kyne, P. M., Yee, J. C., Dickson, A. F. (2017). Tagging and Monitoring of Coastal Marine and Freshwater Elasmobranch Population in Sabah. WWF Malaysia Project Report (Shark Protection Marine Program; Project Number MA010311-000-GENF/ UMS Project Code GL00138), pp. 50. 277 278 279 280 Mohamed, K. S. & Veena, S. (2016). How long does it take for tropical marine fish stocks to recover after declines? Case studies from the Southwest coast of India. Current Science 110: 584 594. 281 282 283 284 Pillans, R. D., Stevens, J. D., Kyne, P. M., Salini, J. (2010). Observations on the distribution, biology, short-term movements and habitat requirements of river sharks Glyphis spp. in northern Australia. Endangered Species Research 10: 321 332. 285 286 287 288 289 White, W. T., Appleyard, S. A., Sabub, B., Kyne, P. M., Harris, M., Lis, R., Baje, L., Usu, T., Smart, J.J., Corrigan, S., Yang, L., Naylor, G. J. P. (2015). Rediscovery of the threatened river sharks, Glyphis garricki and G. glyphis, in Papua New Guinea. PLOS One 10: e0140075. 290 291 Electronic references 292 12

293 294 295 Compagno, L. J. V. (2007). Glyphis gangeticus. The IUCN Red List of Threatened Species 2007: e.t9281a12978210. Available at http://dx.doi.org/10.2305/iucn.uk.2007.rlts.t9281a12978210.en 296 297 298 299 300 301 13

Revised manuscript without track changes 1 Running headline: Critically Endangered Ganges Shark Record 2 3 4 A rare contemporary record of the critically endangered Ganges shark Glyphis gangeticus 5 6 7 R. W. JABADO *, P. M. KYNE, E. NAZARETH, D. N. SUTARIA 8 9 10 11 12 * Gulf Elasmo Project, P.O. Box 29588, Dubai, United Arab Emirates, Research Institute for the Environment and Livelihoods, Charles Darwin University, Darwin, NT 0909, Australia, Saint Xavier College, Mumbai, P.O. Box 400001, India, College of Marine and Environmental Sciences, James Cook University, Townsville, QLD 4811, Australia 13 14 15 16 17 18 19 20 21 22 23 24 * Author to whom correspondence should be addressed. Tel.: +971 50 8885687; email: rimajabado@hotmail.com

25 26 27 28 29 30 31 The first record of the Ganges shark Glyphis gangeticus from anywhere in its range in over a decade is reported from the Arabian Sea. One female specimen was recorded at Sassoon Docks in Mumbai, India in February 2016, measuring 266 cm total length. In light of the critically endangered status of this species and its rarity, urgent management actions are needed to determine population size and trends in abundance in combination with fisher education and awareness campaigns. 32 33 34 Key words: enforcement; euryhaline; conservation; protected species; river shark; threatened species. 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 2

50 51 52 53 54 55 River sharks of the genus Glyphis (Carcharhiniformes: Carcharhinidae) are a group of highly threatened, rare, and elusive sharks. Their distribution and status has been difficult to determine, globally and locally, due to a lack of specimens, taxonomic and nomenclatural issues, and occurrence in often remote, inaccessible or poorly-studied locations. Outside of northern Australia, where intensive research is ongoing (e.g. Kyne, 2012; Feutry et al., 2014; 2017), these species are virtually unknown. 56 57 58 59 60 61 62 63 64 65 66 67 Prior to taxonomic resolution by Li et al. (2015), there were thought to be five species in the genus Glyphis. However, molecular data confirmed that the Borneo river shark Glyphis fowlerae Compagno, White & Cavanagh, 2010 from the Kinabatangan River, Sabah, Malaysian Borneo, and the Irrawaddy river shark Glyphis siamensis (Müller & Henle, 1839) from the Irrawaddy River, Myanmar, are junior synonyms of the Ganges shark Glyphis gangeticus (Müller & Henle, 1839). As such, G. gangeticus has a widespread but patchy distribution in the Indo-West Pacific. A further two species, the Speartooth shark Glyphis glyphis (Müller & Henle, 1839) and the Northern river shark Glyphis garricki Compagno, White & Last, 2008, occur across northern Australia (Pillans et al., 2010) and both were recently rediscovered in Papua New Guinea (White et al., 2015). 68 69 70 71 72 73 74 River sharks are an evolutionarily unique group, specialized to inhabit large rivers and estuaries. They are not however obligate freshwater species, but rather are euryhaline, relying both on riverine and marine environments (Lucifora et al., 2015). Available data from Australia suggest that juvenile Glyphis spp. inhabit tidally-influenced rivers, from low to marine salinities, while adults are generally thought to occur in coastal and marine waters (Pillans et 3

