Species, Sex, Size and Male Maturity Composition of Previously Unreported Elasmobranch Landings in Kuwait, Qatar and Abu Dhabi Emirate

Home , Bigeye houndshark, Chaenogaleus, Cowtail stingray, Golden cownose ray, Graceful shark

Journal of Fish Biology (2012) doi:10.1111/j.1095-8649.2011.03210.x, available online at wileyonlinelibrary.com

Species, sex, size and male maturity composition of previously unreported elasmobranch landings in Kuwait, Qatar and Abu Dhabi Emirate

A. B. M. Moore*†‡, I. D. McCarthy*, G. R. Carvalho§ and R. Peirce

*School of Ocean Sciences, Bangor University, Askew Street, Menai Bridge, Anglesey, LL59 5AB, U.K., †RSK Environment Ltd., Spring Lodge, 172 Chester Road, Helsby, Cheshire, WA6 0AR, U.K., §Molecular Ecology & Fisheries Genetics Laboratory, Environment Centre for Wales, Bangor University, Deiniol Road, Bangor, Gwynedd LL57 2UW, U.K. and Shark Conservation Society, Dulverton House, 8 Crooklets, Bude, Cornwall, EX23 8NE, U.K.

This paper presents data from the first major survey of the diversity, biology and fisheries of elasmobranchs in the Persian (Arabian) Gulf. Substantial landings of elasmobranchs, usually as gillnet by-catch, were recorded in Kuwait, Qatar and the Emirate of Abu Dhabi (part of the United Arab Emirates), although larger elasmobranchs from targeted line fisheries were landed in Abu Dhabi. The elasmobranch fauna recorded was distinctive and included species that are undescribed, rare and have a highly restricted known distribution. Numerical abundance was dominated by sharks (c. 80%), of which carcharhinids were by far the most important. The milk shark Rhizoprionodon acutus and whitecheek shark Carcharhinus dussumieri together comprised just under half of all recorded individuals. Around 90% of recorded sharks were small (50–90 cm total length, LT) individuals, most of which were mature individuals of species with a small maximum size (<100 cm LT), although immature individuals of larger species (e.g. Carcharhinus sorrah and other Carcharhinus spp.) were also important. The most frequently recorded batoid taxa were cownose rays Rhinoptera spp., an undescribed whipray, and the granulated guitarfish Rhinobatos granulatus. The first size, sex and maturity data for a wide range of Gulf elasmobranch species are presented (including LT at 50% maturity for males of four shark species) and include some notable differences from other locations in the Indo-West Pacific Ocean. A number of concerns regarding the sustainability of the fishery were highlighted by this study, notably that most of the batoid species recorded are classed by the IUCN Red List as vulnerable, endangered, data deficient or not evaluated. Despite their considerable elasmobranch landings, none of the three countries sampled have developed a ‘Shark Plan’ as encouraged to do so under the FAO International Plan of Action: Sharks. Furthermore, Kuwait and Qatar currently report zero or no elasmobranch landings to the FAO. © 2012 The Authors Journal of Fish Biology © 2012 The Fisheries Society of the British Isles

Key words: batoid; by-catch; discards; ﬁshery; gillnet; shark.

INTRODUCTION In response to major concerns about their status globally, research on elasmobranch diversity, conservation, ecology and ﬁsheries has ﬂourished in recent years (Dulvy et al., 2008; Clarke, 2009; Simpfendorfer et al., 2011). Much of this activity, however, has tended to focus on a few regions often associated with developed countries. This leaves large areas that are still poorly known: for example, elasmobranch

‡Author to whom correspondence should be addressed. Tel.: +44 (0)1928 728138; email: [email protected] 1 © 2012 The Authors Journal of Fish Biology © 2012 The Fisheries Society of the British Isles 2 A. B. M. MOORE ET AL.

Iraq Iraq Iran Pakistan Saudi Arabia Kuwait Shatt al Arab Gulf Gulf of Oman

29° Sharq Red Se Fahaheel Oman Iran a Yemen Arabian Sea Gulf of Aden

Bahrain Strait of Hormuz The Gulf 26° Al Khor Doha Qatar Saudi Arabia Gulf of Abu Dhabi Oman

0 50 100 200 U.A.E. Oman km

49° 53° 56°

Fig. 1. Map of The Gulf showing political boundaries and the locations sampled during the current survey. research is lacking in the Indian Ocean, despite high and increasing reported landings (Anderson & Simpfendorfer, 2005). In Arabian waters, Oman has led the efforts to characterize the diversity, biology and fisheries of its elasmobranch fauna in the Gulf of Oman and the Arabian Sea, both through landings-based and fisheries-independent data (Henderson et al., 2006, 2007, 2009; Henderson & Reeve, 2011). The elasmobranchs of The Gulf (Fig. 1) have received little attention, however, and are poorly understood (Moore, 2011). A number of concerns about Gulf elasmobranchs have been highlighted including the role of the Islamic Republic of Iran and the United Arab Emirates (U.A.E.) as major contributors to global elasmobranch landings and shark-fin exports, respectively, a possible increase in demand for meat and cartilage locally, as well as a possible fisheries-related change in elasmobranch community composition along the Iranian coast since the 1970s (Moore, 2011). In addition to research efforts, since 1999, the United Nations Food and Agricul- ture Organisation (FAO) has encouraged all states catching elasmobranchs in either targeted or by-catch fisheries to voluntarily participate in the International Plan of Action for the Conservation and Management of Sharks (IPOA-Sharks) and to have developed a ‘Shark-Plan’ by 2001 (FAO, 1999). The IPOA-Sharks is aimed at ensur- ing the sustainable use of all chondrichthyans and places particular emphasis on the importance of catch data to support this aim (FAO, 1999). All of The Gulf states (i.e. Bahrain, Iran, Iraq, Kuwait, Qatar, Saudi Arabia and the U.A.E.; excluding Oman here, whose coastline is largely non-Gulf) operate a range of fisheries for teleosts and invertebrates, including extensive gillnetting (Bishop, 2002). In addition, there are some reports of targeted elasmobranch fisheries in Gulf waters of the U.A.E. (Anderson & Simpfendorfer, 2005). As such, all Gulf states can be assumed to be

© 2012 The Authors Journal of Fish Biology © 2012 The Fisheries Society of the British Isles, Journal of Fish Biology 2012, doi:10.1111/j.1095-8649.2011.03210.x ELASMOBRANCHS IN KUWAIT, QATAR AND ABU DHABI 3 catching elasmobranchs to some degree in their fishing activities, although to date none have adopted a Shark-Plan (FAO, 2011a). Kuwait and Qatar have either not reported elasmobranch landings or reported zero values to the FAO (FAO, 2011b). The U.A.E. has reported landings to the FAO since 1986 (FAO, 2011b), and Abu Dhabi Emirate publishes data on elasmobranch landings (by port, gear and vessel type, and month) as part of annual fisheries statistics (Environmental Research & Wildlife Development Agency, 2005; Environment Agency Abu Dhabi, 2010). The value of these data in assessing the composition of elasmobranch landings is com- promised, however, by broad and unspecified reporting, such as of ‘sharks and rays’ or similar broad taxonomic groupings. Given the concerns noted above and the paucity of data and management locally, there is a clear need for basic information on the diversity, size composition, reproductive biology and fisheries of Gulf elasmobranchs (Moore, 2011). Surveys of fish markets and landing sites have provided a rapid and relatively inexpensive source of important data for elasmobranchs elsewhere on a range of aspects including reproductive biology, fisheries and new species (White & Dharmadi, 2007; Bizarro et al., 2009; Last et al., 2010a). In order to address local data gaps, the current paper reports species, size and sex composition, male maturity and fisheries of elasmobranchs recorded at landing sites and markets at three locations approximately equidistant along the Arabian coastline of The Gulf, i.e. Kuwait (north-western Gulf), Qatar (southern) and Abu Dhabi Emirate, of the U.A.E. (south-eastern) (Fig. 1). The results comprise the first major survey of elasmobranch diversity, biology and fisheries in The Gulf and form an important addition to knowledge on the relatively poorly known status of elasmobranchs in the western Indian Ocean.

