Mar Biodiv DOI 10.1007/s12526-014-0275-7


Shark diversity in the Arabian/ higher than previously thought: insights based on composition of landings in the

Rima W. Jabado & Saif M. Al Ghais & Waleed Hamza & Mahmood S. Shivji & Aaron C. Henderson

Received: 30 July 2014 /Revised: 29 August 2014 /Accepted: 23 September 2014 # Senckenberg Gesellschaft für Naturforschung and Springer-Verlag Berlin Heidelberg 2014

Abstract Although fauna in the Arabian/Persian Gulf the existence of the , have been studied for decades, shark diversity has only been griseum; the tawny , ferrugineus; the silky recently investigated in the region. Here, we present a first shark, falciformis; and the , comprehensive account of shark diversity from the United Carcharhinus plumbeus, in these waters. This inventory pro- Arab Emirates based on -dependent data collected at vides an urgently needed assessment of current regional di- market and landing sites over a two- period of field versity patterns that can now be used as a baseline for future sampling. Landings across the country were dominated by investigations evaluating the effect of on shark pop- carcharhinids, and six species were found to be most abun- ulations. Results emphasize the need for research on life dant, including the - shark, Carcharhinus sorrah,and history traits of the various species in to determine their the , acutus, contributing 31.8 % regional , but also reveal that a precaution- and 29.9 %, respectively, of the total number of . While ary approach to conservation will be necessary to mitigate observed landings varied among regions and across seasons, anthropogenic impacts. results showed that shark landings were dominated by small- sized species, which may be a reflection of . Keywords Shark . Species richness . United Arab Emirates . We are now expanding the existing checklist of shark species Management . Conservation in the Persian Gulf from 27 to 31, having utilized both mor- phological identification and genetic barcoding in validating Introduction Electronic supplementary material The online version of this article (doi:10.1007/s12526-014-0275-7) contains supplementary material, The Arabian/Persian Gulf (hereinafter referred to as the which is available to authorized users. ‘Gulf’) is a highly stressed as a result of the R. W. Jabado (*) : S. M. Al Ghais : W. Hamza prevailing environmental conditions as well as the anthropo- Department, College of , United Arab Emirates genic activities that have introduced a number of stressors University, P.O. Box 15551, Al Ain, United Arab Emirates threatening its ecological integrity and sustainability (Hamza e-mail: [email protected] and Munawar 2009). With the rapid economic growth that has M. S. Shivji taken place in the eight bordering countries of Iran, Iraq, Save Our Shark Center, Nova Southeastern University Kuwait, , Bahrain, Qatar, the United Arab Emir- Oceanographic Center, 8000 North Drive, Dania Beach, ates (UAE), and , the marine environment is swiftly FL 33004, USA changing. A. C. Henderson Although the overall biodiversity at the species level is still The School for Field Studies, Center for Marine Resource Studies, poorly understood compared to that of the Arabian , the South Caicos, Turks and Caicos Islands Gulf is considered biologically impoverished, in part because of its young age, but primarily due to its environmental Present Address: R. W. Jabado characteristics (Randall 1995; Sheppard et al. 2010). It is Gulf Elasmo Project, P.O. Box 29588, Dubai, United Arab Emirates believed that most organisms living in the Gulf survive at Mar Biodiv the limits of their physiological tolerance and that marine taxa (White and Weigmann 2014), was also described in the Gulf, here are derived from the penetration of species bringing the total number of species to 27 (White and through the Strait of Hormuz (Price 1993; Beech 2004a). Weigmann 2014). The limited amount of research currently Basson et al. (1977) reported low species richness in these being directed toward shark diversity, distribution, and biology waters, which was confirmed by most later research on ben- gives rise to doubts about the completeness and accuracy of thic groups such as and (Price and Coles available regional checklists (Jabado et al. 2014). In the UAE, 1992; Sheppard et al. 1992). On the other hand, the Gulf is there is no established list of shark species other than some also recognized as home to at least four species of marine confirmed sightings within the Gulf recorded during a survey turtles, over 10 cetacean species, the second-largest dugong conducted in 2002 by the Environment Agency – Abu Dhabi population in the world, as well as large numbers of endemic (EAD) (Edwin Grandcourt, pers. comm.) and during a 10-day and migratory birds, suggesting that it could be harboring high visit to a landing site in Abu Dhabi by Moore et al. (2012a). This levels of marine biodiversity (Hellyer and Aspinall 2005). general lack of knowledge on the number of shark species, From a fisheries perspective, various research projects have composition and quantities of catches, and the amount of indicated that anywhere from 200 and up to 550 species have efforts directed toward this fishery suggests that shark species been reported in the Gulf, including -associated , richness in the region could be higher than previously recorded. sharks, and rays (Krupp et al. 2000; Grandcourt 2012). In com- This is especially true since it has been shown around the world parison to the fish fauna documented in Oman’s Arabian Sea, it is that with increased research and genetic studies, new species are clear that the Gulf is limited in its fish biodiversity, and few being discovered and described at a rapid rate (Naylor et al. species are endemic to these waters (Randall 1995; Carpenter 2012). et al. 1997; Bishop 2003; Beech 2004b). Furthermore, it appears Globally, shark populations are facing increasing pressure, that there are regional variations in species richness throughout and the advancement of conservation measures requires infor- the Gulf, with fewer species identified in western and southern mation on their biodiversity and conservation status areas, while northern and eastern areas, as well as the deeper (Simpfendorfer et al. 2011). In the UAE, fishermen have waters closer to the Strait of Hormuz, are richer in certain species indicated a general decline in shark catches, abundance, and (Price 1993; Beech 2004b). This is believed to be related to size over the last two decades, suggesting that the shark several factors, including bottom topography and sediment fishery is currently overexploited (Jabado et al. 2014). How- in the Gulf (Beech 2004b). ever, protection of sharks in the Gulf is hampered by limited Fisheries in the region are described as artisanal, multi-gear, available baseline scientific data, along with the challenge of and multi-species (Beech 2004b;Grandcourt2012). Fishermen balancing conservation efforts with the provision of essential operate two types of boats: small fiberglass dories, or ‘tarad’, resources for growing coastal populations. In order to main- and traditional wooden dhows, or ‘lansh’ (Grandcourt 2012; tain the ecological integrity of the Gulf, it is essential to Jabado et al. 2014). The primary fishing gear utilized on these understand and evaluate potential changes in the marine bio- vessels include drift nets, nets, handlines, traps, longlines, diversity of this increasingly threatened . and trolls (Jabado et al. 2014). Although sharks are an important Here, we investigate the diversity of shark species captured component