Sea snakes (Elapidae, Hydrophiinae) in their westernmost extent: an updated and illustrated checklist and key to the species in the Persian Gulf and Gulf of Oman

Abstract The Persian Gulf is known as the westernmost distribution limit for sea snakes, except for Hydrophis platurus (Linnaeus, 1766) that reaches southeastern Africa. Previous identification guides for sea snakes of the Persian Gulf and its adjacent waters in the Gulf of Oman were based on old data and confined mostly to written descriptions. Therefore, a series of field surveys were carried out in 2013 and 2014 through Iranian coastal waters of both gulfs to provide a comprehensive sampling of sea snakes in the area. This paper presents an illustrated and updated checklist and identification tool for sea snakes in the Persian Gulf and Gulf of Oman, which are based on new material and a review of the literature. This checklist includes ten species of marine hydrophiines, of which one, Microcephalophis cantoris (Günther, 1864), is a new record for the area. All specimens examined herein are deposited and available at the Zoological Museum of Shahid Bahonar University of Kerman, Kerman province, Iran.


Introduction
All true sea snakes of the subfamily Hydrophiinae share a common ancestor dating back to approximately six million years ago, although the majority of the extant lineages have diversified in the last three and half million years . Now, more than 60 morphologically and ecologically diverse species of highly venomous marine hydrophiines live throughout tropical and subtropical coastal waters of the Indo-West Pacific region (Rasmussen et al. 2011b), with an exception, the Yellowbellied Sea Snake, Hydrophis platurus (Linnaeus, 1766), that lives in both Indian and Pacific Oceans (Heatwole 1999). These sea snakes colonize various coastal habitats throughout their geographic range and play an important role in the food web of these coastal biomes by consuming various prey (Voris 1972).
The Persian Gulf is a semi-enclosed shallow marine environment (mean depth ca. 35 meters) lying in a subtropical and hyper-arid region in the northwestern Indian Ocean. This water body is considered a young sea (~15,000 years) with impoverished species biodiversity. Biota living in the Gulf must adapt to high temperatures and a hypersaline environment (Price 2002;Sheppard 1993;Sheppard et al. 2010). Sea surface temperature in the Gulf varies from 18 to 34°C throughout the year and salinity is more than 39 ppt in most areas (Sheppard et al. 2010).
Populations of sea snakes in the Persian Gulf are peculiar for two main reasons. First, because the Gulf is known as the westernmost extent of sea snakes (with the exception of H. platurus, which is also found in the east coast of Africa) (Heatwole 1999). Second, because the Persian Gulf can be considered as an excellent natural laboratory to study the adaptive responses of the rapidly evolving sea snakes to high salinities and fluctuating temperatures.
Nonetheless, our knowledge about the sea snake diversity in the Persian Gulf and its adjacent waters is based on older studies (e.g. Smith 1926; Volsøe 1939), documenting the occurrence of nine species of the subfamily Hydrophiinae in the area. Recently, taxonomy of the true sea snakes has been revised based on comprehensive molecular phylogenetic analyses . After Sanders et al. (2013), sea snake species from the Persian Gulf and Gulf of Oman previously allocated to the genera Enhydrina Gray, 1849, Lapemis Gray, 1835and Pelamis Daudin, 1803 are now all assigned to the single genus Hydrophis Latreille in Sonnini & Latreille, 1801; and the Small-headed Sea Snake previously known as Hydrophis gracilis (Shaw, 1802) is now assigned to the genus Microcephalophis Lesson, 1834. Furthermore, our new material examination confirmed the occurrence of a second species of Small-headed Sea Snake, namely M. cantoris (Günther, 1864), in the Gulf of Oman. Therefore, the checklists and identification keys for the sea snakes in the gulfs (e.g. Egan 2007;Gasperetti 1988;Leviton et al. 1992) must be revised and updated by examining new material and using updated taxonomic classification (e.g. Sanders et al. 2013). This paper aims at presenting an illustrated and up to date checklist for sea snakes in the Persian Gulf and Gulf of Oman, as well as easy to use identification keys to the genera and species recorded in both gulfs.