MATERIALS AND METHODS

STUDY REGION The Gulf (Fig. 1) is a shallow (average depth 35 m), semi-enclosed offshoot of the north- west Indian Ocean, connected to the much deeper Gulf of Oman (>3000 m), and subsequently the Arabian Sea, through the narrow Strait of Hormuz. The Gulf is a harsh environment, ◦ and in some cases can be subject to extremes of water temperature (4–39 C) and salinity (brackish to >70); the single major freshwater input discharges into the north-west Gulf through the Shatt al Arab near northern Kuwait (Sheppard et al., 1992; Carpenter et al., 1997). In general, coastal waters of Qatar and the Emirate of Abu Dhabi (the largest in the U.A.E.) are characterized by extensive shallows of <20 m, while waters off Iran (not sampled in this study) slope more steeply than off Arabia. Dominant substrata are mud off Iran and Kuwait and sand off Qatar and the U.A.E. Seagrass is abundant in the southern Gulf but coral reefs and mangroves are relatively unimportant in The Gulf (Sheppard et al., 1992; Carpenter et al., 1997).

DATA COLLECTION The data presented in this study are based on annual Shark Conservation Society (SCS) expeditions to The Gulf between 2008 and 2010 and an additional separate trip in 2011. Timing and location of each of the four sampling events was planned to provide information on within-Gulf patterns at a comparable time of year, i.e. spring (April), as well as variability at the same location (Kuwait) between years (2008 and 2011). Elasmobranch specimens were examined on daily visits to both ﬁsh markets and landing sites in Kuwait (10–24 April 2008 ◦ ◦ ◦ ◦ and 1–15 April 2011) at Sharq (29 23 N; 47 58 E) and Fahaheel (29 04 N; 48 08

◦ ◦ E); in Qatar (12–29 April 2009) at Corniche, Doha (25 17 N; 51 32 E), Doha main ◦ ◦ ◦ ◦ wholesale market (25 17 N; 51 32 E) and Al Khor (25 41 N; 51 31 E); and in the ◦ U.A.E. (Abu Dhabi Emirate) (5–11 April 2010) at Abu Dhabi City (Mina Zayed) (24 30 ◦ N; 54 22 E) (Fig. 1). Elasmobranchs were openly sold in Kuwait in 2008, but in 2011, the Public Authority for Agriculture and Fisheries (PAAFR) was actively enforcing a ban on their sale in the market, so most sampling was performed at the quayside. Further brief SCS visits were made to Qatar (Doha wholesale market) in April of both 2010 and 2011, although these were not sampled and only photographs were taken for later evaluation of broad species composition. A planned SCS market survey to Bahrain in April 2011 was postponed as a result of political unrest. All specimens were identified and measured to the nearest cm using total length (LT, upper caudal fin lobe straightened along the body axis) for sharks and guitarfishes (i.e. Rhinidae, Rhi- nobatidae and Rhynchobatidae), or disk width (WD) for rays (i.e. all non-guitarfish batoids). Sex was recorded and apart from a few instances [including eight pregnant whitecheek shark Carcharhinus dussumieri (Muller¨ & Henle, 1839)], male and female elasmobranchs were not routinely dissected for macroscopic examination of the reproductive tract owing to logistical constraints. For male sharks, maturity was categorized based on a slightly adapted version of the scale in Henderson et al. (2006) but using only external examination of claspers. The classes used were juvenile (i.e. claspers undeveloped, not extending beyond posterior tips of pelvic fins), maturing (extending beyond posterior margin of pelvic fin, but flexible and not fully calcified) and mature (much longer than pelvic-fin rear margin, rigid). From this, a male maturity size range was derived for each species, from the size of the smallest maturing individual to the size above which all males were mature. These data were also used to con- struct maturity ogives and LT at 50% maturity (LT50). For rays, only the size above which all individuals were deemed mature (i.e. fully developed, rigid claspers) is presented here; male maturity data for guitarfishes are not presented as claspers can remain flexible in mature animals (A. Henderson, pers. comm.).

DATA ANALYSIS For those species where a total of >100 individuals were recorded (seven sharks and three batoids) the size-frequency distributions for each sex were tested to see if data conformed to a normal distribution using an Anderson–Darling test. Dependent on whether data were distributed normally or not, intergender size differences were then investigated using either a two-tailed t-test or a Mann–Whitney U-test, to test for possible sex-based differences in fisheries landings. The Mann–Whitney U-test was further used to investigate possible geographic and temporal differences in landed size for both sexes between sampling events in the two most commonly recorded species, i.e. milk shark Rhizoprionodon acutus (Ruppell,¨ 1837) and C. dussumieri. Size-frequency distributions of males and females were compared using a χ 2 contingency test with the size distribution divided up into 5 or 10 cm size class intervals as appropriate to the LT of the species under consideration. To test the null hypothesis of sex ratios being at parity for each sampling event, a χ 2 test was performed for each species. For male sharks with a sample size of >200, LT50 was calculated using the logistic equation −K(LT−LT50) −1 Y = x + (z − x)(1 + e ) ,whereY is the percentage of males mature in the LT size class (cm) and K, x and z are constants. The equation was fitted using the non-linear curve fitting programme in Minitab v14 (www.minitab.com). The relationships between C. dussumieri maternal LT and both litter size and mean embryo LT were investigated using correlation analysis.

RESULTS

IDENTIFICATION AND TAXONOMY A total of 4649 elasmobranchs were examined during the survey (Table I). The vast majority of individuals were successfully identiﬁed to species level, with two

© 2012 The Authors Journal of Fish Biology © 2012 The Fisheries Society of the British Isles, Journal of Fish Biology 2012, doi:10.1111/j.1095-8649.2011.03210.x ELASMOBRANCHS IN KUWAIT, QATAR AND ABU DHABI 5 –65 –70 min min (cm) Male maturity 62–68 NA NA 61–64 NA NA NA 4) 9) 4) 3) · · 3) · · 4) 9) 2) 5) 8) · 9) 0) 8) 1 · · · · · · · · 8 36 19 4 4 5 4 4 4 5 7 15 ± ) size range ± cm) ± ♀ ± ± ± ± ± ± ± ± ± ± 0 · S.D. cm) and male maturity. 3 0 1 6 3 1 2 4 · 8 0 3 4 · · · · · · · · · · · s.d. ± NA ± 6(70 ♂ · ; mean D 56–77 (68 65–84 (72 70–90 (78 61–81 (73 80–88 (85 (mean 56–80 (68 63–83 (76 58–92 (80 ) and female ( 67–130 (84 56–83 63–140 (86 W 117–119 (118 82–166 (100 ♀ ♀ ♀ ♂ ♂ ♂ ♂ ♂ ♂ ♀ ♀ ♂ ♀ ♀ ,rays Male ( T L 73) 87) 46) 80) 38) 04) 17) · · · · · · · 34 87 68 sites (0 (1 (1 (2 (1 (0 (0 Total all 20) 24) 54) 5 1 · · · — 130 —64 —2 23 Abu Dhabi (1 (0 (5 10) 25) 10) 49) 05) 73) 2 5 · · · · · · 30 35 —— 8 (0 (0 (0 (1 (0 (1 Number of individuals 02) 72) 43) 72) 43) · 5 3 · · · · 12 —2 17 —1 2011 Qatar 105 Kuwait (1 (2 (0 (0 above which all males were mature are presented (15 (% total of all species combined) 99) 32) 09) 57) 07) 33) 33) 5 1 5 · · · · · · · 62 15 20 39 2008 Kuwait (0 (1 (4 (2 (0 (0 (0 A spp. I. Elasmobranch taxa recorded in surveys of markets and harbours during April in Kuwait (2008 and 2011), Qatar (2009) and Abu Dhabi able Triakidae Mustelus mosis Carcharhinidae Carcharhinus Paragaleus randalli T Taxon Sharks Hemiscyllidae Chiloscyllium arabicum (2010): number, percentage of total of all species, size range by sex (sharks and guitarﬁshes For sharks, the range of the smallest maturing size above which all males were mature, excluding anomalous outliers, and for rays, only the size Hemigaleidae Chaenogaleus macrostoma Hemipristis elongata Carcharhinus amblyrhynchoides