of fisheries and fish trade, their diversity in the Gulf in the UAE artisanal fishery. We present the results of fishery- is still poorly understood (Jabado et al. 2014).Basedona dependent market and fish landing site surveys that can aid in literature review and results from market surveys, the most conservation initiatives both in the UAE and in the broader recent account of shark species in this basin confirms the pres- region. Specifically, we (1) examine patterns of species com- ence of 26 species (Moore et al. 2012b). Although these reports position, distribution, and relative abundance across sites; (2) are based on limited observations and do not reflect changes in investigate temporal and spatial variability in landings com- geographic and temporal trends that may be occurring in the position; and (3) validate the field identification of each spe- basin, they do hold relative value, as they remain the only cies through genetic analysis of a representative sample of species records and measures of abundance levels for sharks in individual species using the Cytochrome c oxidase subunit 1 the region. Furthermore, despite the fragmented of these gene (COI). We conclude with a discussion of general impli- surveys, the rate of species discovery is relatively high, with cations for the conservation of shark species in the Gulf. recent documentation and confirmation of new shark species, including the slender weasel, randalli (Compagno, Krupp and Carpenter, 1996); sliteye, Loxodon macrorhinus Material and methods (Müller and Henle, 1839); snaggletooth, Hemipristis elongatus (Klunzinger, 1871); graceful, Carcharhinus amblyrhynchoides Study sites (Whitley, 1934); and hardnose, C. macloti (Müller and Henle, 1839) (Compagno et al. 1996; Moore et al. 2010). More recent- The Gulf is an epicontinental semi-enclosed sea lying in a ly, a new species of whaler shark, Carcharhinus humani sp. nov. subtropical zone with hyper-arid climate, stretching 1,000 km Mar Biodiv in length from the Shatt al-Arab waterway to the Strait of then reduced to twice a month in January 2012. After plotting Hormuz, and varying in width from 75 to 350 km (Carpenter the cumulative number of species present at each market visit et al. 1997)(Fig.1). The basin has an average depth of 35 m, against the number of market visits, it was determined that gradually becoming deeper, to 100 m, as it approaches its even with a reduction in sampling frequency, surveys would entrance (Sheppard et al. 1992).Themarineenvironmentis be sufficient to describe species composition at landing sites. harsh and extreme, characterized by low hydrodynamic ener- Each visit lasted three to four hours, depending on the quantity gy; relatively shallow depths; high evaporation rates, surface of sharks landed. Specimens were always landed whole, and water temperatures, and salinities; and minimal water therefore it was possible to identify them to the lowest possi- exchange. ble taxonomic level using keys from Carpenter et al. (1997), The UAE lies along the southeastern Gulf and ex- Compagno et al. (2005), and Last and Stevens (2009). Be- tends to the Gulf of Oman between 22° and 26° N latitude cause shark trade among the emirates does occur, sharks and 51° and 57° E longitude. The country’s coastline stretches sampled were marked with cuts on their left , and visits roughly 740 km, including some 650 km of the western Gulf to markets did not occur on consecutive days and weeks in coast (EAD 2011). The main study area was along the Gulf order to avoid double-counting study specimens. coastline of the UAE. From April through June 2010, several An analysis of species richness was undertaken using exploratory market and landing site visits were carried out to Jaccard’s similarity index to determine the percentage of spe- determine sites with the largest concentrations of shark land- cies shared between landing sites (Magurran 2004). In addi- ings. It was subsequently determined that this study would tion, landings composition was compared across seasons, focus on landing sites in the regions nationally defined as which were defined as spring (March–May), summer (June– Western (Mina Zayed, Abu Dhabi), Central (Jubail, Sharjah), August), autumn (September–November), and winter (De- and Northern (Maarid, Ras Al-Khaimah (RAK)). While sev- cember–February). Full seasons were sampled for both , eral landing sites exist within each region, these three loca- with the exception of autumn, which was sampled for two tions are found along the Gulf coastline where vessels offload months in 2010 and one month in 2012 due to the limited time their catches directly, facilitating the collection of information frame of the project. on capture location. Vessels operating and offloading in this area fish exclusively in Gulf waters, and thus it was possible to Genetic analyses ensure that all species recorded were from the waters of the Gulf and not the Arabian Sea. Furthermore, fishers from Tissue samples were collected from fresh at the four nearby landing sites transport their landings to these markets sampling sites. All samples were immediately placed in at the time of auction, enabling sampling of larger numbers of Eppendorf Tubes, preserved in 95 % ethanol, and stored at specimens during each survey. Species composition of land- −20 °C until required for analysis. To validate species identity, ings from Dubai, as well as from specimens transported to a set of 130 tissue samples comprising five samples from each Dubai from these three regions, were opportunistically record- morphologically identified species, when available, were ed at the Dubai Deira fish market while conducting separate analyzed. trade surveys and were included in this analysis. Genomic DNA was extracted using the DNeasy & Tissue Kit (Qiagen Inc., Valencia, CA, USA) from 25 mg of Market and landing site surveys fresh tissue collected from whole specimens, according to manufacturer instructions. Extracted DNA was checked on Site visits were made prior to the start of the main daily 0.8 % TBE agarose gels containing ethidium bromide for auction, when the majority of landings were on display, and DNA quality and concentration. A DNA fragment from the were at different times: 04:30–08:00 in Abu Dhabi, 16:00– COI gene comprising approximately 650 bp was amplified by 18:30 in Sharjah, 12:30–15:00 in RAK, and 17:00–20:00 in PCR using the individual primers Fish F1 (5’-TCAACCAA Dubai. All sharks found at landing sites were caught from CCACAAAGACATTGGCAC-3’), Fish F2 (5’-TCGACTAA UAE Gulf waters, whereas those found at markets were TCATAAAGATATCGGCAC-3’), Fish R1 (5’-TAGACTTC sometimes transported from other emirates or from Oman. TGGGTGGCCAAAGAATCA-3’), and Fish R2 (5’-ACTT Data were recorded on the origin of each shark at the markets, CAGGGTGACCGAAGAATCAGAA-3’) (Ward et al. 2005). and only those captured in UAE waters were considered in Amplification reactions were performed in 50-μLvolumes, this study. containing 1 μL of the extraction genomic DNA, 10 pmol of Data collection commenced in October 2010 and was each primer, 10X PCR buffer (Qiagen Inc.), 50 μMdNTPs ongoing until September 2012. With the exception of sites in mix (Illustra dNTP set, GE Healthcare), 1 unit of HotStarTaq Dubai, each site was visited twice a month on a rotational DNA Polymerase kit (Qiagen Inc.), and 33.3 μLHPLCpuri- basis until January 2012, when visits were reduced to once a fied water (OmniSolv). The PCR thermal cycling employed month. In Dubai, data were collected four times a month, and was: 95 °C initial denaturation for 15 min, followed by Mar Biodiv

