ORIGINAL PAPER

Shark diversity in the Arabian/Persian Gulf higher thanpreviously thought: insights based on species composition of sharklandings in the United Arab Emirates

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 fish fauna in the Arabian/Persian Gulfhave been studied for decades, shark diversity has only beenrecently investigated in the region. Here, we present a firstcomprehensive account of shark diversity from the UnitedArab Emirates based on fishery-dependent data collected atmarket and landing sites over a two-year period of fieldsampling. Landings across the country were dominated bycarcharhinids, and six species were found to be most abun-dant, including the spot-tail shark, Carcharhinus sorrah, andthe milk shark, Rhizoprionodon acutus, contributing 31.8 %and 29.9 %, respectively, of the total number of sharks. Whileobserved landings varied among regions and across seasons,results showed that shark landings were dominated by small-sized species, which may be a reflection of overexploitation.We are now expanding the existing checklist of shark speciesin the Persian Gulf from 27 to 31, having utilized both mor-phological identification and genetic barcoding in validating

the existence of the grey bamboo shark, Chiloscylliumgriseum; the tawny nurse shark,Nebrius ferrugineus; the silkyshark, Carcharhinus falciformis; and the sandbar shark,Carcharhinus plumbeus, in these waters. This inventory pro-vides an urgently needed assessment of current regional di-versity patterns that can now be used as a baseline for futureinvestigations evaluating the effect of fisheries on shark pop-ulations. Results emphasize the need for research on lifehistory traits of the various species in order to determine theirregional conservation status, but also reveal that a precaution-ary approach to conservation will be necessary to mitigateanthropogenic impacts.

Keywords Shark . Species richness . UnitedArab Emirates .

Management . Conservation

Introduction

The Arabian/Persian Gulf (hereinafter referred to as the‘Gulf’) is a highly stressed ecosystem as a result of theprevailing environmental conditions as well as the anthropo-genic activities that have introduced a number of stressorsthreatening its ecological integrity and sustainability (HamzaandMunawar 2009). With the rapid economic growth that hastaken place in the eight bordering countries of Iran, Iraq,Kuwait, Saudi Arabia, Bahrain, Qatar, the United Arab Emir-ates (UAE), and Oman, the marine environment is swiftlychanging.

Although the overall biodiversity at the species level is stillpoorly understood compared to that of the Arabian Sea, theGulf is considered biologically impoverished, in part becauseof its young age, but primarily due to its environmentalcharacteristics (Randall 1995; Sheppard et al. 2010). It isbelieved that most organisms living in the Gulf survive at

Electronic supplementary material The online version of this article(doi:10.1007/s12526-014-0275-7) contains supplementary material,which is available to authorized users.

R. W. Jabado (*) : S. M. Al Ghais :W. HamzaBiology Department, College of Science, United Arab EmiratesUniversity, P.O. Box 15551, Al Ain, United Arab Emiratese-mail: rimajabado@hotmail.com

M. S. ShivjiSave Our Seas Shark Center, Nova Southeastern UniversityOceanographic Center, 8000 North Ocean Drive, Dania Beach,FL 33004, USA

A. C. HendersonThe School for Field Studies, Center for Marine Resource Studies,South Caicos, Turks and Caicos Islands

Present Address:R. W. JabadoGulf Elasmo Project, P.O. Box 29588, Dubai, United Arab Emirates

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the limits of their physiological tolerance and that marine taxahere are derived from the penetration of Indian Ocean speciesthrough the Strait of Hormuz (Price 1993; Beech 2004a).Basson et al. (1977) reported low species richness in thesewaters, which was confirmed by most later research on ben-thic groups such as corals and echinoderms (Price and Coles1992; Sheppard et al. 1992). On the other hand, the Gulf isalso recognized as home to at least four species of marineturtles, over 10 cetacean species, the second-largest dugongpopulation in the world, as well as large numbers of endemicand migratory birds, suggesting that it could be harboring highlevels of marine biodiversity (Hellyer and Aspinall 2005).

From a fisheries perspective, various research projects haveindicated that anywhere from 200 and up to 550 species havebeen reported in the Gulf, including reef-associated fishes,sharks, and rays (Krupp et al. 2000; Grandcourt 2012). In com-parison to the fish fauna documented inOman’sArabian Sea, it isclear that the Gulf is limited in its fish biodiversity, and fewspecies are endemic to these waters (Randall 1995; Carpenteret al. 1997; Bishop 2003; Beech 2004b). Furthermore, it appearsthat there are regional variations in species richness throughoutthe Gulf, with fewer species identified in western and southernareas, while northern and eastern areas, as well as the deeperwaters closer to the Strait of Hormuz, are richer in certain species(Price 1993; Beech 2004b). This is believed to be related toseveral factors, including bottom topography and sediment typein the Gulf (Beech 2004b).

Fisheries in the region are described as artisanal, multi-gear,and multi-species (Beech 2004b; Grandcourt 2012). Fishermenoperate two types of boats: small fiberglass dories, or ‘tarad’,and traditional wooden dhows, or ‘lansh’ (Grandcourt 2012;Jabado et al. 2014). The primary fishing gear utilized on thesevessels include drift nets, gill nets, handlines, traps, longlines,and trolls (Jabado et al. 2014). Although sharks are an importantcomponent of fisheries and fish trade, their diversity in the Gulfis still poorly understood (Jabado et al. 2014). Based on aliterature review and results from market surveys, the mostrecent account of shark species in this basin confirms the pres-ence of 26 species (Moore et al. 2012b). Although these reportsare based on limited observations and do not reflect changes ingeographic and temporal trends that may be occurring in thebasin, they do hold relative value, as they remain the onlyspecies records and measures of abundance levels for sharks inthe region. Furthermore, despite the fragmented nature of thesesurveys, the rate of species discovery is relatively high, withrecent documentation and confirmation of new shark species,including the slender weasel, Paragaleus randalli (Compagno,Krupp and Carpenter, 1996); sliteye, Loxodon macrorhinus(Müller and Henle, 1839); snaggletooth, Hemipristis elongatus(Klunzinger, 1871); graceful, Carcharhinus amblyrhynchoides(Whitley, 1934); and hardnose, C. macloti (Müller and Henle,1839) (Compagno et al. 1996; Moore et al. 2010). More recent-ly, a new species of whaler shark,Carcharhinus humani sp. nov.