© 2012 The Authors Journal of Fish Biology © 2012 The Fisheries Society of the British Isles, Journal of Fish Biology 2012, doi:10.1111/j.1095-8649.2011.03210.x 6 A. B. M. MOORE ET AL. –204 –123 min min (cm) Male maturity NA 61–71 75–83 206–227 NA 164–184 63–80 NA 85–110 NA 6) 1) 2) 8) 5) 8) 2) 1) 0) · · · · 2) 3) 4) · · · 5) · · 1) · · · 6) 1) · 4) 2) · · · · · 47 46 18 45 cm) 44 25 44 8 5 21 17 6 6 14 24 24 10 12 ) size range ± ± ± ± ± ± ± ± ± ± ± ♀ ± ± ± ± ± ± ± s.d. 0 9 6 4 7 8 9 1 8 6 4 · · · · 4 3 5 6 4 · · · 0 · · · · 8 · · · · · · · ± 60 NA 73 NA ∼ ♀ ♀ ♂ 49–83 (62 53–79 (68 72–92 (83 53–84 (69 36–96 (76 59–94 (71 ) and female ( 66–132 (80 52–152 (82 36–100 (75 68–142 (88 50–166 (90 57–227 (119 71–214 (100 75–158 (109 58–210 (113 69–246 (129 82–183 (113 55–223 (119 ♀ ♀ ♂ ♂ ♂ (cm) (mean ♀ ♂ ♀ ♀ ♀ ♂ ♂ ♀ ♀ ♀ ♂ ♂ ♂ ♂ Male( 60) 54) 62) 19) 02) 69) 62) 51) 92) 02) 69) · 1 1 · · · · · · · · · · 29 29 70 sites 118 288 218 1004 (2 (0 (6 (0 (0 (0 (1 (0 (0 (4 (21 Total all 35) B 40) 45) 02) 20) 30) 48) 24) 24) · 2 · · · · · · · · 39 25 22 —43 Abu I. Continued 155 Dhabi (9 (1 (6 (1 (5 (0 (0 (0 (37 able T 00) 34) 91) 15) 05) 12) · 3 1 · · · · · 27 —6 79 —— 32 —5 525 (1 (3 (0 (0 (3 (26 Number of individuals 89) 86) 00) 86) 29) 72) 00) 14) · 7 5 7 1 · · · · · · · 20 13 16 2011 Qatar 139 Kuwait (2 (1 (1 (2 (0 (1 (0 (19 (% total of all species combined) 30) 81) 06) 65) 52) 11) 11) 72) · · · · · · · · 16 ——63 26 ———1 25 23 32 32 ———1 2008 179 338 Kuwait (1 (1 (1 (2 (2 (1 (22 (11 Taxon Carcharhinus melanopterus Carcharhinus brevipinna Carcharhinus limbatus Carcharhinus macloti Carcharhinus amboinensis Carcharhinus falciformis Loxodon macrorhinus Carcharhinus dussumieri Carcharhinus leucas Carcharhinus sorrah Carcharhinus leiodon

© 2012 The Authors Journal of Fish Biology © 2012 The Fisheries Society of the British Isles, Journal of Fish Biology 2012, doi:10.1111/j.1095-8649.2011.03210.x ELASMOBRANCHS IN KUWAIT, QATAR AND ABU DHABI 7 (cm) Male maturity 45–53 NA 54–68 NA NA NA NA NA 7) 6) 2) 3) 7) · · 4) · · · 1) · 0) 5) 0) 4) 7) · · · · · · 31 25 42 45 17 7 4 9 5 8 32 10 cm) ± ± ± ± ± ± ± ± ± ± ± ) size range ± 0 2 ♀ 5 8 7 1 8 8 · · 4 7 2 · · s.d. · · · · 1 · · · · 87 NA NA ± 180 ♀ ♀ ♂ ♂ 47–88 (65 45–64 (57 67–94 (81 45–85 (66 76–94 (81 43–89 (64 47–120 (74 73–149 (91 72–137 (102 81–177 (138 72–214 (144 39–175 (107 ♀ ♀ ♂ ♂ ♂ ) and female ( ♀ ♀ ♂ ♀ ♀ ♂ ♂ ♂ (cm) (mean Male( 80) 02) 49) 41) 02) 86) 28) 08) · 1 1 · · · · · · · 13 sites 1246 (0 (0 (0 (0 (4 (0 (3 (26 Total all 99) 24) 24) 13) · · · · —23 —19 Abu 112 I. Continued Dhabi (0 (0 (3 (26 able T 11) 15) 10) · 2 · · — — 226 — — 143 931 (0 (0 (46 Number of individuals 60) 73) 43) 58) · · · · 54 —3 10 18 2011 Qatar 130 Kuwait (7 (1 (2 (18 (% total of all species combined) 35) 20) 32) 46) 86) · · 7 · · · ———1 20 ———1 ———13 13 2008 172 185 Kuwait (1 (0 (0 (11 (12 C djiddensis cf. Sphyrnidae Sphyrna lewini Rhizoprionodon oligolinx Rhynchobatidae Rhynchobatus Sphyrna mokarran Taxon Rhizoprionodon acutus Guitarﬁsh Rhinidae Rhina ancylostoma Rhinobatos halavi Rhinobatidae Rhinobatos granulatus

© 2012 The Authors Journal of Fish Biology © 2012 The Fisheries Society of the British Isles, Journal of Fish Biology 2012, doi:10.1111/j.1095-8649.2011.03210.x 8 A. B. M. MOORE ET AL. (cm) Male maturity 43 54 48 53 NA 18 84 119 NA 5) · 0) 3) 0) · 1) 9) 2) 2) 5) · 8) 9) 9) 7) · · 0) 0) · · · · · · · · 15 · · cm) 2 7 7 9 13 4 4 32 11 20 10 11 19 14 ± ) size range ± ± ± ± ± ♀ ± ± ± ± ± 0 ± ± ± ± s.d. · 3 9 7 1 8 0 9 7 2 · · · · · 4 6 3 3 3 · · · · · · · · · ± NA NA 124 ♀ ♂ ♂ 15–23 (19 24–54 (41 33–69 (54 27–58 (42 77–87 (82 14–26 (19 35–96 (50 25–62 (40 32–89 (56 37–94 (61 33–74 (54 ) and female ( 40–121(88 45–106 (87 61–125 (90 ♀ ♀ 105–155 (124 ♂ ♂ ♂ ♂ ♂ ♀ ♀ ♀ ♀ (cm) (mean ♀ ♂ ♀ ♂ ♂ Male( 54) 65) 19) 22) 34) 09) 77) 02) 81) 1 · · · · · · · · · 25 sites (0 (0 (2 (0 (0 (0 (0 (0 (3 Total all 24) 24) 1 · · —30 — 102 —10 —16 —4 — 177 Abu Dhabi (0 (0 I. Continued 05) 30) 20) 15) 10) 15) 84) 1 6 4 2 3 · · · · · · · —— 36 118 able (0 (0 (0 (0 (0 (0 (5 T Number of individuals 29) 29) 15) 72) 01) 57) 14) 9 · · · · · · · 23 15 26 —3 42 11 2011 Qatar Kuwait (3 (1 (2 (3 (6 (1 (0 (% total of all species combined) 86) 59) 75) 92) 46) 12) 20) 9 7 3 · · · · · · · 13 ———1 72 —1 2008 Kuwait (0 (0 (4 (0 (0 (1 (0 species complex 14 punctifer ocellatus poecilura cf. sp. B 17 cf. cf. Himantura uarnak Gymnuridae Gymnura Myliobatidae Aetobatus ﬂagellum Aetobatus Rays Dasyatidae Himantura fai Himantura Taxon Rhinobatos Pastinachus sephen Himantura imbricata