Materials and methods
The sea snakes examined herein were collected from the Iranian coastal waters of the Persian Gulf and Gulf of Oman ( Figure 1). In this study, boundaries of both gulfs were assumed following International Hydrographic Organization (IHO). According to the descriptions of the organization, the Persian Gulf is separated from the Gulf of Oman by an imaginary line from Minab (27°00'N, 57°00'E) on the Iranian coast to Ras Qabr al-Hindi (26°20'N, 56°30'E) on the northeast tip of the Musandam Peninsula. Furthermore, the eastern limit of the Gulf of Oman is an imaginary line running from Ras Jiwani (25°01'N, 61°44'E) on the border of Pakistan and Iran to Ras al-Hadd (22°32'N, 59°47'E) in Oman (Figure 1).
Sea snakes were collected from by-catch of fishing trawlers in coastal waters of Bushehr Province in the western Persian Gulf, Jask and Ras-Meydani (Hormozgan Province) in the western Gulf of Oman and Beris and Pasa-Bandar (Sistan-O-Baluchestan Province) in the eastern Gulf of Oman in 2013 ( Figure 1). Sea snakes were also collected from mangrove swamps of Jask (Hormozgan Province) in the western Gulf of Oman in 2013, and coastal waters of Larak Island (Hormozgan Province) in the eastern Persian Gulf in 2014 ( Figure 1) using boat surveys.
A total of 14 characters was examined: each specimen was measured for total length (TL), snout-vent length (SVL), head length (HL), head width (HW), gap length (GL), snout to nostril length (SNL), nostril to eye length (NEL), neck diameter (ND) and greatest body diameter (GBD). Furthermore, number of supralabials (NSL), number of scale rows on the neck (NSR), number of scale rows on the body (BSR), number of ventrals (NV), and number of bands (NB) were also recorded for each specimen. SVL, HW, GL, SNL and NEL were measured following Ukuwela et al. (2012). HL was measured following Thorpe (1975). NSR and BSR were counted following Rasmussen (2001). NV was counted following Dowling (1951). After detailed morphological examination, a piece of trunk muscle was removed and preserved in ethanol 99% for future DNA analyses. All specimens were then preserved and fixed using the approved protocols (Leviton et al. 1992) and deposited in the Zoological Museum of Shahid Bahonar University of Kerman, Kerman Province, Iran (institutional code: ZMSBUK.HD).
Some external diagnostic characters (e.g. coloration patterns, number, size and shape of head shields, and body and ventral scales) were used to make updated and easy to use identification keys, which allow users to identify sea snakes in the field without the need of a binocular.
Morphological characters are presented using abbreviations (see above). Data of all measurements are in mm. Due to great interspecific and intraspecific variations in external characters of sea snakes (Rasmussen et al. 2011), diagnostic characters provided here are mostly applicable to the specimens from this area. Morphological data derived from previous literature dealing with sea snakes in the area are mentioned in brackets. Synonymies previously used for each species in the region are listed under each species. English common names presented herein are those suggested by the IUCN Red List of threatened species (IUCN 2016). Persian (Farsi) common names presented herein for the species in the genus Hydrophis are those suggested by Firouz (2005). For the two species in the genus Microcephalophis, English common names were directly translated into the Persian and presented herein as Persian common names. Tip of rostral markedly tridentate (Figures 2b, 2c, 3b, 3c); ventrals on midbody larger anteriorly than posteriorly, markedly distinguishable from adjacent scales (Figure 4a Body bands narrower than light interspaces ( Figure 15d) (Figures 14-15     Size. Mean TL 1036 mm, maximum 1230 mm (n = 14) [n = 3, maximum TL 1350 mm (Volsøe 1939)] General distribution. Indo-West Pacific, from the Persian Gulf to Australia (David and Ineich 1999).