75 76 77 78 al., 2010). However, adult specimens of river sharks are rarely encountered, especially in the marine environment. The exception is G. garricki for which adults are regularly recorded in riverine environments (Kyne, unpubl. data), while the first adult G. glyphis were only recorded very recently, being taken from the coast of southern New Guinea (White et al., 2015). 79 80 81 82 83 84 85 86 87 Records of G. gangeticus are patchy, mostly historical, and are often based on jaw material only (Compagno et al., 2010; Li et al., 2015). In the Arabian Sea, the western extent of the species range, there are records based on jaws prior to 2005, but the present status of the species in this region is virtually unknown. The species conservation status is of considerable concern (Compagno, 2007; Jabado et al., 2017). For example, recent targeted surveys in its only known area of occurrence in Borneo, the Kinabatangan River, failed to locate any records (Manjaji-Matsumoto et al., 2017). 88 89 90 91 92 93 94 95 As part of a study investigating shark landings along the northwestern coast of India (Gujarat and Maharashtra states), data on shark landings were collected at the Sassoon Docks, a major shark landing center located in Mumbai (Maharashtra) (Fig. 1). At this site, sampling was carried out once a week from September 2014 to June 2016, between 6 and 8 am, to investigate landings from gillnet boats, purse-seiners, and trawlers generally operating off the coast of Maharashtra. 96 97 98 99 On 7 February 2016, a female G. gangeticus specimen was recorded measuring 266 cm total length (LT) (stretched body). Identification was based on the following combination of 4

100 101 102 103 104 105 106 107 108 characters: broadly rounded short snout, small eyes, the absence of an interdorsal ridge, first dorsal fin origin over rear third of pectoral base, second dorsal-fin height about half of first dorsal-fin height, and an anal fin with deeply notched posterior margins, characteristic upper teeth with high broad serrated triangular hooked cusps, and lower medials moderately large, erect and hooked-cusped, narrowly symmetrical with arched roots with weakly serrated cutting edges (Compagno et al., 2010; Ebert et al., 2013). While some photos were taken (Fig. 2), additional information on the origin of the shark, detailed morphometric measurements, and tissue samples for molecular analysis could not be collected due to rapid processing by fishers and traders at the site. The specimen was most likely an adult, based on its large size. 109 110 111 112 113 114 115 116 117 118 119 This G. gangeticus specimen represents the first confirmed record from across the species range in over a decade, the first field observation of a whole large (and most certainly mature) specimen, and the only record from the Arabian Sea outside of Pakistan. The last available accounts of this species are from fishers and jaw traders in Pakistan (M. Harris and G. Naylor, pers. comm.). These include six jaws collected in Karachi in 2001 2002, from sharks estimated to be approximately 180 200 cm LT, as well as an additional set of jaws collected from commercial gillnet landings at the Manora Basin in 2005, likely caught in shallow coastal waters south of Karachi and around the Indus River mouth, and estimated to be from a 275 cm LT shark (M. Harris, pers. comm.). 120 121 122 123 124 Information on the fishing location of this record is not available, and it is possible it could have been caught anywhere along the northeast coast of the Arabian Sea. However, even though records of this species are sparse, Glyphis species utilize rivers as nursery areas with 5