© 2012 The Authors Journal of Fish Biology © 2012 The Fisheries Society of the British Isles, Journal of Fish Biology 2012, doi:10.1111/j.1095-8649.2011.03210.x ELASMOBRANCHS IN KUWAIT, QATAR AND ABU DHABI 9 (cm) Male maturity 69 NA 40 71 105 NA 9) 5) 1) 0) 8) 6) · · 1) 8) · · · · · · cm) 6 7 25 17 14 11 11 11 ) size range 3) · ± ± ♀ ± ± ± ± ± ± s.d. 6 5 16 0 2 7 6 · · 1 1 · · · · · · ± 100 ± NA 105 ∼ 5 99–122 ♂ · ♂ ♀ ♀ (110 35–72 (45 58–60 (63 48–90 (68 45–85 (69 24–72 (51 43–96 (77 ) and female ( 47–123 (76 43–116 (80 ♂ ♂ ♂ ♀ ♀ (cm) (mean ♂ ♂ ♀ ♀ Male( not accurately identiﬁed. 60) 28) 02) 54) 04) 04) · · · · · · sites 214 4649 (100) (4 (0 (2 (0 (0 (0 Total all C. brevipinna – 24) 1 · —13 —94 —25 —2 Abu 415 (100) Dhabi (0 I. Continued C.limbatus able T and 10) 42) 51) 45) 10) 2 · · · · · 69 91 —— 2 2019 (100) (0 (3 (4 (0 (0 ) C. limbatus Number of individuals – 14) 14) 86 29) 1 1 6 · · · · —9 2011 Qatar 699 (100) Kuwait (0 (0 (0 (0 (% total of all species combined) C. leiodon recorded. – T L 58) 98) 06) 33) 5 · · · · 24 —2 16 —— 2 2008 (100) Kuwait (1 (7 (1 (0 , minimum size not available. . 140–200 cm c min C. amblyrhynchoides milvus cf. spp. 121 eregoodootenkee cf. Probably comprising Excised embryo. Unsexed specimens of Aetomylaeus nichoﬁi Rhinoptera Rhinopteridae Rhinoptera javanica Mobulidae Mobula All species combined 1516 Taxon Aetomylaeus NA, not applicable;A NA B C Rhinoptera jayakari

© 2012 The Authors Journal of Fish Biology © 2012 The Fisheries Society of the British Isles, Journal of Fish Biology 2012, doi:10.1111/j.1095-8649.2011.03210.x 10 A. B. M. MOORE ET AL. exceptions: (1) two subtly different species of cownose rays Rhinoptera sp., for which field identification characters (Last et al., 2010b) only became available at the end of the survey, and (2) a number of morphologically similar Carcharhinus species in the initial part of the first survey (Kuwait in 2008). Undescribed taxa [whipray Himantura sp. B sensu Manjaji, 2004; guitarfish Rhinobatos cf. punctifer (‘RHY’ sensu Henderson et al., 2007)] were also recorded, as was a cryptic species complex [Himantura uarnak (Gmelin 1789)]. Preliminary examination of barcode data, photographs and specimens indicates that taxonomic clarification is also required for several more batoid species collected in this survey (White et al., 2010; R. D. Ward, W. White, P. Last, pers. comms.).

TAXONOMIC COMPOSITION A total of 39 elasmobranch species (including the H. uarnak species complex) were recorded during the survey, comprising 21 shark, five guitarfish and 13 ray species (Table I). These belonged to a total of 13 families, of which the most species-rich were whaler sharks (Carcharhinidae, 14 species) and stingrays (Dasy- atidae, five species). The vast majority (c. 80%) of elasmobranchs were sharks, with rays comprising c. 16%; guitarfishes were relatively unimportant overall (c. 4%). Amongst the sharks, carcharhinids dominated (c. 73% of total individuals), with weasel sharks (Hemigaleidae) and carpetsharks (Hemiscyllidae) comprising c.3% each. Houndsharks (Triakidae) and hammerhead sharks (Sphyrnidae) each comprised <1% of recorded sharks. Amongst the rays, stingrays (Dasyatidae) and cownose rays (Rhinopteridae) were the most important (c. 7 and 5% of total individuals) with eagle rays (Myliobatidae) contributing c. 4%; butterfly rays (Gymnuridae) and devil rays (Mobulidae) were unimportant (<1% total). At a species level, two species of small (i.e. maximum recorded LT < 100 cm) carcharhinid sharks C. dussumieri and R. acutus comprised just under half (c. 48%) of all elasmobranch individuals, and when combined with three other abundant carcharhinids [sliteye shark Loxodon macrorhinus Muller¨ & Henle, 1839; grey sharp- nose shark Rhizoprionodon oligolinx Springer 1964; spot-tail shark Carcharhinus sorrah (Muller¨ & Henle 1839)] this figure rose to nearly two thirds (c. 64%). With the exception of the similar Rhinoptera species, the most frequently recorded batoids identified to species level were the undescribed whipray Himantura sp. B and Rhi- nobatos granulatus Cuvier 1829. There were some notable differences in the broad taxonomic composition of landings between sampling events (Fig. 2). In Kuwait, carpetsharks and guitarfishes comprised a far greater component of recorded individuals in 2011 (c. 20 and 15%) than they had in 2008 (c. 1% each). Rays were rarely recorded at Abu Dhabi, and carpetsharks were not common in Qatar and absent in Abu Dhabi. The largest proportion of individuals of larger shark species (i.e. maximum LT > 100 cm) was recorded in Kuwait in 2008 and in Abu Dhabi. Photographs from the brief visits to Qatar in 2010 and 2011 indicated that the species composition was broadly similar to that recorded in the full survey in 2009, although a single individual of an additional species was also recorded, i.e. the blacktip reef shark Carcharhinus melanopterus (Quoy & Gaimard 1824). In Kuwait in 2008, no additional species were found after around two thirds (i.e. c. 1000) of all individuals had been examined. Similarly, in Qatar, only one

(a) (b)

Fig. 2. Broad taxonomic composition of elasmobranchs recorded at each sampling event: (a) Kuwait 2008, (b) Qatar 2009, (c) Abu Dhabi 2010 and (d) Kuwait 2011. , Chiloscyllium arabicum; , Triakids & Hemigaleids; , small (<100 cm maximum total length, LT) carcharhinids; , larger (>100 cm maximum LT) carcharhinids and sphyrnids; , guitarﬁshes; ,rays. further species was recorded beyond approximately three quarters (c. 1500) of the total individuals recorded, suggesting that these surveys adequately recorded species richness of landings at the time of the survey. Conversely, new taxa were recorded throughout the much smaller survey in Abu Dhabi, indicating that species richness was insufﬁciently sampled at this location.