(White and Weigmann 2014), was also described in the Gulf,bringing the total number of species to 27 (White andWeigmann 2014). The limited amount of research currentlybeing directed toward shark diversity, distribution, and biologygives rise to doubts about the completeness and accuracy ofavailable regional checklists (Jabado et al. 2014). In the UAE,there is no established list of shark species other than someconfirmed sightings within the Gulf recorded during a surveyconducted in 2002 by the Environment Agency – Abu Dhabi(EAD) (Edwin Grandcourt, pers. comm.) and during a 10-dayvisit to a landing site in AbuDhabi byMoore et al. (2012a). Thisgeneral lack of knowledge on the number of shark species,composition and quantities of catches, and the amount of fishingefforts directed toward this fishery suggests that shark speciesrichness in the region could be higher than previously recorded.This is especially true since it has been shown around the worldthat with increased research and genetic studies, new species arebeing discovered and described at a rapid rate (Naylor et al.2012).

Globally, shark populations are facing increasing pressure,and the advancement of conservation measures requires infor-mation on their biodiversity and conservation status(Simpfendorfer et al. 2011). In the UAE, fishermen haveindicated a general decline in shark catches, abundance, andsize over the last two decades, suggesting that the sharkfishery is currently overexploited (Jabado et al. 2014). How-ever, protection of sharks in the Gulf is hampered by limitedavailable baseline scientific data, along with the challenge ofbalancing conservation efforts with the provision of essentialresources for growing coastal populations. In order to main-tain the ecological integrity of the Gulf, it is essential tounderstand and evaluate potential changes in the marine bio-diversity of this increasingly threatened aquatic ecosystem.

Here, we investigate the diversity of shark species capturedin the UAE artisanal fishery. We present the results of fishery-dependent market and fish landing site surveys that can aid inconservation initiatives both in the UAE and in the broaderregion. Specifically, we (1) examine patterns of species com-position, distribution, and relative abundance across sites; (2)investigate temporal and spatial variability in landings com-position; and (3) validate the field identification of each spe-cies through genetic analysis of a representative sample ofindividual species using the Cytochrome c oxidase subunit 1gene (COI). We conclude with a discussion of general impli-cations for the conservation of shark species in the Gulf.

Material and methods

Study sites

The Gulf is an epicontinental semi-enclosed sea lying in asubtropical zone with hyper-arid climate, stretching 1,000 km

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in length from the Shatt al-Arab waterway to the Strait ofHormuz, and varying in width from 75 to 350 km (Carpenteret al. 1997) (Fig. 1). The basin has an average depth of 35 m,gradually becoming deeper, to 100 m, as it approaches itsentrance (Sheppard et al. 1992). The marine environment isharsh and extreme, characterized by low hydrodynamic ener-gy; relatively shallow depths; high evaporation rates, surfacewater temperatures, and salinities; and minimal waterexchange.

The UAE lies along the southeastern Gulf coast and ex-tends to the Gulf of Oman between 22° and 26° N latitudeand 51° and 57° E longitude. The country’s coastline stretchesroughly 740 km, including some 650 km of the western Gulfcoast (EAD 2011). The main study area was along the Gulfcoastline of the UAE. From April through June 2010, severalexploratory market and landing site visits were carried out todetermine sites with the largest concentrations of shark land-ings. It was subsequently determined that this study wouldfocus on landing sites in the regions nationally defined asWestern (Mina Zayed, Abu Dhabi), Central (Jubail, Sharjah),and Northern (Maarid, Ras Al-Khaimah (RAK)). While sev-eral landing sites exist within each region, these three loca-tions are found along the Gulf coastline where vessels offloadtheir catches directly, facilitating the collection of informationon capture location. Vessels operating and offloading in thisarea fish exclusively in Gulf waters, and thus it was possible toensure that all species recorded were from the waters of theGulf and not the Arabian Sea. Furthermore, fishers fromnearby landing sites transport their landings to these marketsat the time of auction, enabling sampling of larger numbers ofspecimens during each survey. Species composition of land-ings from Dubai, as well as from specimens transported toDubai from these three regions, were opportunistically record-ed at the Dubai Deira fish market while conducting separatetrade surveys and were included in this analysis.

Market and landing site surveys

Site visits were made prior to the start of the main dailyauction, when the majority of landings were on display, andwere at different times: 04:30–08:00 in Abu Dhabi, 16:00–18:30 in Sharjah, 12:30–15:00 in RAK, and 17:00–20:00 inDubai. All sharks found at landing sites were caught fromUAE Gulf waters, whereas those found at markets weresometimes transported from other emirates or from Oman.Data were recorded on the origin of each shark at the markets,and only those captured in UAE waters were considered inthis study.

Data collection commenced in October 2010 and wasongoing until September 2012. With the exception of sites inDubai, each site was visited twice a month on a rotationalbasis until January 2012, when visits were reduced to once amonth. In Dubai, data were collected four times a month, and

then reduced to twice a month in January 2012. After plottingthe cumulative number of species present at each market visitagainst the number of market visits, it was determined thateven with a reduction in sampling frequency, surveys wouldbe sufficient to describe species composition at landing sites.Each visit lasted three to four hours, depending on the quantityof sharks landed. Specimens were always landed whole, andtherefore it was possible to identify them to the lowest possi-ble taxonomic level using keys from Carpenter et al. (1997),Compagno et al. (2005), and Last and Stevens (2009). Be-cause shark trade among the emirates does occur, sharkssampled were marked with cuts on their left gills, and visitsto markets did not occur on consecutive days and weeks inorder to avoid double-counting study specimens.

An analysis of species richness was undertaken usingJaccard’s similarity index to determine the percentage of spe-cies shared between landing sites (Magurran 2004). In addi-tion, landings composition was compared across seasons,which were defined as spring (March–May), summer (June–August), autumn (September–November), and winter (De-cember–February). Full seasons were sampled for both years,with the exception of autumn, which was sampled for twomonths in 2010 and one month in 2012 due to the limited timeframe of the project.