Fig. 1 Map indicating the location of landing sites across the UAE where sampling was undertaken

35 cycles of 94 °C for 1 min, 50 °C for 1 minute, 72 °C for compromising its power. Taxonomic clustering among 2 min, and a 2-min final extension step at 72 °C. Amplifica- barcoded samples was analyzed by constructing tions were performed using the BioRad iCycler thermal cy- phylogenetic trees using three different methods: neighbor- cler. Amplified fragments were confirmed on 1.2 % agarose joining (NJ), maximum likelihood (ML) and maximum par- gel stained with ethidium bromide and viewed on a Foto/ simony (MP). Estimation of the NJ (Kimura two-parameter spectrum Transilluminator (FotoDyne). PCR reactions were distance model [Kimura 1980]) and MP trees was performed cleaned with QIAquick PCR Purification Kit (Qiagen) and using 1,000 bootstrap replications (MEGA 4) (Tamura et al. eluted in 30 μL of Buffer EB. For each sample, 10 μLof 2007). cleaned cycle sequencing reaction per well was loaded in a MicroAmp 96-Well Reaction Plate (Applied Biosystems, USA), and sequencing was completed using the dye-labeled termination method (BigDye Terminator v3.1, Cycle Se- Results quencing Kit, Applied Biosystems) on a 3130xl Genetic Analyzer (Applied Biosystems) in either forward or Overall species composition reverse direction. Sequences were inspected and cleaned of ambiguous bases A total of 12,478 individual sharks originating from UAE by visualizing the corresponding chromatogram using the Gulf waters were recorded from 205 site visits. After 150 BioEdit program (Hall 1999). Species identification was per- visits, from which 28 species of sharks were confirmed, the formed using both the BOLD Identification Engine (www. frequency of surveys was reduced, as it was determined that and GenBank nucleotide database (www. extra market visits would not serve to increase the diversity of ncbi.nlm.nih.ggoc/nucleotide). The BOLD and GenBank species encountered. An additional two species were docu- engines each matched uploaded sequences with others mented in 2012, however, raising the number of confirmed present in their databases, and provided high specimen species to 30, which consisted of nine families from three similarity or maximum identity percentages, respectively, orders (Table 1). The family Carcharhinidae was the most with matching sequences. All sequences were then aligned diverse, with 18 species, followed by with using Clustal XI software and trimmed to 417 bp in order to three species, and Sphyrnidae and with include as many species in the analysis as possible without two species each. Mar Biodiv

Table 1 Taxonomic list of shark species, including IUCN Red List Status, recorded from UAE waters from 205 surveys

Family/Species IUCN status Abu Dhabi Dubai Sharjah Ras Al-Khaimah Autumn Winter Spring Summer TOTAL