SIZE, MATURITY AND SEX COMPOSITION Table I presents details of species abundance, size ranges for males and females and male maturity for the individuals sampled in the 2008–2011 surveys. The vast majority (c. 90%) of all sharks recorded were small with an LT between 50 and 90 cm, and this pattern was broadly consistent across the four sampling events (Kuwait 2008 c. 85%; Qatar c. 94%; Abu Dhabi c. 87%; Kuwait 2011 c. 87%) (Fig. 2). The sample comprised mostly of species with a small reported maximum size of <100 cm LT, i.e. C. dussumieri, L. macrorhinus, R. acutus and R. oligolinx. Medium-sized sharks of 91–150 and 151–200 cm LT comprised c. 7 and 1%, respectively, of total shark individuals recorded. Large sharks of >200 cm LT [comprising pigeye Carcharhinus amboinensis (Muller¨ & Henle 1839), spinner Carcharhinus

(a) Small Common small Larger sharks non-carcharhinids carcharhinids >100 cm max LT <100 cm max LT 100

. (36) spp

M. mosis (19) C. leucas (20) P. randalli (39)R. acutus (901) C. macloti (15) C. leiodonC. (14) sorrah S.(150) mokarran (6) C. arabicum (64) R. oligolinx (92) C. limbatus (52) C. brevipinna (14) C. macrostoma (36) C. dussumieri (732) L. macrorhinus (151) C. amboinensis (26) Carcharhinus C. amblyrhynchoides (3)

Mature males (%) (b) Benthic Bentho-pelagic 100

(83) tus (7) B (110) spp. sp. ocella . milvus (15) H. P. sephen (36) poecilura (19) A. nichofii cf(47) A. flagellumcf. (22) cf. A. A. G. Rhinoptera H. uarnak complex (21)

Fig. 3. Percentage of male (a) sharks and (b) rays (see Table I) that were assessed as mature ( )orimmature ( ). The number of males assessed for each species are presented in parentheses. LT, total length. brevipinna (Muller¨ & Henle 1839), blacktip shark Carcharhinus limbatus (Muller¨ & Henle 1839) and great hammerhead Sphyrna mokarran (Ruppell¨ 1837)] were relatively unimportant in terms of overall abundance (<1%); sharks of this size were most commonly recorded in Abu Dhabi. For male sharks, a high percentage (c. 70–80%) of the common small carcharhinids (i.e. C. dussumieri, L. macrorhinus, R. acutus and R. oligolinx)were mature, and for the four species of small non-carcharhinids, namely, Arabian car- pet shark Chiloscyllium arabicum Goubanov 1979, Arabian smoothhound Mustelus mosis Hemprich & Ehrenberg 1899, hooktooth shark Chaenogaleus macrostoma (Bleeker 1852) and slender weasel shark Paragaleus randalli Compagno, Krupp & Carpenter 1996, the percentage mature was even greater (Fig. 3). In contrast, for the larger C. sorrah, only c. 11% of males examined were mature. Similarly, most males of a number of other carcharhinid and sphyrnid shark species with a

Table II. Sex ratios of elasmobranchs recorded in surveys of markets and harbours at locations in The Gulf deviating signiﬁcantly from parity in favour of one sex

Species Male Female Mustelus mosis Kuwait 2011*** Chaenogaleus macrostoma Kuwait 2011* Qatar** Carcharhinus dussumieri Kuwait 2008***, Qatar*** Loxodon macrorhinus Abu Dhabi*** Rhizoprionodon acutus Kuwait 2008***, Qatar*** Rhizoprionodon oligolinx Kuwait 2011*** Himantura sp. B Qatar**, Kuwait 2011* Pastinachus sephen Kuwait 2008** Gymnura cf. poecilura Kuwait 2011* Aetobatus ﬂagellum Kuwait 2011* Aetomylaeus nichoﬁi Kuwait 2008** Qatar* Rhinoptera spp. Qatar*** Kuwait 2008***, Kuwait 2011*

*P<0·05; **P<0·01; ***P<0·001.

maximum reported size >150 cm LT [e.g. graceful shark Carcharhinus amblyrhynchoides (Whitley 1934), C. amboinensis, C. brevipinna, smoothtooth blacktip shark Carcharhinus leiodon Garrick 1985, bull shark Carcharhinus leucas (Muller¨ & Henle 1839), C. limbatus and S. mokarran] were immature (Fig. 3). For the rays, the majority of males of benthic species (dasyatids and Gymnura cf. poecilura) were mature; some bentho-pelagic species [e.g. Aetomylaeus nichofii (Bloch & Schneider 1801)] were mostly mature, although around half of the rhinopterids and c. 75% of Aetobatus flagellum (Bloch & Schneider 1801) recorded were immature (Fig. 3). For the majority of species, sex ratios did not differ significantly from parity (χ 2 test, d.f. = 1, P>0·05) or did so only at one location (Table II). For the two most common elasmobranchs, C. dussumieri and R. acutus, samples in both Kuwait in 2008 and Qatar had a highly significant departure from parity towards males (χ 2 test, d.f. = 1, P<0·001), although there was no significant departure from parity for either species in Kuwait in 2011 (χ 2 test, d.f. = 1, P>0·05). Rhinoptera spp. was notable in that it was the only taxon with a highly significant bias towards a different sex at two separate locations, i.e. females in Kuwait in 2008 and males in Qatar (χ 2 test, d.f. = 1, P<0·001).

SIZE DIFFERENCES In most cases, there were no signiﬁcant differences between the average size of males and females landed for commonly recorded species, with the exception of C. sorrah, R. oligolinx and R. granulatus (Mann–Whitney U-test, P<0·001 for each species), with females larger in all three of these species. Size-frequency distributions for C. sorrah, R. oligolinx and R. granulatus are presented in Fig. 4. Signiﬁcant differences in size distribution of all three species were observed with most of the larger size classes comprising females: C. sorrah (χ 2 test, d.f. = 5, P<0·01), R. oligolinx (χ 2 test, d.f. = 5, P<0·001), R. granulatus (χ 2 test, d.f. = 4, P<0·001).

100 (a)

41–50 51–60 61–70 71–80 81–90 91–100 101–110111–120 121–130131–140141–150151–160 161–170

80 (b) 70

50 ency

u 40

Freq 30

0 60 6– 31–35 36–40 41–45 46–50 51–55 5 61–65 66–70 71–75 76–80 81–85 86–90

25 (c)

0–1011–2021–3031–4041–5051–6061–7071–8081–90 91–100101–110111–120121–130131–140141–150151–160161–170171–180181–190191–200

LT (cm)

Fig. 4. Total length (LT)-frequency distributions for male ( ) and female ( ) elasmobranchs for (a) Carcharhinus sorrah, (b) Rhizoprionodon oligolinx and (c) Rhinobatus granulatus.

The landed size of both sexes of the commonest shark species varied between sampling events. Males of C. dussumieri landed in Qatar were signiﬁcantly larger compared to those in Kuwait in both 2008 and 2011 (Mann-Whitney U-test, P<0·001 and P<0·05, respectively); C. dussumieri males at Kuwait in 2011 were larger than

100 100 (a) (b) 90 90 80 80 70 70 60 60 50 50 40 40 30 30 20 20 10 10 0 0 30 35 40 45 50 55 60 65 70 75 80 85 90 95 50 55 60 65 70 75 80

100 100 (c) (d)

Mature males (%) 90 90 80 80 70 70 60 60 50 50 40 40 30 30 20 20 10 10 0 0 50 55 60 65 70 75 80 40 45 50 55 60 65 70

LT (cm)

Fig. 5. Male maturity ogives for (a) Carcharhinus dussumieri,(b)Loxodon macrorhinus,(c)Rhizoprionodon acutus and (d) Rhizoprionodon oligolinx. The sample size (n), total length (LT) at 50% maturity (LT50) −K(L −L ) −1 and coefﬁcients for the logistic model Y = x + (z − x)(1 + e T T50 ) used to determine LT50 are 2 (a) n = 730, LT50 = 72·1cm,K = 0·619, x = 0·5, z = 99·6(r = 0·991); (b) n = 147, LT50 = 64·0cm, 2 K = 0·441, x =−3·2, z = 100·2(r = 0·947); (c) n = 811, LT50 = 61·7cm,K = 0·714, x = 0·1, z = 2 2 99·1(r = 0·993); (d) n = 92, LT50 = 53·0, K = 18·45, x =−4·7, z = 97·0(r = 0·990). those in the same location in 2008 (Mann–Whitney U-test, P<0·05). Qatar C. dussumieri females were larger than those from Kuwait in 2011 (Mann–Whitney U-test, P<0·05). Both males and females of R. acutus at Abu Dhabi were signiﬁcantly larger than that in Kuwait in 2008 (Mann–Whitney U-test, both P<0·001), Qatar (Mann–Whitney U-test, both P<0·001) and Kuwait in 2011 (Mann–Whitney U- test, males P<0·05; females P = 0·001).