Genetic analyses

Tissue samples were collected from fresh animals at the foursampling sites. All samples were immediately placed inEppendorf Tubes, preserved in 95 % ethanol, and stored at−20 °C until required for analysis. To validate species identity,a set of 130 tissue samples comprising five samples from eachmorphologically identified species, when available, wereanalyzed.

Genomic DNA was extracted using the DNeasy Blood &Tissue Kit (Qiagen Inc., Valencia, CA, USA) from 25 mg offresh tissue collected from whole specimens, according tomanufacturer instructions. Extracted DNA was checked on0.8 % TBE agarose gels containing ethidium bromide forDNA quality and concentration. A DNA fragment from theCOI gene comprising approximately 650 bp was amplified byPCR using the individual primers Fish F1 (5’-TCAACCAACCACAAAGACATTGGCAC-3’), Fish F2 (5’-TCGACTAATCATAAAGATATCGGCAC-3’), Fish R1 (5’-TAGACTTCTGGGTGGCCAAAGAATCA-3’), and Fish R2 (5’-ACTTCAGGGTGACCGAAGAATCAGAA-3’) (Ward et al. 2005).

Amplification reactions were performed in 50-μL volumes,containing 1 μL of the extraction genomic DNA, 10 pmol ofeach primer, 10X PCR buffer (Qiagen Inc.), 50 μM dNTPsmix (Illustra dNTP set, GE Healthcare), 1 unit of HotStarTaqDNA Polymerase kit (Qiagen Inc.), and 33.3 μL HPLC puri-fied water (OmniSolv). The PCR thermal cycling employedwas: 95 °C initial denaturation for 15 min, followed by

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35 cycles of 94 °C for 1 min, 50 °C for 1 minute, 72 °C for2 min, and a 2-min final extension step at 72 °C. Amplifica-tions were performed using the BioRad iCycler thermal cy-cler. Amplified fragments were confirmed on 1.2 % agarosegel stained with ethidium bromide and viewed on a Foto/spectrum Transilluminator (FotoDyne). PCR reactions werecleaned with QIAquick PCR Purification Kit (Qiagen) andeluted in 30 μL of Buffer EB. For each sample, 10 μL ofcleaned cycle sequencing reaction per well was loaded in aMicroAmp 96-Well Reaction Plate (Applied Biosystems,USA), and sequencing was completed using the dye-labeledtermination method (BigDye Terminator v3.1, Cycle Se-quencing Kit, Applied Biosystems) on a 3130xl GeneticAnalyzer (Applied Biosystems) in either forward orreverse direction.

Sequences were inspected and cleaned of ambiguous basesby visualizing the corresponding chromatogram using theBioEdit program (Hall 1999). Species identification was per-formed using both the BOLD Identification Engine (www.boldsystems.org) and GenBank nucleotide database (www.ncbi.nlm.nih.ggoc/nucleotide). The BOLD and GenBankengines each matched uploaded sequences with otherspresent in their databases, and provided high specimensimilarity or maximum identity percentages, respectively,with matching sequences. All sequences were then alignedusing Clustal XI software and trimmed to 417 bp in order toinclude as many species in the analysis as possible without

compromising its power. Taxonomic clustering amongbarcoded samples was analyzed by constructingphylogenetic trees using three different methods: neighbor-joining (NJ), maximum likelihood (ML) and maximum par-simony (MP). Estimation of the NJ (Kimura two-parameterdistance model [Kimura 1980]) and MP trees was performedusing 1,000 bootstrap replications (MEGA 4) (Tamura et al.2007).

Results

Overall species composition

A total of 12,478 individual sharks originating from UAEGulf waters were recorded from 205 site visits. After 150visits, from which 28 species of sharks were confirmed, thefrequency of surveys was reduced, as it was determined thatextra market visits would not serve to increase the diversity ofspecies encountered. An additional two species were docu-mented in 2012, however, raising the number of confirmedspecies to 30, which consisted of nine families from threeorders (Table 1). The family Carcharhinidae was the mostdiverse, with 18 species, followed by Hemigaleidae withthree species, and Sphyrnidae and Hemiscylliidae withtwo species each.

Fig. 1 Map indicating thelocation of landing sites across theUAE where sampling wasundertaken

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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