Hemiscylliidae Chiloscyllium NT 1 3 1 0 1 0.02 2 0.06 1 0.02 1 0.04 50.04 arabicum Chiloscyllium NT 0 0 1 0 0 0.0 0 0.0 1 0.02 0 0.0 10.01 griseum Nebrius ferrugineus VU 0 0 2 0 0 0.0 1 0.03 0 0.0 1 0.04 20.02 Stegostomatidae Stegostoma VU 0 5 4 0 1 0.02 0 0.0 7 0.2 1 0.04 90.07 fasciatum Rhincodontidae Rhincodon typus VU 0 1 0 0 0 0.0 1 0.03 0 0.0 0 0.0 10.01 Odontaspididae taurus VU 1 0 0 0 0 0.0 0 0.0 1 0.02 0 0.0 10.01 Triakidae Mustelus mosis DD 1 17 55 131 37 0.9 48 1.6 101 2.8 18 0.8 204 1.63 Hemigaleidae Chaenogaleus VU 2 7 23 28 8 0.2 25 0.8 21 0.6 6 0.2 60 0.48 macrostoma Hemipristis elongata VU 3 5 26 15 18 0.47 7 0.2 13 0.3 11 0.4 49 0.39 Paragaleus randalli NT 0 9 22 54 9 0.23 17 0.5 31 0.8 28 1.2 85 0.68 Carcharhinidae Carcharhinus NT 33 8 41 8 15 0.39 6 0.2 62 1.7 7 0.3 90 0.72 amblyrhynchoides Carcharhinus NT 0 4 3 1 3 0.07 0 0.0 0 0.0 5 0.2 80.06 amblyrhynchos Carcharhinus DD 61 16 42 8 19 0.5 32 1.0 61 1.7 15 0.6 127 1.02 amboinensis Carcharhinus NT 8 33 17 8 6 0.15 12 0.4 36 1.0 12 0.5 66 0.53 brevipinna Carcharhinus NT 136 63 212 150 187 4.94 189 6.3 96 2.7 86 3.8 561 4.50 dussumieri Carcharhinus NT 0 6 0 0 6 0.15 0 0.0 0 0.0 0 0.0 60.05 falciformis Carcharhinus VU 1 2 0 0 2 0.05 1 0.03 0 0.0 0 0.0 30.02 leiodon Carcharhinus leucas NT 93 44 18 12 19 0.5 62 2.0 68 0.0 18 0.8 167 1.34 Carcharhinus NT 906 300 516 64 581 15.3 455 15.3 516 14.7 234 10.4 1786 14.31 limbatus Carcharhinus NT 0 60 11 102 73 1.93 42 1.4 43 1.2 15 0.6 173 1.39 macloti Carcharhinus NT 10 15 10 3 8 0.2 5 0.1 9 0.2 16 0.7 38 0.3 melanopterus Carcharhinus VU 1 0 6 6 4 0.1 5 0.1 1 0.02 3 0.1 13 0.1 plumbeus Carcharhinus sorrah NT 615 716 1460 1182 997 26.3 675 22.7 1179 33.7 1122 50.2 3973 31.84 Galeocerdo cuvier NT 0 0 1 0 0 0.0 0 0.0 1 0.02 0 0.0 10.01 Loxodon LC 8 320 88 704 415 10.9 235 7.9 270 7.7 200 8.9 1120 8.98 macrorhinus acutidens VU 30 3 7 1 19 0.5 4 0.1 11 0.3 7 0.3 41 0.33 Rhizoprionodon LC 818 870 989 1060 1315 3.46 1083 36.4 924 26.4 415 18.5 3737 29.95 acutus Rhizoprionodon LC 0 0 1 11 4 0.1 8 0.2 0 0.0 0 0.0 12 0.1 oligolinx Sphyrnidae lewini EN 0 7 2 6 8 0.2 1 0.03 4 0.1 2 0.08 15 0.12 Sphyrna mokarran EN 80 8 30 6 17 0.4 50 1.6 45 1.2 12 0.5 124 0.99 TOTAL 2808 2522 3588 3560 3782 30.3 2968 23.7 3495 28.0 2233 17.8 12478 100

(EN Endangered; NT Near Threatened; VU Vulnerable; DD Data Deficient; LC Least Concern); species composition and quantities of sharks recorded in Abu Dhabi, Dubai, Sharjah, and Ras Al-Khaimah, based on their location of origin, seasonal and total catch composition (n=number of individuals; % of shark landings) Mar Biodiv

2000 Carcharhinids dominated landings in terms of number, 1800 with 95.5 % (n=11,922) of the total shark landings, followed 1600 1400 by the triakids, consisting of one species, Mustelus mosis 1200 1000 Autumn (Hemprich and Ehrenberg, 1899), but accounting for 1.6 % 800 Winter of the total landings. While the total number of species was 600 Spring Number of sharks of Number 400 relatively high, many of them were found only in small 200 Summer quantities and landings were dominated by a few species. 0 Abu Dhabi Dubai Sharjah Ras Al Central region The most abundant species was Carcharhinus sorrah (Müller Khaimah and Henle, 1839), contributing 31.8 % to the total number of Location sharks, followed by Rhizoprionodon acutus (Rüppell, 1837), Fig. 2 Seasonal shark landings recorded for each landing site location, with Dubai and Sharjah landings shown separately as the Central region with 29.9 % of the total. In terms of number, C. limbatus (Valenciennes, 1839), L. macrorhinus, C. dussumieri (Valen- ciennes, in Müller and Henle, 1839), and M. mosis were also (17.8 %). The numbers also varied with regard to seasonal relatively abundant, contributing 14.3 %, 8.9 %, 4.5 %, and shark landings by site location. Abu Dhabi had the highest 1.6 %, respectively, to the total shark numbers. The remaining landings in autumn (37.9 %), followed