REPRODUCTIVE BIOLOGY

Male LT50 occurred at 72·1cmin C. dussumieri,64·0cmin L. macrorhinus, 61·7cminR. acutus and 53·0cminR. oligolinx (Fig. 5). It was not possible to determine an LT50 for C. sorrah owing to the relatively small number of mature individuals recorded. Sizes of maturity classes for C. sorrah were up to 92 cm LT (n = 127) for juveniles, 85–110 cm LT(n = 6) for maturing and ≥108 cm LT for mature (n = 17). Eight pregnant female C. dussumieri (79·0–100·7cmLT; mean ± s.d. 89·3 ± 7·0 cm) were dissected and each contained two to five fully formed embryos of 32·0–38·7cmLT; (mean ± s.d. 35·4 ± 16·0 cm). The overall sex ratio of embryos in the seven litters where this was recorded was not significantly different from parity (χ 2 test, d.f. = 1, P>0·05). There was a significant positive correlation

© 2012 The Authors Journal of Fish Biology © 2012 The Fisheries Society of the British Isles, Journal of Fish Biology 2012, doi:10.1111/j.1095-8649.2011.03210.x 16 A. B. M. MOORE ET AL. between maternal LT and litter size (Pearson r = 0·785, n = 8, P<0·05) but not between maternal LT and mean embryo LT (Pearson r = 0·332, n = 8, P>0·05). The LT of the embryos and that of the smallest animals recorded in landings indicate that birth size locally is c. 36–38 cm LT. A female R. oligolinx of 67·4cmLT contained three embryos (males of 23·6 and 28·2 and a female of 26·2cmLT). An 83·5cm LT M. mosis from Abu Dhabi contained 11 fully formed embryos (six males 25·5–28·4cmLT; five females 26·5–26·7cmLT). In addition to five embryos, the right uterus also contained a yolk-coloured oval ovum of solid waxy material c. 5 cm long, which is unusual (A. Henderson, pers. comm.). Other notable opportunistic observations from females of elasmobranch species whose biology is poorly known were an aborted recently formed candle (i.e. eggs within a common shell) from a 180 cm LT bowmouth guitarfish Rhina ancylostoma Bloch & Schneider 1801 (Abu Dhabi); mature oocytes of ≤1·4 cm diameter in a 23·2cmWD scaly whipray Himantura imbricata (Bloch & Schneider 1801) in Qatar; several female cowtail stingray Pastinachus sephen (Forsskal˚ 1775) of ≥61 cm WD with emergent fully formed embryos (Kuwait 2008); several females of Rhinoptera sp. (probably Rhinoptera jayakari Boulenger 1895) of ≥80 cm WD with emergent fully formed embryos and aborted embryos of 22·5–28·5cmWD (Kuwait 2008).

FISHERIES, BY-CATCH, DISCARDING AND UTILIZATION The majority of elasmobranchs recorded in this study were landed by small (c. 7–10 m) open speedboats operating gillnets to target teleosts in local, coastal waters. In addition to small gillnetters, larger (c. 15–20 m) dhows also operated, tar- geting teleosts with either hemispherical wire fish traps (gargoor) or gillnets, but these vessels appeared to contribute less to the overall elasmobranch landings recorded. In Abu Dhabi, these dhows (reportedly operating in Gulf waters) also landed large elasmobranchs from hook-and-line fishing as a targeted but apparently supplemen- tary activity. While all quayside landings recorded at Abu Dhabi were caught in The Gulf, the retail market sold both locally caught elasmobranchs and those imported overland originating from the Gulf of Oman. A small number of small sharks at each survey location had apparently been caught by handline, presumably opportunisti- cally during gillnetting. In addition, recent footage from Bahrain demonstrated that large gargoor (c. 250 cm height) can occasionally capture quite large (c. 150 cm LT) rhynchobatids (A. B. M. Moore & R. Peirce, pers. obs.). All elasmobranchs recorded were landed and marketed whole, with no direct evidence of removal of fins at sea. Fins were observed being removed from sharks and guitarfishes in Kuwait and Qatar both by fishers at the quayside and by stall- holders upon sale for consumption, apparently for onward sale. Large sharks and guitarfishes landed whole in Abu Dhabi were transported overland to other Emirates for processing, presumably for the fin market (A. B. M. Moore pers. obs.; R. Jabado pers. comm.). While prices were not recorded, sharks were marketed at relatively low prices compared to teleosts. Rays appeared to be of particularly low value and catches in Kuwait were commonly observed being discarded for disposal (either back at sea, in the harbour or in refuse), although rays picked from the gillnets of incoming vessels at Doha Corniche, Qatar, were always marketed. Rhynchobatid guitarfishes were the only commonly encountered batoid taxa that were apparently of some value, both as meat and apparently for fins. Weather conditions appeared

© 2012 The Authors Journal of Fish Biology © 2012 The Fisheries Society of the British Isles, Journal of Fish Biology 2012, doi:10.1111/j.1095-8649.2011.03210.x ELASMOBRANCHS IN KUWAIT, QATAR AND ABU DHABI 17 to have a notable effect on elasmobranch discarding practices in Kuwait, with the unsettled weather in April 2011 resulting in nets being emptied at the quayside rather than at sea. This factor is likely to explain the high number of low-value C. arabicum and R. granulatus recorded in 2011.

DISCUSSION

OVERVIEW The current study is the first detailed, large-scale survey of the diversity, biology and fisheries of Gulf elasmobranchs and provides a foundation for more refined characterization. This is despite its limitations in terms of seasonal coverage and relatively small sample size compared with other recent works sampling elasmobranch landings at (sub-) tropical locations (White & Dharmadi, 2007; Bizarro et al., 2009). Detailed assessment of reproductive status was not recorded in this study. The find- ings confirm that the elasmobranch landings in the parts of The Gulf covered by this survey are dominated by a few species of common, small carcharhinids which are caught largely as by-catch, and the species and size composition of these landings are notably different from those reported in adjacent Oman, which also has targeted fisheries for large pelagic species (Henderson et al., 2007, 2009). These data also confirm regional differences in the reproductive biology of common fisheries species, as well as sex-based and sampling event-based differences in the landed size of some common species, which may be due to fisheries or biological factors. Together, these highlight the need for local characterizations of elasmobranch fisheries in the western Indian Ocean. This study further confirms that significant numbers of multiple species of elasmobranchs are landed in Kuwait and Qatar, although the FAO does not list any landings of elasmobranchs from these countries. Furthermore, Kuwait, Qatar and the U.A.E. routinely catch and land elasmobranchs and should therefore strive to develop a shark plan, although it should be noted that all other Gulf states (Bahrain, Iran, Iraq and Saudi Arabia) have some documentary evidence of elasmobranchs occurring in fisheries, particularly as by-catch (Moore, 2011). Given the multiple nations that surround The Gulf, a shark plan may be best achieved with a regional approach, as was done for the Mediterranean Sea (UNEP, 2003).