Key to the genera of the subfamily Hydrophiinae in the Persian Gulf and Gulf of Oman
IUCN Red List Category. Least concern (IUCN 2016).

Remarks.
Hydrophis schistosus is distinct from other species in the Persian Gulf and Gulf of Oman due to its beaked-shaped rostral and dagger-shaped mental. Results of our field surveys showed that the species is more abundant in the Gulf of Oman rather than in the Persian Gulf. This is supported by other studies as eight specimens have been hitherto examined from the Gulf of Oman (Boulenger 1887(Boulenger , 1896Smith 1926;Volsøe 1939) versus three specimens from the Persian Gulf (Corkill 1932;Smith 1926;present study). Furthermore, during two months boat surveys in Hara (mangrove) Biosphere Reserve in the eastern Persian Gulf, only two specimens of the species were found (Rezaie-Atagholipour et al. 2012). Nonetheless, two specimens collected by Rezaie-Atagholipour et al. (2012) and the only specimen collected in this study were from Strait of Hormoz in the boundary of the two gulfs. Therefore these three specimens may be vagrant, and can not be strictly allocated to a particular population in the Persian Gulf. Concerning the two remaining specimens reported from the Gulf by Corkill (1932) and Smith (1926), no exact locality was mentioned. In conclusion, populations of H. schistosus in the Persian Gulf seem likely to be in low abundance. On the other hand, results of this study showed that the species is one of the most abundant sea snakes in the Gulf of Oman. In total,  26% of all specimens examined here were H. schistosus, all but one collected from the Gulf of Oman. Approximately 71% (261 of 367 specimens) of sea snakes that Safaei and Esmaili (2009) collected from coastal waters of Hormozgan Province (eastern Persian Gulf and western Gulf of Oman) were H. schistosus. They mentioned that most of these specimens were collected from Gulf of Oman. They failed however to report the exact proportions. Mating behavior of the species was sighted during a boat survey through coastal waters of Jask (western Gulf of Oman) in December 2013, the two animals having been seen intertwined and floating on the surface (Figure 7). Hydrophis schistosus is an aggressive sea snake. This snake is prey-specific, mostly consuming spiny catfishes (Glodek and Voris 1982;Voris and Moffett 1981).
Recent morphological and molecular evidence revealed that this species consists of two convergent lineages through its geographical distribution range. Now, the Australian lineage is elevated to species status and provisionally referred as to H. zweifeli (see Ukuwela et al. 2013).
Coloration. Dark gray dorsally, dirty white ventrally; with or without pale body bands broadest dorsally; tip of tail usually black (Figure 9d).
General distribution. Indian Ocean, from the Persian Gulf to Malay Archipelago (David and Ineich 1999).

Remarks.
Hydrophis viperinus is distinct from other sea snakes in the Persian Gulf and Gulf of Oman by having markedly rectangular-shaped and enlarged ventrals on the anterior part of the body. Smith (1926) and Wall (1921) mentioned that the Persian Gulf is the westernmost distribution limit of H. viperinus. Volsøe (1939) had doubts about it: "their only exact records from the Persian Gulf are however from Muscat, which is situated about 400 km outside the Strait of Hormoz". We agree with Volsøe (1939) as the two specimens we examined in this study and the specimens examined in other studies in the area (e.g. Boulenger 1887; Volsøe 1939) have all been collected from the Gulf of Oman. We did not find any specimen of H. viperinus in Iranian coastal waters of the Persian Gulf during our field surveys. Therefore, population of H. viperinus in the Persian Gulf, if present, seems likely to be in low abundance.
General distribution. Indo-West Pacific, from the Persian Gulf to Australia (David and Ineich 1999).