by winter (31.1 %) and 24 species comprised between 0.01 % and 1.4 % of the total spring (25.9 %), while almost no shark landings were record- shark landings. ed in the summer (4 %). In Dubai, landings were stable during autumn (30.9 %) and spring (32 %), but declined during winter (16.2 %) and summer (20.7 %). Landings in Sharjah Spatial and seasonal species composition were relatively stable across seasons, although spring yielded the highest number, with 29 % of the total, followed by With respect to the 30 shark species identified, Sharjah was summer (25.7 %), winter (23.8 %), and autumn (21.4 %). the region most rich in species, with a total of 26 species, RAK showed a different pattern as well, with landings followed closely by Dubai, with 24 species. RAK had 21 peaking in autumn (32.7 %), followed by spring (27 %), species, while Abu Dhabi displayed the lowest species rich- winter (23 %), and summer (17.2 %). When landings in Dubai ness, with 19 species recorded. With regard to the similarity in and Sharjah were combined, Central region numbers showed ’ species composition among landing sites, Jaccard s index similar patterns to RAK, with a peak in spring (30.2 %), but indicated that the degree of species overlap among regions then followed by autumn (25.3 %), summer (23.7 %), and was moderately high, with regions sharing anywhere from winter (20.7 %) (Fig. 2). 60.7 % to 80.7 % of species (Table 2). Overall species composition varied across locations and Although the sampling effort was consistent in each loca- seasons. While six species dominated overall among the land- tion and cross-seasonally, there was some degree of variability ings, some variability in the dominant species was noted with in the number of observed landings among regions and across regard to regional occurrence and abundance (Fig. 3). The seasons (Table 1). Among regions, Dubai had the fewest shark most frequently observed species at all sites were C. sorrah landings, with 20.2 % of the total, followed by Abu Dhabi and R. acutus. With the exception of landings of M. mosis and with 22.5 %. When viewed from a regional perspective, the C. macloti, the most abundant species were similar between Central region, comprising both the Dubai and Sharjah land- Dubai and Sharjah, and landings composition for these two ing sites, contributed 49.5 % of the total number of landings. sites were combined as the Central region. There was no significant difference in the number of spe- Noteworthy species occurrence included M. mosis, ac- cies across seasons, with 25 species recorded in autumn, 24 in counting for a low proportion of catches in most locations both winter and spring, and 23 in summer. There was varia- (n=1 in Abu Dhabi) but common in RAK, thereby increasing tion, however, in the total number of landings, with autumn its abundance in the national catch composition overall; yielding the highest number, with 30.3 % of the total captures, C. macloti, which was absent in Abu Dhabi landings but whereas a significant decline was observed in the summer was recorded at all other locations across seasons, with 58.9 % of catches recorded in RAK; C. leucas (Müller and Table 2 Jaccard’s similarity index values illustrating the degree of sim- ilarity in the species composition among sampling sites in the UAE Henle, 1839), which was found in catches across seasons but predominantly in Abu Dhabi (55.6 %), where it was abundant; Abu Dhabi Dubai Sharjah Ras Al-Khaimah C. leiodon (Garrick, 1985), which was only present in Dubai and Abu Dhabi in autumn and winter; C. falciformis (Müller Abu Dhabi * 0.65 0.60 0.66 and Henle, 1839), which was recorded in Dubai in autumn but Dubai * * 0.72 0.73 not present at other landing sites or during other seasons; Sharjah * * * 0.80 R. oligolinx (Springer, 1964), which was only found in RAK Ras Al-Khaimah * * * * (n=11) and Dubai (n=1) during autumn and winter; and Mar Biodiv