TAXONOMY AND SPECIES RECORDS The current study has provided valuable information on the diversity of elasmobranchs in the north-western Indian Ocean, an area which is in general poorly sampled despite indications that its elasmobranch fauna has significant biogeographic and taxonomic interest (Moore, 2011). While 39 taxa were recorded, many of these occurred infrequently, and the commercial harvest was dominated by a small number of small-sized sharks. The surveys provided a number of new records, the most notable of which was the rediscovery of C. leiodon in Kuwait, previously known only from a single specimen collected over 100 years ago from 3000 km away in Yemen (Moore et al., 2011). The surveys also provided significant range extensions for a number of shark (Moore et al., 2010) and batoid species, including the first

© 2012 The Authors Journal of Fish Biology © 2012 The Fisheries Society of the British Isles, Journal of Fish Biology 2012, doi:10.1111/j.1095-8649.2011.03210.x 18 A. B. M. MOORE ET AL. substantiated record of a devil ray (Mobulidae) from The Gulf (unpubl. data). In addition, the surveys provided material and data on several taxa in need of descrip- tion or taxonomic resolution that will contribute to an improved understanding of Indo-Paciﬁc Ocean elasmobranch diversity.

PATTERNS OF DIVERSITY AND DISTRIBUTION Local patterns of diversity from this study are difficult to compare quantitatively when based on samples of differing sizes from landings of different fleets. Based on a qualitative comparison of the data (and excluding those species recorded on only a handful of occasions), Kuwait was notable in that a number of species (C. leiodon, R. oligolinx, R. granulatus and A. flagellum) were only recorded there, which may be due to the proximity of the Shatt al Arab. These data and those from other studies indicate geographical differences in the abundance of common small carcharhinid species such as the prevalence of C. dussumieri along the coasts of Kuwait, Qatar (this study) and Iran (Blegvad, 1944 as Carcharias menisorrah), but relative rarity off the Omani coast (Henderson et al., 2007; A. Henderson, pers. comm.). Loxodon macrorhinus was absent from Kuwait in both 2008 and 2011 but relatively abundant in Qatar, Abu Dhabi (this study) and in Oman’s landings (Henderson et al., 2007). This may be related to this species apparently preferring low turbidity environments (Gutteridge et al., 2011). Rhizoprionodon oligolinx was only recorded (but relatively abundant) in Kuwait, where the morphologically similar L. macrorhinus was absent. Excluding two species recorded as single individuals from Abu Dhabi that had probably originated from the Gulf of Oman [silky shark Carcharhinus falciformis (Muller¨ & Henle 1839) and scalloped hammerhead Sphyrna lewini (Griffith & Smith 1834)] and the H. uarnak species complex, the number of elasmobranch species recorded in the current study from The Gulf was 36. Again, excluding H. uarnak, this is notably less than the 56 reported from Oman (Henderson & Reeve, 2011) and largely reflects the lack of species associated with deeper waters in the shallow Gulf. Notable temporal differences were observed in the abundance of two species of carcharhinid (R. acutus and C. sorrah) that were common in Kuwait in 2008 but were rare or absent at this location in 2011. This absence could be due to a large number of variables, possibly including windy conditions at sea in 2011 reducing gillnet catches of these species, or temporal variation in estuarine discharges affecting distribution. Surface water temperature was probably not a factor, being similar at ◦ ◦ the time of both surveys (22·2 C in 2008 and 21·4 C in 2011, measured at the same station off east Failaka Island; F. Al-Yamani, unpubl. data).

SHARK BIOLOGY There was a highly signiﬁcant bias towards (mostly mature) males for both C. dussumieri and R. acutus, in both Kuwait in 2008 and Qatar. This may be related to spatial segregation from males by birthing or near-term pregnant females, as both species are reported as having peaks in parturition in spring or summer in the region (Assadi, 2001; Henderson et al., 2006). Interpretation of elasmobranch sex ratio data from landings is, however, problematic, as any signiﬁcant differences may be due to a number of confounding factors (e.g. gear bias) as well as natural segregation, which is commonly reported in elasmobranchs (reviewed in Sims, 2005).

Carcharhinus dussumieri in this study attained the maximum reported LT of 100 cm (Compagno et al., 2005), consistent with previous work locally off Iran (Blegvad, 1944, as C. menisorrah) and larger than the maximum of 93·7cmLT recorded off Indonesia (White, 2007). Male maturity size range of C. dussumieri in the current study was 63–80 cm LT (all mature animals ≥66 cm LT and an LT50 of 72·1 cm) and broadly consistent with male size at first maturity (67 cm LT) and LT50 (69 cm) recorded off Iran’s Gulf of Oman coast (Assadi, 2001) but slightly smaller than that of c.74cmLT reported from Indonesia (White, 2007). The size at male maturity recorded for C. sorrah in this study (i.e. all mature by c. 110 cm LT) is broadly consistent with that for Indonesia and most other locations [recorded and reviewed by White, 2007)]. One female C. sorrah from Qatar of 166 cm LT extends the reported maximum size for this species (160 cm LT; Compagno et al., 2005; White, 2007, Henderson et al., 2009). Landings of this species were conspicuous in their dominance by juveniles of the 70–85 cm size class (c. 77% of all C. sorrah recorded), indicating that this group is particularly vulnerable to capture locally in spring. Given a reported birth size of 45–60 cm (Compagno et al., 2005) and rapid growth of neonates of c. 20 cm in the first year off northern Australia (Davenport & Stevens, 1988), it is probable that this group represents individuals in their first year or so of life. In Chiloscyllium arabicum maximum LT has been reported as 70 cm (Compagno et al., 2005), yet, in this study, males and females were often larger than this (≤77 and ≤80 cm LT, respectively) which accords with 78 cm LT reported in an earlier study from The Gulf (Goubanov & Shleib, 1980). Maturity in this species was reported to occur between 44·6 and 54·1cmLT (Dingerkus & DeFino, 1983 as C. confusum, sex not specified), yet in this study all stages were notably larger than this (juvenile 56 and 62 cm LT, n = 2; maturing 62 and 68 cm LT, n = 2; mature 60–77 cm LT, n = 60). In this study, C. arabicum was notable in that it was the only species whose size frequency distribution (pooled samples for both males and females) was normal, indicating that a wide range of life stages are vulnerable to capture locally in April. Loxodon macrorhinus size ranges from the current study are similar to those recorded from Oman (Henderson et al., 2009), although the maximum reported size from both of these studies is smaller than that of 99 cm LT recorded in Indonesia (White, 2007). Further regional differences in the biology of this species are the size at male maturity, which in this study (61–71 cm LT;64·0 LT50) is notably smaller than that recorded from Indonesia (80–83 cm LT,81·9cmLT50; White, 2007) and southern Africa (73–75 cm LT; Bass et al., 1975). The highly significant bias towards (large, mature) males in the April sample at Abu Dhabi is consistent with notable sex and size segregation reported for this species from longline surveys in the Maldives (Anderson & Ahmed, 1993). The average size of R. acutus at Abu Dhabi (probably originating from the Gulf of Oman) was significantly greater than at other locations, and the mean size for both males and females of R. acutus from Oman (Henderson et al., 2009) was also greater than that found in this study. While this may simply represent gear bias, it may also indicate that populations of this species from The Gulf and the Gulf of Oman have different size characteristics. The LT50 for males of R. acutus from the current study (61·7cmLT) was also smaller than that from Oman (64·7cmLT; Henderson et al., 2006), Indonesia (71·8cmLT) and other locations in the Indo-West Pacific (White, 2007). Maximum size of R. acutus in this study (89 cm LT) is at