n % n % n % n % n %

Hemiscylliidae

Chiloscylliumarabicum

NT 1 3 1 0 1 0.02 2 0.06 1 0.02 1 0.04 5 0.04

Chiloscylliumgriseum

NT 0 0 1 0 0 0.0 0 0.0 1 0.02 0 0.0 1 0.01

Ginglymostomatidae

Nebrius ferrugineus VU 0 0 2 0 0 0.0 1 0.03 0 0.0 1 0.04 2 0.02

Stegostomatidae

Stegostomafasciatum

VU 0 5 4 0 1 0.02 0 0.0 7 0.2 1 0.04 9 0.07

Rhincodontidae

Rhincodon typus VU 0 1 0 0 0 0.0 1 0.03 0 0.0 0 0.0 1 0.01

Odontaspididae

Carcharias taurus VU 1 0 0 0 0 0.0 0 0.0 1 0.02 0 0.0 1 0.01

Triakidae

Mustelus mosis DD 1 17 55 131 37 0.9 48 1.6 101 2.8 18 0.8 204 1.63

Hemigaleidae

Chaenogaleusmacrostoma

VU 2 7 23 28 8 0.2 25 0.8 21 0.6 6 0.2 60 0.48

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

Carcharhinusamblyrhynchoides

NT 33 8 41 8 15 0.39 6 0.2 62 1.7 7 0.3 90 0.72

Carcharhinusamblyrhynchos

NT 0 4 3 1 3 0.07 0 0.0 0 0.0 5 0.2 8 0.06

Carcharhinusamboinensis

DD 61 16 42 8 19 0.5 32 1.0 61 1.7 15 0.6 127 1.02

Carcharhinusbrevipinna

NT 8 33 17 8 6 0.15 12 0.4 36 1.0 12 0.5 66 0.53

Carcharhinusdussumieri

NT 136 63 212 150 187 4.94 189 6.3 96 2.7 86 3.8 561 4.50

Carcharhinusfalciformis

NT 0 6 0 0 6 0.15 0 0.0 0 0.0 0 0.0 6 0.05

Carcharhinusleiodon

VU 1 2 0 0 2 0.05 1 0.03 0 0.0 0 0.0 3 0.02

Carcharhinus leucas NT 93 44 18 12 19 0.5 62 2.0 68 0.0 18 0.8 167 1.34

Carcharhinuslimbatus

NT 906 300 516 64 581 15.3 455 15.3 516 14.7 234 10.4 1786 14.31

Carcharhinusmacloti

NT 0 60 11 102 73 1.93 42 1.4 43 1.2 15 0.6 173 1.39

Carcharhinusmelanopterus

NT 10 15 10 3 8 0.2 5 0.1 9 0.2 16 0.7 38 0.3

Carcharhinusplumbeus

VU 1 0 6 6 4 0.1 5 0.1 1 0.02 3 0.1 13 0.1

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 1 0.01

Loxodonmacrorhinus

LC 8 320 88 704 415 10.9 235 7.9 270 7.7 200 8.9 1120 8.98

Negaprion acutidens VU 30 3 7 1 19 0.5 4 0.1 11 0.3 7 0.3 41 0.33

Rhizoprionodonacutus

LC 818 870 989 1060 1315 3.46 1083 36.4 924 26.4 415 18.5 3737 29.95

Rhizoprionodonoligolinx

LC 0 0 1 11 4 0.1 8 0.2 0 0.0 0 0.0 12 0.1

Sphyrnidae

Sphyrna 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 recordedin AbuDhabi, Dubai, Sharjah, and Ras Al-Khaimah, based on their location of origin, seasonal and total catch composition (n=number of individuals; %of shark landings)

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Carcharhinids dominated landings in terms of number,with 95.5 % (n=11,922) of the total shark landings, followedby the triakids, consisting of one species, Mustelus mosis(Hemprich and Ehrenberg, 1899), but accounting for 1.6 %of the total landings. While the total number of species wasrelatively high, many of them were found only in smallquantities and landings were dominated by a few species.The most abundant species was Carcharhinus sorrah (Müllerand Henle, 1839), contributing 31.8 % to the total number ofsharks, followed by Rhizoprionodon acutus (Rüppell, 1837),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 alsorelatively abundant, contributing 14.3 %, 8.9 %, 4.5 %, and1.6 %, respectively, to the total shark numbers. The remaining24 species comprised between 0.01 % and 1.4 % of the totalshark landings.

Spatial and seasonal species composition

With respect to the 30 shark species identified, Sharjah wasthe region most rich in species, with a total of 26 species,followed closely by Dubai, with 24 species. RAK had 21species, while Abu Dhabi displayed the lowest species rich-ness, with 19 species recorded. With regard to the similarity inspecies composition among landing sites, Jaccard’s indexindicated that the degree of species overlap among regionswas moderately high, with regions sharing anywhere from60.7 % to 80.7 % of species (Table 2).

Although the sampling effort was consistent in each loca-tion and cross-seasonally, there was some degree of variabilityin the number of observed landings among regions and acrossseasons (Table 1). Among regions, Dubai had the fewest sharklandings, with 20.2 % of the total, followed by Abu Dhabiwith 22.5 %. When viewed from a regional perspective, theCentral region, comprising both the Dubai and Sharjah land-ing sites, contributed 49.5 % of the total number of landings.

There was no significant difference in the number of spe-cies across seasons, with 25 species recorded in autumn, 24 inboth winter and spring, and 23 in summer. There was varia-tion, however, in the total number of landings, with autumnyielding the highest number, with 30.3 % of the total captures,whereas a significant decline was observed in the summer

(17.8 %). The numbers also varied with regard to seasonalshark landings by site location. Abu Dhabi had the highestlandings in autumn (37.9 %), followed by winter (31.1 %) andspring (25.9 %), while almost no shark landings were record-ed in the summer (4 %). In Dubai, landings were stable duringautumn (30.9 %) and spring (32 %), but declined duringwinter (16.2 %) and summer (20.7 %). Landings in Sharjahwere relatively stable across seasons, although spring yieldedthe highest number, with 29 % of the total, followed bysummer (25.7 %), winter (23.8 %), and autumn (21.4 %).RAK showed a different pattern as well, with landingspeaking in autumn (32.7 %), followed by spring (27 %),winter (23 %), and summer (17.2 %). When landings in Dubaiand Sharjah were combined, Central region numbers showedsimilar patterns to RAK, with a peak in spring (30.2 %), butthen followed by autumn (25.3 %), summer (23.7 %), andwinter (20.7 %) (Fig. 2).

Overall species composition varied across locations andseasons. While six species dominated overall among the land-ings, some variability in the dominant species was noted withregard to regional occurrence and abundance (Fig. 3). Themost frequently observed species at all sites were C. sorrahand R. acutus. With the exception of landings ofM. mosis andC. macloti, the most abundant species were similar betweenDubai and Sharjah, and landings composition for these twosites were combined as the Central region.

Noteworthy species occurrence included M. mosis, ac-counting for a low proportion of catches in most locations(n=1 in Abu Dhabi) but common in RAK, thereby increasingits abundance in the national catch composition overall;C. macloti, which was absent in Abu Dhabi landings butwas recorded at all other locations across seasons, with58.9 % of catches recorded in RAK; C. leucas (Müller andHenle, 1839), which was found in catches across seasons butpredominantly in Abu Dhabi (55.6 %), where it was abundant;C. leiodon (Garrick, 1985), which was only present in Dubaiand Abu Dhabi in autumn and winter; C. falciformis (Müllerand Henle, 1839), which was recorded in Dubai in autumn butnot present at other landing sites or during other seasons;R. oligolinx (Springer, 1964), which was only found in RAK(n=11) and Dubai (n=1) during autumn and winter; and

Table 2 Jaccard’s similarity index values illustrating the degree of sim-ilarity in the species composition among sampling sites in the UAE

Abu Dhabi Dubai Sharjah Ras Al-Khaimah

Abu Dhabi * 0.65 0.60 0.66

Dubai * * 0.72 0.73

Sharjah * * * 0.80

Ras Al-Khaimah * * * *

0200400600800

100012001400160018002000

Abu Dhabi Dubai Sharjah Ras AlKhaimah

Central region

Num

ber

of s

hark

s

Location

Autumn

Winter

Spring

Summer

Fig. 2 Seasonal shark landings recorded for each landing site location,with Dubai and Sharjah landings shown separately as the Central region

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P. randalli, C. amblyrhynchos (Bleeker, 1856), and Sphyrnalewini (Griffith and Smith, 1834), which were not recorded inAbu Dhabi but present at other sites.