1.6% 1.8% 7.5% 4.5% 8.7% 3.6% 4.2% 29.9% 29.7% 8.9% 19.7% 7.5% 0.9% 0.9% 14.3% 4.5% 33.2% 6.6% 30.4% 31.8% 13.3% 2.8% 5.7% 3.3% 35.6% 4.8% 29.1%

32.2% 21.9%

Fig. 3 Relative landings composition (%) of the top six species for each of the three regions (Western, Central, and Northern). The chart at the upper left shows the overall species composition for the three regions combined.

P. randalli, C. amblyrhynchos (Bleeker, 1856), and Sphyrna sequences, including the only sample of C. griseum collected. lewini (Griffith and Smith, 1834), which were not recorded in All sequences were compared with those in BOLD and GenBank Abu Dhabi but present at other sites. databases to confirm initial morphological identification, and the results of matching sequences, along with the amplicon size Range extensions and new species confirmations in the Gulf produced for each sample, are provided in Appendix A. Genetic analysis based on morphological characteristics un- Four previously unconfirmed species in this basin were re- equivocally confirmed 24 species among those recorded in this corded, extending their current known distribution. They in- study. Of these, 12 sequences were the first available from the cluded the grey bamboo shark, Chiloscyllium griseum (Müller Gulf for C. arabicum (Gubanov and Schleib 1980), and Henle, 1839); the , Nebrius ferrugineus N. ferrugineus, Stegostoma fasciatum (Hermann, 1783), (Lesson, 1830); the , C. falciformis; and the sand- Rhincodon typus (Smith, 1828), Carcharias taurus (Rafinesque, bar shark, C. plumbeus (Nardo, 1827). Furthermore, 1810), C. amblyrhynchos, C. falciformis, C. melanopterus (Quoy Galeocerdo cuvier (Peron and Lesueur, 1822) and and Gaimard, 1824), C. plumbeus, Negaprion acutidens C. amblyrhynchoides specimens were confirmed for the first (Rüppell, 1837),G.cuvier,and S. lewini. Taxonomic identifica- time in southern Gulf waters. tion from barcodes, however, was ambiguous for five species. Only two of five samples of C. arabicum provided good DNA Barcoding sequence quality, and although results from both BOLD and GenBank assigned these sequences to the Chiloscyllium ge- DNA COI barcoding was attempted on 130 samples from the nus, species resolution was not possible. Rhizoprionodon 30 species identified morphologically in this study. The final oligolinx sequences provided a 100 % match with the same barcode data set comprised 120 sequences from 29 species, species in BOLD, but the closest match in GenBank was 93 % with sequence lengths varying from 485 to 637 bp. Sequences with R. porosus (Poey, 1861). For P. randalli and have been deposited in the GenBank database under accession Chaenogaleus macrostoma (Bleeker, 1852), there was no numbers: KM973088-KM973199. Ten samples were exclud- consistency in the nomenclature of records between BOLD ed from the analysis: three of them yielded ambiguous species and GenBank. Finally, although sequences for C. limbatus identifications, while seven samples failed to provide good samples had slightly different barcodes between them, they all Mar Biodiv matched this species in both databases. However, sequences was recorded in this study, that species has historically been from C. amblyrhynchoides yielded ambiguous results, and reported in the Gulf, and more recently, large aggregations matched both C. limbatus and C. amblyrhynchoides. have been documented in the offshore waters of Qatar (Rob- inson et al. 2013). While incidental of this species Taxonomic clustering may still occur, they presumably go unreported or catches may not be retained since they are protected in the UAE While there were differences in classifications at the family (Jabado et al. 2014). Similarly, reports of C. melanopterus and order levels, all three trees provided similar outcomes in from the Gulf are widespread, but few specimens have been terms of taxonomic clustering. In all trees, specimens from confirmed (Gubanov and Schleib 1980;Bishop2003). Moore database sequence matches that could have been either et al. (2011) suggested that this species may have been re- C. limbatus or C. amblyrhynchoides were all assigned to one placed by C. leiodon in shallow water habitats of the Gulf. cluster and were not distinguishable. Some P. randalli and However, in the UAE, C. melanopterus is common around C. macrostoma samples clustered as one species, while one many coastal and offshore islands (RWJ, personal observa- C. macrostoma sample stood out as a separate species. Results tion) where fishing is prohibited, and the low number of based on the NJ tree are illustrated in Appendix B. sharks (n=38) recorded in this study may not reflect their abundance. Furthermore, as noted by Jabado et al. (2014), most species with low market value, such as C. arabicum and S. fasciatum, are generally discarded at sea Discussion and thus are presumably not accurately represented in land- ings. This could also be due to fishing practices and the This fishery-dependent assessment is the first comprehensive positioning of fishing gear, which may preclude the capture study on shark species found in southern Gulf waters, and it of demersal or bottom-associated species such as these. Final- has enabled the development of an updated regional checklist ly, it is possible that other, less abundant species or seasonal of species by providing an overview of the composition of migrants would have been documented if more frequent sam- shark landings at various sites in the UAE. The study greatly pling had been undertaken or if the study had focused on improves the current knowledge regarding species richness, certain remote areas where targeted shark fisheries were pres- relative abundance, and distribution of sharks exploited by the ent. For instance, the C. taurus in this study was reported UAE fishery. Although data are still incomplete, and in some opportunistically when a showed the project inves- cases insufficient to draw conclusions regarding the abun- tigator pictures of his catches on an offshore island in Abu dance and conservation status of each species in the region, Dhabi (Jabado et al. 2013). our results indicate that sharks are an important component of The presence of species documented in this study that had the marine biodiversity of the Gulf. Here, we discuss the not been previously reported from southern Gulf waters, in- various results from this study and their implications for shark cluding C. amblyrhynchos and G. cuvier, may indicate that conservation in the region, and then offer some recommenda- they are either less abundant or migratory. For instance, the tions for further study and management measures. C. leiodon specimens were recorded only in November and December, suggesting that this species may be present in these Species diversity and occurrence waters during limited times of the year (Moore et al. 2013). To date, however, the only evidence of the occurrence of The latest annotated checklist confirmed the presence of 26 N. acutidens was from a photograph in Saudi Arabia (Basson shark species in the Gulf (Moore et al. 2012b). The present et al. 1977). The collection of 41 individuals during the study has raised this number to 31 and has validated the present study suggests that this species is more common than occurrence of species such as C. griseum, C. plumbeus, previously thought. Finally, the actual number of shark spe- N. ferrugineus,andC. falciformis that had been previously cies in the Gulf may be even higher, as the sighting of a mentioned in the literature but with no supporting evidence , Alopias sp., was reported by a diver at an such as photographs or samples (Gubanov and Schleib 1980; offshore wreck in Dubai. It was recognized based on its Randall 1986;Bishop2003; Compagno et al. 2005). Since the ‘shark’ appearance and its elongated tail (David Holdman, number of species encountered rose very little after the first pers. comm.), a characteristic feature in this family of sharks year of study, it is likely that the actual species composition of (Compagno et al. 2005). While verification of this sighting is sharks in the region, along with the abundant species found in not possible, it is important to note that thresher sharks have UAE Gulf waters, have been accurately documented. How- been reported in the literature, and the remains of four caudal ever, it is important to note that these surveys may have vertebrae belonging to threshers have been documented at underestimated protected, discarded, rare, or even migratory archeological sites in Abu Dhabi (Beech 2004b). Furthermore, species. For instance, while only one shark, R. typus, both the , Alopias pelagicus (Nakamura, Mar Biodiv