© 2012 The Authors Journal of Fish Biology © 2012 The Fisheries Society of the British Isles, Journal of Fish Biology 2012, doi:10.1111/j.1095-8649.2011.03210.x 20 A. B. M. MOORE ET AL. least c. 5 cm smaller than that recorded in several other Indo-West Pacific Ocean locations (Henderson et al., 2009). Rhizoprionodon oligolinx has few published studies on its biology. Males from this study were found to mature at a notably larger size (45–53 LT, with LT50 at 53 cm) than previously reported (i.e. in Indonesia, 43–45 cm LT, with LT50 at 44·6 cm; White, 2007; 29–38 cm LT, Compagno et al., 2005). Furthermore, females from this study attained a greater maximum size (85 cm LT) than previously reported (70 cm LT; Compagno et al., 2005). The near-term embryo 28·2cmLT recorded is of a similar size to the smallest mature individuals reported elsewhere (Compagno et al., 2005). The average size of females of this species was significantly larger than males, and in Kuwait in 2011, females (at least some of which were pregnant) dominated recorded landings. All shark landings were dominated by individuals of 50–90 cm LT, with relatively few recorded above or below this size. The elasmobranch most commonly recorded (R. acutus) is known to have localized abundance of free-swimming neonates of <40 cm LT in April, at least off Qatar (R. Peirce, pers. obs.), but these and other very small sharks did not occur in landings. Reasons for this are probably due to gillnet selectivity but might also include discarding at sea or absence in fished areas. The relative lack of larger sharks in landings may be explained by a number of factors including them not being targeted and gear bias (e.g. longlining not widely used), fisheries bias (e.g. areas of abundance not being fished, transhipment at sea) or low abundance (e.g. seasonality and localized depletion). For a large proportion of the shark individuals recorded, the current International Union for the Conservation of Nature (IUCN) Red List (IUCN, 2011) status is least concern (R. acutus, R. oligolinx and L. macrorhinus), given the relatively favourable life-history characters of these small carcharhinids compared to many other shark species. The commonly recorded C. dussumieri and C. sorrah have been assessed, however, as near threatened (IUCN, 2011). Larger shark species recorded in this study have been classed as near threatened, vulnerable or endangered (IUCN, 2011), and it was notable that individuals of these species were mostly either juvenile males or females of a similar size markedly below the smallest maturity size reported in Compagno et al. (2005). The Kuwait fishery also caught juveniles and pregnant females of C. leiodon, which has a highly restricted known distribution (Moore et al., 2011; A. B. M. Moore, unpubl. data).

BATOID BIOLOGY AND FISHERIES Nearly all of the batoid species recorded in this study are either classed in the IUCN Red List as vulnerable, endangered, data deficient, are undescribed, or require taxonomic resolution and are therefore not evaluated (IUCN, 2011). There is a paucity of detailed, recent studies on the biology and fisheries of inshore (sub-) tropical Indo-West Pacific Ocean batoids outside Australia, with a few exceptions (Raje, 2003; White & Dharmadi, 2007; Raje & Zacharia, 2009). Declining catches of some batoid species from the Arabian Sea have been reported recently, despite increased effort (Raje & Zacharia, 2009). This study provides some of the first biology and fisheries data for batoids from the sub-tropical western Indian Ocean and highlights significant by-catch (at least in Kuwait and Qatar) of a number of poorly known and vulnerable species. Rays

© 2012 The Authors Journal of Fish Biology © 2012 The Fisheries Society of the British Isles, Journal of Fish Biology 2012, doi:10.1111/j.1095-8649.2011.03210.x ELASMOBRANCHS IN KUWAIT, QATAR AND ABU DHABI 21 were often discarded as unmarketable and took considerable effort to remove from gillnets by fishers (A. B. M. Moore, pers. obs.), suggesting that any measures developed to reduce this by-catch would be favourably received. Excluding guitarfishes, the rarity of rays encountered at Abu Dhabi is consistent with year-round fisheries statistics for this port (Environment Agency Abu Dhabi, 2010) and probably reflects bias from fisheries or discarding practices. Species composition of batoids in Iranian waters of the easternmost Gulf was reported by Vossoughi & Vosoughi (1999), who, notwithstanding probable nomenclatural errors, found a broadly similar suite of taxa to that reported in this study. Although from separate years and potentially confounded by species identification, the highly significant sex biases recorded for Rhinoptera spp. towards females (in Kuwait in 2008) and males (Qatar) are of interest and may reflect real geographical differences. Indicative data from this study suggests male and female maturity at c. 70 and 80 cm WD, respectively. Data from Kuwait in 2008 and Qatar are notable in that smaller (and probably immature) males and females of <75 cm WD occurred in approximately the same numbers, but a disproportionate amount of larger (and probably mature) animals >75 cm WD of just one sex occurred. In Kuwait in 2008, all animals >75 cm WD were female and were an order of mag- nitude more abundant than males of any size. As several of these females were pregnant with well-developed embryos, this observation may be related to parturition. In Rhinoptera species elsewhere, sexual segregation of adults around the time of parturition has been reported (Smith & Merriner, 1987), as has migration into areas at similar latitudes in April (Goodman et al., 2011) and large schools consisting mostly of pregnant females off southern India (James, 1962). The schooling nature of Rhinoptera species, as well as limiting life-history characters (e.g. low fecundity, Bizarro et al., 2006) may make them particularly vulnerable to fisheries impacts.

FISHERIES MONITORING AND MANAGEMENT These data suggest that species, sex and size composition of elasmobranch landings in The Gulf can vary markedly both geographically and between years at the same location. Additionally, the wide range of water temperature in The Gulf means that seasonal variation in abundance and distribution is likely to occur (Moore, 2011). With a view to collating data for input to a shark plan, a starting point for basic and inexpensive elasmobranch monitoring by Gulf states could therefore be a similar survey approach to that of this study in each of the four seasons and on an annual basis, but with appropriate consideration of geographical scale where neces- sary (e.g. the extensive coastline of Iran). This might, however, still underestimate total fishing mortality by not recording at-sea factors such as discards, as well as possibly under-representing valuable large sharks that may be finned at sea and landed elsewhere. These data highlight that recording at a species level is essential in any future monitoring. While largely accurate in itself, reporting of higher taxa such as Carcharhinidae, as is done for Abu Dhabi (Environment Agency Abu Dhabi, 2010) will fail to differentiate between small species and juveniles of larger species that are likely to be more vulnerable to fisheries. Species-level identification locally is especially important as rare, threatened and geographically restricted species occur, such as of juveniles of C. leiodon, alongside abundant small carcharhinid species in Kuwait.

The market surveys were supported in Kuwait in 2008 by the Kuwait Ministry of Interior (S. Al-Fahad and J. Failkawi), Y. Al-Khorafi, the Kuwait Scientific Centre, Gulf Telecom and the Kuwait Institute for Scientific Research (KISR); in Qatar by Qatar University Envi- ronmental Studies Centre (M. Al-Ansi, I. Al-Maslamani), Qatar Ministry of Environment, Department of Fisheries (M. Mohannadi); and in Kuwait in 2011 by the Kuwait Environmen- tal Research and Awareness Centre (KERA) and H. Muraad (PAAFR). We thank W. White and P. Last (CMAR, Australia), A. Henderson (SQU, Oman), L. Compagno (Shark Research Center, Iziko-South African Museum) for confirming identifications of problematic specimens and informative discussions; A. Marriott (Bangor University) for statistical help; K. Samimi- Namin (Netherlands Centre for Biodiversity Naturalis, Leiden) for the map and F. Al-Yamani (KISR) for temperature data. For invaluable assistance with market sampling, we thank D. Almojil and A. Alhafez (KERA), R. Jabado (U.A.E. University), A. Reeve (SCS/SQU Oman) and volunteers of the SCS (M. Barnes, T. Bennett, M. Boothman, S. Benzie, M. Bradfield, S. Collins, G. Gilgannon, D. Green, E.-L. Nichols, S. Nicholls, J. Peirce, C. Sayle, M. Sharland, A. Sweeney and M. Webb). Finally, we thank the many fishers and market traders for their patience, humour and generous help and the editor and referees for their helpful comments on an earlier draft version of the paper. The contents of this paper do not necessarily represent the views of the RSK Group.

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