Range extensions and new species confirmations in the Gulf

Four previously unconfirmed species in this basin were re-corded, extending their current known distribution. They in-cluded the grey bamboo shark,Chiloscyllium griseum (Müllerand Henle, 1839); the tawny nurse shark, Nebrius ferrugineus(Lesson, 1830); the silky shark, C. falciformis; and the sand-bar shark, C. plumbeus (Nardo, 1827). Furthermore,Galeocerdo cuvier (Peron and Lesueur, 1822) andC. amblyrhynchoides specimens were confirmed for the firsttime in southern Gulf waters.

DNA Barcoding

DNA COI barcoding was attempted on 130 samples from the30 species identified morphologically in this study. The finalbarcode data set comprised 120 sequences from 29 species,with sequence lengths varying from 485 to 637 bp. Sequenceshave been deposited in the GenBank database under accessionnumbers: KM973088-KM973199. Ten samples were exclud-ed from the analysis: three of them yielded ambiguous speciesidentifications, while seven samples failed to provide good

sequences, including the only sample of C. griseum collected.All sequences were compared with those in BOLD and GenBankdatabases to confirm initial morphological identification, and theresults of matching sequences, along with the amplicon sizeproduced for each sample, are provided in Appendix A.

Genetic analysis based on morphological characteristics un-equivocally confirmed 24 species among those recorded in thisstudy. Of these, 12 sequences were the first available from theGulf for C. arabicum (Gubanov and Schleib 1980),N. ferrugineus, Stegostoma fasciatum (Hermann, 1783),Rhincodon typus (Smith, 1828), Carcharias taurus (Rafinesque,1810),C. amblyrhynchos, C. falciformis, C. melanopterus (Quoyand Gaimard, 1824), C. plumbeus, Negaprion acutidens(Rüppell, 1837), G. cuvier, and S. lewini. Taxonomic identifica-tion from barcodes, however, was ambiguous for five species.

Only two of five samples of C. arabicum provided goodsequence quality, and although results from both BOLD andGenBank assigned these sequences to the Chiloscyllium ge-nus, species resolution was not possible. Rhizoprionodonoligolinx sequences provided a 100 % match with the samespecies in BOLD, but the closest match in GenBank was 93%with R. porosus (Poey, 1861). For P. randalli andChaenogaleus macrostoma (Bleeker, 1852), there was noconsistency in the nomenclature of records between BOLDand GenBank. Finally, although sequences for C. limbatussamples had slightly different barcodes between them, they all

29.9%

31.8%

14.3%

8.9%

4.5%

1.6%

8.7%

29.7%

33.2%

19.7%

4.2%3.6%

1.8% 7.5%

29.1%

21.9%32.2%

4.8%

3.3% 2.8% 5.7%

30.4%

35.6%

13.3%

6.6%

4.5% 0.9%7.5% 0.9%

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 leftshows the overall species composition for the three regions combined.

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matched this species in both databases. However, sequencesfrom C. amblyrhynchoides yielded ambiguous results, andmatched both C. limbatus and C. amblyrhynchoides.

Taxonomic clustering

While there were differences in classifications at the familyand order levels, all three trees provided similar outcomes interms of taxonomic clustering. In all trees, specimens fromdatabase sequence matches that could have been eitherC. limbatus or C. amblyrhynchoides were all assigned to onecluster and were not distinguishable. Some P. randalli andC. macrostoma samples clustered as one species, while oneC. macrostoma sample stood out as a separate species. Resultsbased on the NJ tree are illustrated in Appendix B.

Discussion

This fishery-dependent assessment is the first comprehensivestudy on shark species found in southern Gulf waters, and ithas enabled the development of an updated regional checklistof species by providing an overview of the composition ofshark landings at various sites in the UAE. The study greatlyimproves the current knowledge regarding species richness,relative abundance, and distribution of sharks exploited by theUAE fishery. Although data are still incomplete, and in somecases insufficient to draw conclusions regarding the abun-dance and conservation status of each species in the region,our results indicate that sharks are an important component ofthe marine biodiversity of the Gulf. Here, we discuss thevarious results from this study and their implications for sharkconservation in the region, and then offer some recommenda-tions for further study and management measures.

Species diversity and occurrence

The latest annotated checklist confirmed the presence of 26shark species in the Gulf (Moore et al. 2012b). The presentstudy has raised this number to 31 and has validated theoccurrence of species such as C. griseum, C. plumbeus,N. ferrugineus, and C. falciformis that had been previouslymentioned in the literature but with no supporting evidencesuch as photographs or samples (Gubanov and Schleib 1980;Randall 1986; Bishop 2003; Compagno et al. 2005). Since thenumber of species encountered rose very little after the firstyear of study, it is likely that the actual species composition ofsharks in the region, along with the abundant species found inUAE Gulf waters, have been accurately documented. How-ever, it is important to note that these surveys may haveunderestimated protected, discarded, rare, or even migratoryspecies. For instance, while only one whale shark, R. typus,

was recorded in this study, that species has historically beenreported in the Gulf, and more recently, large aggregationshave been documented in the offshore waters of Qatar (Rob-inson et al. 2013). While incidental bycatch of this speciesmay still occur, they presumably go unreported or catchesmay not be retained since they are protected in the UAE(Jabado et al. 2014). Similarly, reports of C. melanopterusfrom the Gulf are widespread, but few specimens have beenconfirmed (Gubanov and Schleib 1980; Bishop 2003). Mooreet al. (2011) suggested that this species may have been re-placed by C. leiodon in shallow water habitats of the Gulf.However, in the UAE, C. melanopterus is common aroundmany coastal and offshore islands (RWJ, personal observa-tion) where fishing is prohibited, and the low number ofsharks (n=38) recorded in this study may not reflect theirabundance. Furthermore, as noted by Jabado et al. (2014),most carpet shark species with low market value, such asC. arabicum and S. fasciatum, are generally discarded at seaand thus are presumably not accurately represented in land-ings. This could also be due to fishing practices and thepositioning of fishing gear, which may preclude the captureof demersal or bottom-associated species such as these. Final-ly, it is possible that other, less abundant species or seasonalmigrants would have been documented if more frequent sam-pling had been undertaken or if the study had focused oncertain remote areas where targeted shark fisheries were pres-ent. For instance, the C. taurus in this study was reportedopportunistically when a fisherman showed the project inves-tigator pictures of his catches on an offshore island in AbuDhabi (Jabado et al. 2013).