1935), and the big thresher, A. superciliosus (Lowe, Anderson and Ahmed 1993;Bonfil2001; Capapé et al. 1841), are present in Omani waters (Henderson et al. 2007). 2006; Henderson et al. 2007;FAO2009;LastandStevens Considering that the Gulf is regarded as a highly stressful 2009; Moore et al. 2012a).There are few available historical environment for many species, the total number of shark records of C. limbatus in the Gulf region, and it is not fre- species recorded from this study is high. Indeed, studies from quently found in landings from Kuwait, Qatar, or Bahrain the , an enclosed body of water considered a marine (Moore et al. 2012a; Moore and Peirce 2013). However, it biodiversity hotspot, have confirmed only 29 species of sharks represents one of the eight most abundant species in Omani (Golani and Bogorodsky 2010; Spaet et al. 2011). Surveys landings (Henderson et al. 2007), which is consistent with conducted in Omani waters have documented 36 shark spe- findings in this study. Loxodon macrorhinus has been docu- cies from the Arabian Sea, while 34 species have been report- mented in Oman landings as the third most abundant, and in ed in the (Anderson and Ahmed 1993; Henderson Maldives, where it represented 70 % of sharks caught based and Reeve 2011). However, compared with other countries in on a research survey (Anderson and Ahmed 1993). During the the broader Indian Ocean region such as , which has first year of their study, Henderson et al. (2007) noted that documented 66 shark species, and Sri Lanka with 61 species, L. macrorhinus was absent from landings in Al Batinah, Al the species richness in the Gulf is significantly lower (Joseph Wusta, and Musandam, but subsequently became the most 1999;Rajeetal.2002;Herath2012). This may be due to a abundant landed species in Musandam. In our study, individ- variety of reasons, including the diversity of fishing gear used uals were recorded from all sites and were most common in in other countries as well as exploited habitats. Indeed, in RAK (comprising 62.8 % of landings), which is situated countries that fish in the Gulf, operations are characterized adjacent to the Musandam Peninsula. However, they were by artisanal fisheries limited to wooden dhows and fiberglass rare in Abu Dhabi (n = 8), and it is likely that the high number dories using traditional gear (Carpenter et al. 1997), whereas of records from Abu Dhabi (155 individuals) reported by other countries in the region utilize a diversity of fishing Moore et al. (2012a), which lack information regarding their vessels that operate with a variety of gear at different depths place of capture, reflect the transport of sharks overland from (Joseph 1999). other areas in the UAE or Oman for sale at the market The limited bathymetry of the Gulf likely precludes habi- (unpublished data). Reports of C. dussumieri suggest that this tation by deepwater species such as the , species is widespread and abundant in the Gulf, especially in brucus (Bonnaterre, 1788), that has been docu- Kuwait and Iran, although it is not frequently recorded in mented in Oman, or even small species favoring deep waters, Bahraini or Omani landings (Blegvad and Loppenthin 1944; such as the bigeye hound shark, omanensis (Norman, Basson et al. 1977; Gubanov and Schleib 1980; Henderson 1939), that are commonly found in the Arabian Sea (Hender- et al. 2007;FAO2009; Moore et al. 2012a; Moore and Peirce son et al. 2007; Javadzadeh et al. 2010; Henderson and Reeve 2013). Mustelus mosis has been reported in various publica- 2011). The global deepwater chondrichthyan fauna, for exam- tions (Blegvad and Loppenthin 1944; Basson et al. 1977; ple, is highly biodiverse yet remains largely undocumented Gubanov and Schleib 1980), but information regarding its (Kyne and Simpfendorfer 2007). Several studies have now abundance remains scarce. Moore and Peirce (2013)notedit indicated that shark species richness can be affected by both as the second most abundant species from landings in Bahrain, bottom-water temperature and depth, with distinctive fauna and while it was documented in Oman by Henderson et al. characterized by spatial distribution of species (Menni et al. (2007), no details were provided regarding its occurrence. 2010; Guisande et al. 2013). Therefore, since the deepest All species reported from Kuwait, Qatar, and Bahrain waters in the Gulf are close to the Strait of Hormuz, where landings were also present in UAE landings (Moore et al. there is a lack of fisheries data and research, it is possible that 2012a; Moore and Peirce 2013). The lower number of species shark species not previously recorded for this basin may be recorded in northwestern Gulf surveys may be a result of the present, and that these could be subdivided based on different limited temporal sampling there, which occurred only during variables such as depth and temperature. April. Indeed, even in the UAE, some species were recorded Carcharhinidae was the dominant species (95.5 %) among only at specific times of the year, such as C. falciformis in the landings investigated in this study. It has been shown that this autumn months. Furthermore, with the exception of the two family is very important in both commercial and artisanal Chiloscyllium species, N. ferrugineus, and R. oligolinx, the fisheries across the world, and species within the family majority of species reported here were also documented in dominate shark landings in many tropical areas (Castillo- Omani landings (Henderson and Reeve 2011). Geniz et al. 1998;Compagnoetal.2005; Henderson et al. 2007;White2007; Last and Stevens 2009). The most abun- Spatial and seasonal distribution dant species recorded in this study, C. sorrah and R. acutus, are also widespread regionally, dominating landings in areas A total of 26 species of sharks were recorded in Sharjah, while where they occur (Krishnamoorthi and Jagadis 1986; only 19 species were recorded in Abu Dhabi, and these two Mar Biodiv sites had the lowest species overlap. While these differences locations likely are a true reflection of local relative are likely not due to fishing methods utilized, since similar abundance (Jabado et al. 2014). gear is used across the country, they may be explained by the With the exception of C. limbatus, the dominant species in variability in fishing grounds used by fishermen in these two the UAE are relatively small sharks, measuring less than emirates and differences in habitat and environmental condi- 1,500 mm LT, that commonly form large schools in inshore tions in the two areas. Although Abu Dhabi waters include waters (Compagno et al. 2005; Last and Stevens 2009). While some offshore islands with deeper waters, most of the western little is known about the behavior of M. mosis,itmostlikely inshore is characterized by shallow embayments with higher forms groups in inshore areas in a similar to other water temperatures and salinities (EAD 2011). On the other species of triakids known to be abundant in coastal waters hand, fishermen in Sharjah largely utilize offshore and deeper (Compagno et al. 2005). Likewise, C. limbatus, a larger shark waters towards the northeastern UAE region, which are reaching over 2,500 mm LT, is known to prefer inshore areas supplied with oceanic water inflowing from the Arabian and is commonly found in large surface schools (Compagno Sea (Price 1993). Studies have shown that the richest areas et al. 2005). This aggregating behavior and preference for for fish fauna within the Gulf are closer to the Strait of inshore waters may explain the particularly high abundance Hormuz, where waters are deeper (Price 1993). The simi- of these species in landings. Similarly, the market dominance larities in species recorded for Sharjah, RAK, and even of predominantly small-bodied sharks from a limited number Dubai likely reflect the use of similar fishing grounds. of species has been recorded in other areas. Data from Oman Landings of M. mosis, on the other hand, were notable in have reported that the dominance of eight species among RAK but less frequent in Dubai and Sharjah, potentially landings (Henderson et al. 2007). Five species represented indicating a difference in species behavior. 64 % of landings in the northeastern Gulf (Moore et al. While there were some seasonal variations in the number of 2012a); three species were dominant in Iran (FAO 2009); 12 species caught, the overall dominant species did not change species were most abundant in Sri Lankan catches (Herath throughout the sampling period. However, there was a shift in 2012);andfivespeciescomprisedupto90%ofshark seasonal dominance between C. sorrah and R. acutus,where specimens recorded in Chinese markets (Lam and Sadovy C. sorrah was more common during spring and summer, de Mitcheson 2011). In this study, while some species of while R. acutus was more abundant in autumn and winter large-bodied sharks were found in landings, they were largely landings. All other species were caught in lower numbers either immature specimens (unpublished data), such as during the summer, which was also the season that yielded C. limbatus, or species that did not contribute substantially the lowest number of landed species overall, comprising only to landings, such as C. brevipinna and S. mokarran. 