Hydrophis platurus (Linnaeus, 1766)
Coloration. This species has a unique color pattern making it distinguishable from other sea snakes; dorsal half of head and body black, dark green or dark brown, ventral half of head and body yellow, a markedly sharp contrast between dorsal and ventral portions; tail yellow in ventral portion, spotted or barred in dorsal portion ( Figure  13d); sometimes with pale dorsal color.
General distribution. Indo-Pacific, from east and south of Africa to the west coast of Americas (Heatwole 1999).
General distribution. Indian Ocean, from the Persian Gulf to Malay Archipelago (David and Ineich 1999).
Coloration. Body dark olive, grayish, or dirty white, dorsally darker and ventrally paler; 51-56 [44-54 (Volsøe 1939)] black rings broader dorsally, or broader bands tapering to points on laterals, on body and tail ( Figure 19d); head black in juveniles, usually with a yellow horseshoe-shaped mark above ( Figure 19b); adults with head sometimes of same color as body without the horseshoe-shaped mark (Figure 20b).
General distribution. Indo-West Pacific, from the Persian Gulf to Japan (David and Ineich 1999).
IUCN Red List Category. Least concern (IUCN 2016). Remarks. In the Persian Gulf and Gulf of Oman, juveniles of Hydrophis cyanocinctus (smaller than one meter) are morphologically close to H. lapemoides. In this case, focusing on the shape of scales in the thickest part of the body (with rounded or bluntly pointed tips versus more or less hexagonal or quadrangular in shape in H. lapemoides) is helpful (see diagnostic features for both species). But adults exceed one meter, which is very rare in H. lapemoides. Wall (1921) mentioned that H. cyanocinctus is probably the most abundant species in the region. Volsøe (1939) however mentioned that in the Persian Gulf it is equaled or even surpassed by H. lapemoides and H. curtus. Gasperetti (1988)   scales in thickest part of body more or less quadrangular or hexagonal in shape and juxtaposed; [29-31 scale rows on neck, 41-46 on body (Volsøe 1939)].
Coloration. Body olive-whitish, dirty white, darker dorsally and paler ventrally; [41-55 (Volsøe 1939)] black rings broader dorsally, or broader bands tapering to points on the sides, on the body and tail ( Figure 22a); head black in juveniles, usually with a yellow horseshoe-shaped mark above; adults with head sometimes of same color as body without the horseshoe-shaped mark.
Remarks. Hydrophis lapemoides may be easily misidentified with juveniles H. cyanocinctus in the Persian Gulf and Gulf of Oman (for more details see remarks on H. cyanocinctus). Rasmussen (1993) suggested that H. lapemoides is very abundant in the Persian Gulf. Gasperetti (1988) mentioned that H. lapemoides along with H. cyanocinctus are the most abundant sea snakes in both gulfs. We however could catch only one specimen during our field surveys, which was collected from Jask in the western Gulf of Oman.

Microcephalophis Lesson, 1834
Microcephalophis gracilis (Shaw, 1802) Common names: English -Graceful Small-headed Sea Snake, Slender Sea Snake; Farsi -Mâr-e daryâï-ye sarkuchak-e barâzandeh    HD.36), TL 900, SVL 820, HL 12.2, HW 5.1, GL 9, SNL 3.   Size. TL 1124 mm (n = 1) [1450 mm in males and 1880 mm in females (Leviton et al. 2003)] General distribution. Indian Ocean, from the Gulf of Oman to Malay Archipelago. IUCN Red List Category. Data deficient (IUCN 2016). Remarks. It is the first record of M. cantoris in this area. By this record, westernmost extent of M. cantoris expands from Pakistan to the Gulf of Oman. Safaei and Esmaili (2009) recorded four specimens of this species from the same area localities (Jask), but they have presented neither morphological data nor descriptions of the specimens. Furthermore, their specimens were not deposited in any public museum or collection and we couldn't find them for further morphological examination. Regarding the single specimen examined herein, the shape of the fangs was found to be unique: elongated fangs markedly protruding outside the lower jaw when mouth is closed. This unusual characteristic could be age-dependent or likely a specific character which was overlooked by other authors. Further studies on this specimen are much recommended.