The presence of species documented in this study that hadnot been previously reported from southern Gulf waters, in-cluding C. amblyrhynchos and G. cuvier, may indicate thatthey are either less abundant or migratory. For instance, theC. leiodon specimens were recorded only in November andDecember, suggesting that this species may be present in thesewaters during limited times of the year (Moore et al. 2013). Todate, however, the only evidence of the occurrence ofN. acutidens was from a photograph in Saudi Arabia (Bassonet al. 1977). The collection of 41 individuals during thepresent study suggests that this species is more common thanpreviously thought. Finally, the actual number of shark spe-cies in the Gulf may be even higher, as the sighting of athresher shark, Alopias sp., was reported by a diver at anoffshore wreck in Dubai. It was recognized based on its‘shark’ appearance and its elongated tail (David Holdman,pers. comm.), a characteristic feature in this family of sharks(Compagno et al. 2005). While verification of this sighting isnot possible, it is important to note that thresher sharks havebeen reported in the literature, and the remains of four caudalvertebrae belonging to threshers have been documented atarcheological sites in AbuDhabi (Beech 2004b). Furthermore,both the pelagic thresher, Alopias pelagicus (Nakamura,

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1935), and the big eye thresher, A. superciliosus (Lowe,1841), are present in Omani waters (Henderson et al. 2007).

Considering that the Gulf is regarded as a highly stressfulenvironment for many species, the total number of sharkspecies recorded from this study is high. Indeed, studies fromthe Red Sea, an enclosed body of water considered a marinebiodiversity hotspot, have confirmed only 29 species of sharks(Golani and Bogorodsky 2010; Spaet et al. 2011). Surveysconducted in Omani waters have documented 36 shark spe-cies from the Arabian Sea, while 34 species have been report-ed in the Maldives (Anderson and Ahmed 1993; Hendersonand Reeve 2011). However, compared with other countries inthe broader Indian Ocean region such as India, which hasdocumented 66 shark species, and Sri Lanka with 61 species,the species richness in the Gulf is significantly lower (Joseph1999; Raje et al. 2002; Herath 2012). This may be due to avariety of reasons, including the diversity of fishing gear usedin other countries as well as exploited habitats. Indeed, incountries that fish in the Gulf, operations are characterizedby artisanal fisheries limited to wooden dhows and fiberglassdories using traditional gear (Carpenter et al. 1997), whereasother countries in the region utilize a diversity of fishingvessels that operate with a variety of gear at different depths(Joseph 1999).

The limited bathymetry of the Gulf likely precludes habi-tation by deepwater species such as the bramble shark,Echinorhinus brucus (Bonnaterre, 1788), that has been docu-mented in Oman, or even small species favoring deep waters,such as the bigeye hound shark, Iago omanensis (Norman,1939), that are commonly found in the Arabian Sea (Hender-son et al. 2007; Javadzadeh et al. 2010; Henderson and Reeve2011). The global deepwater chondrichthyan fauna, for exam-ple, is highly biodiverse yet remains largely undocumented(Kyne and Simpfendorfer 2007). Several studies have nowindicated that shark species richness can be affected by bothbottom-water temperature and depth, with distinctive faunacharacterized by spatial distribution of species (Menni et al.2010; Guisande et al. 2013). Therefore, since the deepestwaters in the Gulf are close to the Strait of Hormuz, wherethere is a lack of fisheries data and research, it is possible thatshark species not previously recorded for this basin may bepresent, and that these could be subdivided based on differentvariables such as depth and temperature.

Carcharhinidae was the dominant species (95.5 %) amonglandings investigated in this study. It has been shown that thisfamily is very important in both commercial and artisanalfisheries across the world, and species within the familydominate shark landings in many tropical areas (Castillo-Geniz et al. 1998; Compagno et al. 2005; Henderson et al.2007; White 2007; Last and Stevens 2009). The most abun-dant species recorded in this study, C. sorrah and R. acutus,are also widespread regionally, dominating landings in areaswhere they occur (Krishnamoorthi and Jagadis 1986;

Anderson and Ahmed 1993; Bonfil 2001; Capapé et al.2006; Henderson et al. 2007; FAO 2009; Last and Stevens2009; Moore et al. 2012a).There are few available historicalrecords of C. limbatus in the Gulf region, and it is not fre-quently found in landings from Kuwait, Qatar, or Bahrain(Moore et al. 2012a; Moore and Peirce 2013). However, itrepresents one of the eight most abundant species in Omanilandings (Henderson et al. 2007), which is consistent withfindings in this study. Loxodon macrorhinus has been docu-mented in Oman landings as the third most abundant, and inMaldives, where it represented 70 % of sharks caught basedon a research survey (Anderson and Ahmed 1993). During thefirst year of their study, Henderson et al. (2007) noted thatL. macrorhinus was absent from landings in Al Batinah, AlWusta, and Musandam, but subsequently became the mostabundant landed species in Musandam. In our study, individ-uals were recorded from all sites and were most common inRAK (comprising 62.8 % of landings), which is situatedadjacent to the Musandam Peninsula. However, they wererare in Abu Dhabi (n = 8), and it is likely that the high numberof records from Abu Dhabi (155 individuals) reported byMoore et al. (2012a), which lack information regarding theirplace of capture, reflect the transport of sharks overland fromother areas in the UAE or Oman for sale at the market(unpublished data). Reports of C. dussumieri suggest that thisspecies is widespread and abundant in the Gulf, especially inKuwait and Iran, although it is not frequently recorded inBahraini or Omani landings (Blegvad and Loppenthin 1944;Basson et al. 1977; Gubanov and Schleib 1980; Hendersonet al. 2007; FAO 2009; Moore et al. 2012a; Moore and Peirce2013). Mustelus mosis has been reported in various publica-tions (Blegvad and Loppenthin 1944; Basson et al. 1977;Gubanov and Schleib 1980), but information regarding itsabundance remains scarce. Moore and Peirce (2013) noted itas the secondmost abundant species from landings in Bahrain,and while it was documented in Oman by Henderson et al.(2007), no details were provided regarding its occurrence.