125 126 127 128 129 130 131 132 133 134 female philopatry demonstrated in G. glyphis (Feutry et al., 2017). It could be assumed that the fishing vessel may have traversed north towards the Indus River (adjacent to Karachi, Pakistan), an important site for the species in the northwestern Indian Ocean. However, although the distribution and habitat preferences of adult river sharks remain a critical knowledge gap, studies from Australia and Papua New Guinea indicate that adults can occur outside of rivers in coastal marine environments (Pillans et al., 2010; White et al., 2015). In fact, it is possible that adults may travel long distances with recent molecular data indicating contemporary gene flow between the populations of G. gangeticus in Myanmar (= G. siamensis), Borneo (= G. fowlerae), and those of India and Pakistan, suggesting marine dispersal of several thousand kilometers (Li et al., 2015). 135 136 137 138 139 140 141 142 143 144 145 146 147 148 149 The historical population size of G. gangeticus within the region is unknown, but the population has likely been severely depleted due to a long history of fisheries and other threats in the northern Arabian Sea (Jabado et al., 2017). Over the past three decades, India has ranked as the second or third largest catcher of sharks and rays in the world, contributing up to nine percent of reported global landings (Bineesh et al., 2014; Dent & Clarke, 2015; Kizhakudan et al., 2015), while Pakistan has been considered in the top ten nations contributing to global shark and ray captures (Dent & Clarke, 2015). Landings data, as well as anecdotal information from Indian and Pakistani fishermen, suggest that shark catches, as well as the mean size of sharks landed, has noticeably diminished over the past 15 years with some stocks having already collapsed, especially in nearshore waters (Jabado et al., 2017; Khan, 2012; Kizhakudan et al., 2015; Mohamed & Veena, 2016; Sutaria, unpubl. data). This raises concerns over the long-term sustainability of these fisheries and the status of G. gangeticus throughout its known range and its different life-stages. Fishing pressure is intense in India with over 13,400 6

150 151 152 153 154 155 156 157 158 159 160 161 gillnetters operating off Gujarat, as well as many other types of net gear also deployed in coastal areas (CMFRI, 2010). Furthermore, the reliance of G. gangeticus on riverine and estuarine habitat makes it particularly susceptible to many intensifying threats, including habitat modification and degradation, increased river use, and dams and barrages which alter flow, river productivity, and migration pathways. For example, there are four large dams and 22 barrages on the Indus River, Pakistan, which have fragmented the river habitat, with fragment size declining steadily as more barrages are built (Braulik et al., 2015). The construction of barrages has also led to the collapse of the commercial Hilsa shad Tenualosa ilisha (Hamilton, 1822) fishery due to the disruption of their migration (Braulik et al., 2015). Because of habitat overlap, it is possible that this fishery historically took juvenile G. gangeticus as bycatch, while net entanglement would be an ongoing threat in the river if juvenile sharks persist due to ongoing fishing pressure from other sources. 162 163 164 165 166 167 168 169 170 171 172 173 174 While G. gangeticus has been protected since 2001 under Schedule I, Part II A of the Indian Wildlife (Protection) Act, 1972, the effectiveness of this measure is likely limited, with ongoing issues in enforcement and compliance, as well as the accurate identification of protected species in catches. Recent extensive landing site surveys along the western coast of India have failed to record this species (Kizhakudan et al., 2015). Given the consistency of landing surveys, which are increasingly recording new species from Indian waters (Akhilesh et al., 2011; Kizhakudan et al., 2015), the lack of records of G. gangeticus has led to questioning of the occurrence of this species in Indian waters, the possibility of its extinction, as well as its misidentification in recorded landings (Akhilesh et al., 2014). The lack of specimens suggests that this species might have a very low population size in this region or that it may have been extirpated in some portion of its range. The lack of records likely 7