17.8 % of total landings. Studies on demersal fish While little information is available on whether larger species in the Gulf show patterns of distribution and abun- sharks were more common at one time, fishermen have stated dance that vary seasonally and among habitat types (Basson that the size of sharks in the Gulf has greatly diminished et al. 1977; Shallard and Associates 2003). Grandcourt (2012) (Jabado et al. 2014). As such, it is possible that many larger suggested that this was likely due to higher water temperatures species have been overfished to some extent, and that the during the summer and the lower volume of fishing activity at fishery is now reliant on smaller sharks that are dominant in that time of the year. In fact, it is believed that the reduced landings. It is important to note that individual species may abundance of reef fish during the summer is a result of the have different levels of susceptibility or resilience to exploi- movement of species to deeper and cooler waters (Shallard tation (Stevens et al. 2000; Bonfil 2001). Small-bodied and Associates 2003). Some studies have shown that the most carcharhinids such as R. acutus tend to grow fast, mature common species of sharks can change seasonally (Bizzarro early, have short life spans, and display aseasonal reproductive et al. 2009). Data from the artisanal shark fishery in Mexico cycles (Wourms 1977; Stevens and McLoughlin 1991). On showed landings that were highly seasonal and that varied the other hand, larger sharks such as C. brevipinna mature among regions, which was attributed to the migratory behav- much later and exhibit slower growth rates, while typically ior of various species of sharks (Castillo-Geniz et al. 1998). displaying seasonal breeding cycles and producing annual, Similarly, landings in Oman showed marked differences biennial, or triennial litters (Wourms 1977; Last and Stevens among seasons and across survey sites, also believed to be a 2009). Thus the overall life history traits of small shark species result of the migration patterns of different shark species generally lead to higher biological productivity, making them (Henderson et al. 2008). Lastly, seasonal differences in less susceptible to fishing pressure, which may explain their landings may be due to variations in relative abundance dominance at various markets. Musick et al. (1993) noted that of shark species in local waters. Indeed, as fishermen overexploitation of large sharks in areas off southeastern were found to be highly opportunistic, and as most areas Africa and the northwest Atlantic could have led to the pro- within UAE waters have been utilized for fishing, the liferation of small-bodied sharks. A declining trend in the species composition of landings across seasons and number of large sharks and a shift in efforts towards smaller Mar Biodiv individuals have also been documented in Mexico, , and of species associated with COI sequences in the databases , where species composition of landings for the (White and Last 2012). whole area has been affected (McVean et al. 2006;Bizzarro The success of barcoding is dependent upon low levels of et al. 2009;LamandSadovydeMitcheson2011). Henderson sequence variation within species and much higher levels et al. (2007) documented such a shift in the Omani shark between species (Holmes et al. 2009). As such, some closely fishery, where in just a few years, larger sharks such as related species may not be easily identifiable despite their C. limbatus and S. lewini were displaced by the smaller morphological differences. In our study, the C. limbatus and L. macrorhinus and C. macloti. C. amblyrhynchoides species pair could not be convincingly A change in species composition or size of fished sharks differentiated by barcoding. Ward et al. (2008)reportedlow could have serious implications for the sustainability of a COI sequence divergence and low bootstrap support for these fishery (Stevens et al. 2000). Furthermore, population studies species, and Moore et al. (2011)statedthattheCOIgenewas of coastal shark species have indicated that even a slight barely distinguishable between them. Similar outcomes were increase in juvenile mortality can greatly impair the sustain- also reported for the closely related species C. plumbeus and ability of coastal shark fisheries (Cortes 1998). It is well C. altimus (Springer, 1950), leading to the conclusion that the known that anthropogenic impacts such as and COI barcode may not be suitable for discriminating among habitat degradation have altered populations of sharks around some closely related shark species, and that an additional the world (Stevens et al. 2000). The risk to many species is marker with a higher rate of evolution would be necessary also believed to be depth-related, where species occupying (Ward et al. 2008). shallower waters are more accessible to fishing activities It has been recommended that developing a voucher col- (Dulvy et al. 2014). Considering the relatively small size and lection is a necessity when undertaking genetic analysis in shallow depth characteristics of the Gulf, as well as the in- order to resolve questions about specimen identification creasing anthropogenic disturbances that this entire basin is (Ward et al. 2005). A collection could not be started in this facing, it is important to monitor shark catches in the UAE in study because of limited resources and lack of storage facili- order to document changes in species and size composition of ties necessary when dealing with large animals such as sharks. shark landings. Only one study has focused on developing a specimen and barcode collection for fish species in the Gulf, which included two shark species, C. macrostoma and M. mosis (Asgharian Species identification et al. 2011). Therefore, it seems that to better understand the evolution of species within the Gulf, a centralized facility A complete and reliable taxonomic account of shark species is would be warranted. the most crucial, albeit challenging, aspect of fishery sam- pling, and is an integral component of effective fishery man- Considerations for shark conservation agement, as it allows identification of species richness and diversity (White and Last 2012). In many instances, molecular A number of species considered to be of global conservation methods such as the use of the COI gene sequence have concern were recorded in this study, including C. limbatus, become important identification tools for distinguishing be- C. dussumieri, C. falciformis, C. plumbeus, S. lewini, and tween closely related species (White and Last 2012). In most S. mokarran, which are listed either as threatened or Near cases here, morphologically identified species were congru- Threatened on the IUCN Red List (IUCN 2012). However, ently matched in the BOLD and GenBank COI databases and because IUCN assessments generally lack information from conspecific species clustered together in the NJ analysis. the Gulf, accurate data obtained locally are needed to deter- However, some questions about specimen identification mine which species here are most threatened. While data remain. collected in this study are not a clear indication of the status The inability to assign C. arabicum to a species in either of shark stocks in the UAE, they do provide a baseline that database is due to the fact that a barcode for this species is not should prove beneficial for effective future monitoring and available for comparison. Similarly, the lack of a match for sustainable exploitation of targeted shark stocks. Results sug- R. oligolinx in GenBank also indicates a lack of sequences for gest that there may be a depletion of larger shark species in this species within the database. The clustering of P. randalli these waters, where there is a clear lack of species-specific and C. macrostoma sequences that also matched P. tengi regional life history data and quantitative mortality (Chen, 1963), a species that has not been recorded from the assessments. western Indian Ocean (Compagno et al. 2005), may be due to While some laws for shark management already exist in the a variety of reasons, including the possibility that these species UAE, they should be reexamined in light of the data gathered share haplotypes, or that there was misidentification in the from this study and before unmonitored catches further com- field, mislabeling errors for the samples, or misidentification promise the recovery of already-depleted stocks in the Gulf. Mar Biodiv

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