All species reported from Kuwait, Qatar, and Bahrainlandings were also present in UAE landings (Moore et al.2012a; Moore and Peirce 2013). The lower number of speciesrecorded in northwestern Gulf surveys may be a result of thelimited temporal sampling there, which occurred only duringApril. Indeed, even in the UAE, some species were recordedonly at specific times of the year, such as C. falciformis in theautumn months. Furthermore, with the exception of the twoChiloscyllium species, N. ferrugineus, and R. oligolinx, themajority of species reported here were also documented inOmani landings (Henderson and Reeve 2011).

Spatial and seasonal distribution

A total of 26 species of sharks were recorded in Sharjah, whileonly 19 species were recorded in Abu Dhabi, and these two

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sites had the lowest species overlap. While these differencesare likely not due to fishing methods utilized, since similargear is used across the country, they may be explained by thevariability in fishing grounds used by fishermen in these twoemirates and differences in habitat and environmental condi-tions in the two areas. Although Abu Dhabi waters includesome offshore islands with deeper waters, most of the westerninshore is characterized by shallow embayments with higherwater temperatures and salinities (EAD 2011). On the otherhand, fishermen in Sharjah largely utilize offshore and deeperwaters towards the northeastern UAE region, which aresupplied with oceanic water inflowing from the ArabianSea (Price 1993). Studies have shown that the richest areasfor fish fauna within the Gulf are closer to the Strait ofHormuz, where waters are deeper (Price 1993). The simi-larities in species recorded for Sharjah, RAK, and evenDubai likely reflect the use of similar fishing grounds.Landings of M. mosis, on the other hand, were notable inRAK but less frequent in Dubai and Sharjah, potentiallyindicating a difference in species behavior.

While there were some seasonal variations in the number ofspecies caught, the overall dominant species did not changethroughout the sampling period. However, there was a shift inseasonal dominance between C. sorrah and R. acutus, whereC. sorrah was more common during spring and summer,while R. acutus was more abundant in autumn and winterlandings. All other species were caught in lower numbersduring the summer, which was also the season that yieldedthe lowest number of landed species overall, comprising only17.8 % of total landings. Studies on demersal teleost fishspecies in the Gulf show patterns of distribution and abun-dance that vary seasonally and among habitat types (Bassonet al. 1977; Shallard and Associates 2003). Grandcourt (2012)suggested that this was likely due to higher water temperaturesduring the summer and the lower volume of fishing activity atthat time of the year. In fact, it is believed that the reducedabundance of reef fish during the summer is a result of themovement of species to deeper and cooler waters (Shallardand Associates 2003). Some studies have shown that the mostcommon species of sharks can change seasonally (Bizzarroet al. 2009). Data from the artisanal shark fishery in Mexicoshowed landings that were highly seasonal and that variedamong regions, which was attributed to the migratory behav-ior of various species of sharks (Castillo-Geniz et al. 1998).Similarly, landings in Oman showed marked differencesamong seasons and across survey sites, also believed to be aresult of the migration patterns of different shark species(Henderson et al. 2008). Lastly, seasonal differences inlandings may be due to variations in relative abundanceof shark species in local waters. Indeed, as fishermenwere found to be highly opportunistic, and as most areaswithin UAE waters have been utilized for fishing, thespecies composition of landings across seasons and

locations likely are a true reflection of local relativeabundance (Jabado et al. 2014).

With the exception of C. limbatus, the dominant species inthe UAE are relatively small sharks, measuring less than1,500 mm LT, that commonly form large schools in inshorewaters (Compagno et al. 2005; Last and Stevens 2009). Whilelittle is known about the behavior of M. mosis, it most likelyforms groups in inshore areas in a similar fashion to otherspecies of triakids known to be abundant in coastal waters(Compagno et al. 2005). Likewise, C. limbatus, a larger sharkreaching over 2,500 mm LT, is known to prefer inshore areasand is commonly found in large surface schools (Compagnoet al. 2005). This aggregating behavior and preference forinshore waters may explain the particularly high abundanceof these species in landings. Similarly, the market dominanceof predominantly small-bodied sharks from a limited numberof species has been recorded in other areas. Data from Omanhave reported that the dominance of eight species amonglandings (Henderson et al. 2007). Five species represented64 % of landings in the northeastern Gulf (Moore et al.2012a); three species were dominant in Iran (FAO 2009); 12species were most abundant in Sri Lankan catches (Herath2012); and five species comprised up to 90 % of sharkspecimens recorded in Chinese markets (Lam and Sadovyde Mitcheson 2011). In this study, while some species oflarge-bodied sharks were found in landings, they were largelyeither immature specimens (unpublished data), such asC. limbatus, or species that did not contribute substantiallyto landings, such as C. brevipinna and S. mokarran.