175 176 indicates overexploitation from fishing given the intensity of fishing in the northeastern Arabian Sea (Jabado et al., 2017). 177 178 179 180 181 182 183 184 185 186 187 188 189 190 Considering the potential rarity of this species, and its critically endangered status, even lowlevels of illegal take likely have negative population-level effects (Kyne & Feutry, 2017). Landings such as this record represent a conservation issue and mitigation measures should be urgently considered in view of the suspected low population sizes. Since river sharks exhibit river-specific female reproductive behaviour, a depleted stock in a river is unlikely to be replenished by other populations (Feutry et al., 2014). Given the localized records of G. gangeticus in the Arabian Sea, and the habitat specificity of species, urgent management actions are needed. These should focus on increased surveys to determine the population size, trends in abundance, and spatial distribution of this species around the Indus River in Pakistan and possibly extending into northwestern India. Importantly, these efforts should be combined with education of fishers and training in protected species identification as well as increased monitoring and enforcement of regulations. 191 192 193 194 195 196 197 Authors wish to thank the Save Our Seas Foundation for the grant (number 282) provided to undertake this study. We are also thankful to G. J. P. Naylor and M. Harris for providing information on historical records from the Arabian Sea region. PMK was supported by the Marine Biodiversity Hub, a collaborative partnership supported through funding from the Australian Government s National Environmental Science Program (NESP). 198 199 References 8

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225 226 Last PR, White WT, Pogonoski JJ (eds) Descriptions of New Sharks and Rays from Borneo. CSIRO Marine and Atmospheric Research Paper 032, 29 44. 227 228 229 Dent, F. & Clarke, S. (2015). State of the global market for shark products. FAO Fisheries and Aquaculture Technical Paper no. 590. pp. 187. FAO, Rome. 230 231 232 Ebert, D., Fowler, S., Compagno, L. (2013). Sharks of the World. Plymouth, United Kingdom: Wild Nature Press. 233 234 235 236 Feutry, P., Kyne, P. M., Pillans, R. D., Chen, X., Naylor, G. J. P., Grewe, P. M. (2014). Mitogenomics of the Speartooth Shark challenges ten years of control region sequencing. BMC Evolutionary Biology 14, 232. 237 238 239 240 241 Feutry, P., Berry, O., Kyne, P. M., Pillans, R. D., Hillary, R. M., Grewe, P. M., Marthick, J. R., Johnson, G., Gunasekera, R. M., Bax, N. J., Bravington, M. (2017). Inferring contemporary and historical genetic connectivity from juveniles. Molecular Ecology 26,444-456. 242 243 244 245 246 Jabado, R.W., Kyne, P. M., Pollom, R. A., Ebert, D. A., Simpfendorfer, C. A., Ralph, G. M., Dulvy, N. K. (eds.) (2017). The Conservation Status of Sharks, Rays, and Chimaeras in the Arabian Sea and Adjacent Waters. pp. 236. Environment Agency Abu Dhabi, UAE, and IUCN Species Survival Commission Shark Specialist Group, Vancouver, Canada. 247 248 249 Khan, M. M. (2012). Status report on bycatch of tuna gillnet operations in Pakistan. In IOTC (ed) IOTC-2012- WPEB08-13. Indian Ocean Tuna Commission, Karachi, Pakistan. 10

250 251 252 253 Kizhakudan, S. J., Zacharia, P. U., Thomas, S., Vivekanandan, E., Muktha, M. (2015). Guidance on National Plan of Action for Sharks in India. CMFRI Marine Fisheries Policy Series, pp. 102. 254 255 256 257 258 259 Kyne, P. M. (2014). Threatened fishes and marine turtles of Kakadu National Park (with notes on marine mammals). In: Winderlich S, Woinarski J (eds) Kakadu National Park Landscape Symposia Series. Symposium 7: Conservation of Threatened Species, 26 27 March 2013, Bowali Visitor Centre, Kakadu National Park. Internal Report 623, Supervising Scientist, Darwin, pp. 58 74. 260 261 262 Kyne, P. M. & Feutry, P. (2017) Recreational fishing impacts on threatened river sharks: a potential conservation issue. Ecological Management and Restoration 18,209 213. 263 264 265 266 Li, C., Corrigan, S., Yang, L., Straube, N., Harris, M., Hofreiter, M., White, W. T., Naylor, G. J. P. (2015). DNA capture reveals transoceanic gene flow in endangered river sharks. Proceeding of the National Academy of Sciences USA 112, 13302 13307. 267 268 269 Lucifora, L., de Carvalho, M. R., Kyne, P. M., White, W. T. (2015). Freshwater sharks and rays. Current Biology 25, R965-R979. 270 271 272 273 274 Manjaji-Matsumoto, B. M., Kyne, P. M., Yee, J. C., Dickson, A. F. (2017). Tagging and Monitoring of Coastal Marine and Freshwater Elasmobranch Population in Sabah. WWF Malaysia Project Report (Shark Protection Marine Program; Project Number MA010311-000-GENF/ UMS Project Code GL00138), pp. 50. 11

275 276 277 278 Mohamed, K. S. & Veena, S. (2016). How long does it take for tropical marine fish stocks to recover after declines? Case studies from the Southwest coast of India. Current Science 110: 584 594. 279 280 281 282 Pillans, R. D., Stevens, J. D., Kyne, P. M., Salini, J. (2010). Observations on the distribution, biology, short-term movements and habitat requirements of river sharks Glyphis spp. in northern Australia. Endangered Species Research 10: 321 332. 283 284 285 286 287 White, W. T., Appleyard, S. A., Sabub, B., Kyne, P. M., Harris, M., Lis, R., Baje, L., Usu, T., Smart, J.J., Corrigan, S., Yang, L., Naylor, G. J. P. (2015). Rediscovery of the threatened river sharks, Glyphis garricki and G. glyphis, in Papua New Guinea. PLOS One 10: e0140075. 288 289 Electronic references 290 291 292 293 Compagno, L. J. V. (2007). Glyphis gangeticus. The IUCN Red List of Threatened Species 2007: e.t9281a12978210. Available at http://dx.doi.org/10.2305/iucn.uk.2007.rlts.t9281a12978210.en 294 295 296 297 298 299 12

Revised figure captions with track changes 1 2 FIG. 1. Map of the Arabian Sea, northwest Indian Ocean, indicating the locations in Pakistan and India where the Ganges Shark shark (Glyphis gangeticus) has been recorded. 3 4 5 6 7 8 9 10 11 12 FIG. 2. Female Ganges shark (Glyphis gangeticus, 266 cm LTTL,) landed at Sassoon Docks in Mumbai, India. Pictures show the following combination of characters: (a) broadly rounded short snout and small eyesthe characteristic shape of the head, (b) upper teeth with high broad serrated triangular hooked cusps, and lower medials moderately large, erect and hookedcuspedteeth, and (c, d) lateral view of the body with first dorsal fin origin over rear third of pectoral base, second dorsal-fin height about half of first dorsal-fin heightlateral view of the body including second dorsal fin about half height of first dorsal fin, and (e, f) anal fin with deeply notched posterior margins. Formatted: Font: Italic Formatted: Subscript * Author to whom correspondence should be addressed. Tel.: +971 50 8885687; email: rimajabado@hotmail.com

Revised figure captions without track changes 1 2 FIG. 1. Map of the Arabian Sea, northwest Indian Ocean, indicating the locations in Pakistan and India where the Ganges shark Glyphis gangeticus has been recorded. 3 4 5 6 7 8 9 FIG. 2. Female Ganges shark Glyphis gangeticus, 266 cm LT, landed at Sassoon Docks in Mumbai, India. Pictures show the following combination of characters: (a) broadly rounded short snout and small eyes, (b) upper teeth with high broad serrated triangular hooked cusps, and lower medials moderately large, erect and hooked-cusped, (c, d) lateral view of the body with first dorsal fin origin over rear third of pectoral base, second dorsal-fin height about half of first dorsal-fin height, and (e, f) anal fin with deeply notched posterior margins. 10 * Author to whom correspondence should be addressed. Tel.: +971 50 8885687; email: rimajabado@hotmail.com

Figure 1 Click here to download Figure Figure_1.tif

Figure 2 Click here to download Figure Figure_2.tif