While little information is available on whether largersharks were more common at one time, fishermen have statedthat the size of sharks in the Gulf has greatly diminished(Jabado et al. 2014). As such, it is possible that many largerspecies have been overfished to some extent, and that thefishery is now reliant on smaller sharks that are dominant inlandings. It is important to note that individual species mayhave different levels of susceptibility or resilience to exploi-tation (Stevens et al. 2000; Bonfil 2001). Small-bodiedcarcharhinids such as R. acutus tend to grow fast, matureearly, have short life spans, and display aseasonal reproductivecycles (Wourms 1977; Stevens and McLoughlin 1991). Onthe other hand, larger sharks such as C. brevipinna maturemuch later and exhibit slower growth rates, while typicallydisplaying seasonal breeding cycles and producing annual,biennial, or triennial litters (Wourms 1977; Last and Stevens2009). Thus the overall life history traits of small shark speciesgenerally lead to higher biological productivity, making themless susceptible to fishing pressure, which may explain theirdominance at various markets. Musick et al. (1993) noted thatoverexploitation of large sharks in areas off southeasternAfrica and the northwest Atlantic could have led to the pro-liferation of small-bodied sharks. A declining trend in thenumber of large sharks and a shift in efforts towards smaller

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individuals have also been documented inMexico, China, andMadagascar, where species composition of landings for thewhole area has been affected (McVean et al. 2006; Bizzarroet al. 2009; Lam and Sadovy de Mitcheson 2011). Hendersonet al. (2007) documented such a shift in the Omani sharkfishery, where in just a few years, larger sharks such asC. limbatus and S. lewini were displaced by the smallerL. macrorhinus and C. macloti.

A change in species composition or size of fished sharkscould have serious implications for the sustainability of afishery (Stevens et al. 2000). Furthermore, population studiesof coastal shark species have indicated that even a slightincrease in juvenile mortality can greatly impair the sustain-ability of coastal shark fisheries (Cortes 1998). It is wellknown that anthropogenic impacts such as overfishing andhabitat degradation have altered populations of sharks aroundthe world (Stevens et al. 2000). The risk to many species isalso believed to be depth-related, where species occupyingshallower waters are more accessible to fishing activities(Dulvy et al. 2014). Considering the relatively small size andshallow depth characteristics of the Gulf, as well as the in-creasing anthropogenic disturbances that this entire basin isfacing, it is important to monitor shark catches in the UAE inorder to document changes in species and size composition ofshark landings.

Species identification

A complete and reliable taxonomic account of shark species isthe most crucial, albeit challenging, aspect of fishery sam-pling, and is an integral component of effective fishery man-agement, as it allows identification of species richness anddiversity (White and Last 2012). In many instances, molecularmethods such as the use of the COI gene sequence havebecome important identification tools for distinguishing be-tween closely related species (White and Last 2012). In mostcases here, morphologically identified species were congru-ently matched in the BOLD and GenBank COI databases andconspecific species clustered together in the NJ analysis.However, some questions about specimen identificationremain.

The inability to assign C. arabicum to a species in eitherdatabase is due to the fact that a barcode for this species is notavailable for comparison. Similarly, the lack of a match forR. oligolinx in GenBank also indicates a lack of sequences forthis species within the database. The clustering of P. randalliand C. macrostoma sequences that also matched P. tengi(Chen, 1963), a species that has not been recorded from thewestern Indian Ocean (Compagno et al. 2005), may be due toa variety of reasons, including the possibility that these speciesshare haplotypes, or that there was misidentification in thefield, mislabeling errors for the samples, or misidentification

of species associated with COI sequences in the databases(White and Last 2012).

The success of barcoding is dependent upon low levels ofsequence variation within species and much higher levelsbetween species (Holmes et al. 2009). As such, some closelyrelated species may not be easily identifiable despite theirmorphological differences. In our study, the C. limbatus andC. amblyrhynchoides species pair could not be convincinglydifferentiated by barcoding. Ward et al. (2008) reported lowCOI sequence divergence and low bootstrap support for thesespecies, and Moore et al. (2011) stated that the COI gene wasbarely distinguishable between them. Similar outcomes werealso reported for the closely related species C. plumbeus andC. altimus (Springer, 1950), leading to the conclusion that theCOI barcode may not be suitable for discriminating amongsome closely related shark species, and that an additionalmarker with a higher rate of evolution would be necessary(Ward et al. 2008).

It has been recommended that developing a voucher col-lection is a necessity when undertaking genetic analysis inorder to resolve questions about specimen identification(Ward et al. 2005). A collection could not be started in thisstudy because of limited resources and lack of storage facili-ties necessary when dealing with large animals such as sharks.Only one study has focused on developing a specimen andbarcode collection for fish species in the Gulf, which includedtwo shark species, C. macrostoma and M. mosis (Asgharianet al. 2011). Therefore, it seems that to better understand theevolution of species within the Gulf, a centralized facilitywould be warranted.

Considerations for shark conservation

A number of species considered to be of global conservationconcern were recorded in this study, including C. limbatus,C. dussumieri, C. falciformis, C. plumbeus, S. lewini, andS. mokarran, which are listed either as threatened or NearThreatened on the IUCN Red List (IUCN 2012). However,because IUCN assessments generally lack information fromthe Gulf, accurate data obtained locally are needed to deter-mine which species here are most threatened. While datacollected in this study are not a clear indication of the statusof shark stocks in the UAE, they do provide a baseline thatshould prove beneficial for effective future monitoring andsustainable exploitation of targeted shark stocks. Results sug-gest that there may be a depletion of larger shark species inthese waters, where there is a clear lack of species-specificregional life history data and quantitative mortalityassessments.

While some laws for shark management already exist in theUAE, they should be reexamined in light of the data gatheredfrom this study and before unmonitored catches further com-promise the recovery of already-depleted stocks in the Gulf.

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Globally, the conservation of sharks has been confounded bydelayed responses regarding fishery restrictions, typicallyresulting in the implementation of management strategiesfollowing overexploitation of targeted shark populations (Ste-vens et al. 2000). Although there is no baseline informationwith which to compare the results from this study, all of thedata here and from interviews with Emirati fishermen indicatethat there is a high level of pressure on shark populations inUAE Gulf waters (Jabado et al. 2014). In view of the lifehistory traits and the possible detrimental impacts of fishingon many shark species, a precautionary approach to managingthese resources is warranted.

Acknowledgments We are grateful for the grant from the United ArabEmirates University to Rima W. Jabado that supported this project. Thegenetic analysis of the samples was supported by the Save Our SeasFoundation. We are grateful to Kimberley Atwater for the laboratorygenetic work and to the volunteers who participated in the field surveys,without whom this study would not have been possible.

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