Pristis pristis, PRISTIS (LINNAEUS, 1758)

Faria, Vicente V., Mcdavitt, Matthew T., Charvet, Patricia, Wiley, Tonya R., Simpfendorfer, Colin A. & Naylor, Gavin J. P., 2013, Species delineation and global population structure of Critically Endangered sawfishes (Pristidae), Zoological Journal of the Linnean Society 167 (1), pp. 136-164 : 146-152

PRISTIS PRISTIS ( LINNAEUS, 1758)

FIG. 4 ; TABLES 4 AND 5

Squalus pristis Linnaeus, 1758: 235 (valid as). Typelocality: ‘Europa’.

Pristis antiquorum Latham, 1794: 277 , pl. 26 (synonym). Unnecessary replacement name for Squalus pristis Linnaeus 1758

Pristis canaliculata Bloch & Schneider, 1801: 351 (synonym). Based on Latham: 277, pl. 26, which is Pristis antiquorum (= Squalus pristis ).

Pristis leichhardti Whitley, 1945: 44 (synonym). Type locality: Lynd River , northern Queensland, Australia .

Pristis microdon Latham, 1794: 280 , pl. 26 (synonym). Type-locality: not stated.

Pristis perotteti Müller & Henle 1841: 108 , 192 (synonym). Type locality: Senegal. No type material – possible paratype: MNHN A-9699, female 2850 mm total length (TL), stuffed ( Séret & McEachran, 1986).

Pristis zephyreus Jordan 1895: 383 (synonym). Type locality: Presidio River, Sinaloa, Mexico ( East Pacific ). Holotype: CAS-SU 12670; rostrum, head, and skin.

Diagnosis: A sawfish with robust rostrum, noticeably diverging posteriorly (rostrum width between two posteriormost rostral teeth 1.7–2 times the width between the second anteriormost rostral teeth). The number of rostral teeth per side ranges from 14 to 23. Rostral teeth with groove on the posterior margin. First dorsal-fin origin well anterior to pelvic-fin origins. Lower lobe of the caudal fin well defined (lower anterior margin about half as long as the upper anterior margin).

Nomenclatural discussion: The original P. pristis description ( Linnaeus, 1758) is here interpreted as representing a composite species. The Linnaean P. pristis description consisted of an identifying phrase (‘shark with a flat bony, sword-shaped snout toothed on both sides’, translated from the Latin). The nine references cited within this source described or depicted different sawfish specimens with either largetooth ( Clusius, 1605) or smalltooth ( Rondelet, 1554) characteristics. Subsequently, Latham (1794) revised the sawfishes. But in an odd nomenclatural decision, Latham (1794) made P. pristis a synonym to his newly described Pristis antiquorum . Cited references in the P. antiquorum description included Linnaeus’s original P. pristis description and the nine references originally cited by Linnaeus. The only new aspect in Latham’s (1794) P. antiquorum description was a drawing of a largetooth sawfish rostrum and a listing of body proportions. The rostrum depicted in Latham’s paper is clearly that of a largetooth sawfish. However, the body proportions were only poorly described. For example, pelvic fins were loosely described as ‘situated almost underneath the first dorsal’. The caudal fin was described as ‘occupying the tail both above and beneath, but longer on the upper part’. We hypothesize that the poor description and citations referring to different sawfish species made it confusing for subsequent authors to interpret and identify P. antiquorum as a largetooth sawfish. Specifically, we believe Müller & Henle (1841) misidentified one smalltooth sawfish as P. antiquorum . Müller & Henle’s (1841) morphological traits for P. antiquorum are 20–30 rostral teeth per side, gaps between rostral teeth increasing 3–4 times at the base, first dorsal fin origin above the origin of pelvic fins, and no lower caudal lobe. All of these characters describe a generalized smalltooth sawfish ( P. clavata , P. pectinata , or P. zijsron ). Duméril (1865) subsequently solidified the error in the literature by combining elements of Latham’s (1794) description of the P. antiquorum (largetooth) rostrum with Müller & Henle’s (1841) description of the body proportions for a smalltooth Pristis . Finally, Garman (1913) correctly asserted that P. pristis had priority over P. antiquorum . He defined P. pristis as a Mediterranean (European) sawfish with morphological characters as described in Duméril (1865). As this chimaeric ‘species’ would never be found in nature, Garman (1913) unwittingly established the myth of the extremely rare Mediterranean/West African P. pristis in the literature.

Relevant aspects of other junior synonyms are as follows: (1) P. microdon ( Latham, 1794) is a juvenile P. pristis , based on the rostrum depicted in the original description of the species; (2) Bloch & Schneider (1801) renamed P. antiquorum to Pristis caniculata to reflect the grooved posterior margins of the rostral teeth, a trait mentioned by Latham (1794) to define P. antiquorum , but one that is actually diagnostic for the genus Pristis ; (3) Müller & Henle (1841) clearly described a P. pristis specimen collected from freshwater in Senegal (West Africa) as their P. perotteti ; (4) Jordan (1895) described P. zephyreus based on differences in morphological proportions from West African P. perotteti , also invoking biogeographical differences to justify his designation of the Eastern Pacific population as a separate species. Finally, Pristis mississippiensis Rafinesque, 1820 is not a synonym of P. pristis , as the specimen on which this species was based has 26/27 rostral teeth per side, counts that are

F, female; M, male.

too high for P. pristis . Similarly, Pristis woermanni Fischer, 1884 is not a synonym of P. pristis , as its holotype also bears a high number of rostral teeth: 25/25.

Remarks: Garman (1913) was the first to link P. pristis to a drawing in Clusius (1605), one of the references cited by Linnaeus (1758) in the species description. Zorzi (1995) cited this link based on Garman (1913), but disagreed with him on the interpretation of the drawing. Garman (1913) considered that the specimen depicted lacked a subcaudal lobe, whereas Zorzi (1995) considered it to have one. We agree with Zorzi’s (1995) interpretation of the drawing, but disagree with Garman (1913), and consequently also with Zorzi, that P. pristis is based on Clusius (1605). As stated above, we interpret P. pristis originally as a composite species.

Description: A large sawfish with a shark-like body, head flattened with a comparatively broad-based, robust, and stout rostrum that tapers posteriorly and bears a series of lateral rostral teeth. The rostrum originates just anterior to the eyes (dorsally) and nostrils (ventrally). The tip of the rostrum is rounded.

Rostral teeth are triangular, slender, and elongated. The rostral teeth have a groove at the posterior margins at all maturation stages (detected as early as in neonates). Rostral teeth are relatively evenly spaced, although slightly closer toward tip of rostrum. The posteriormost rostral teeth are located just anterior to base of rostrum. The number of rostral teeth varies in number between 14 and 23.

Spiracles are located well behind eyes, on top of the head. Nostrils, mouth, and gill slits (five pairs) are located entirely ventrally on the head. Nostrils are short and broad, anterior to and separated from mouth, partially covered by large nasal flaps. Mouth is transverse and nearly straight.

The trunk is elongated and cylindrical dorsally, but strongly flattened below. Pectoral fins are distinct from head, broadly triangular, and not forming a disk as in the more modified batoids. Hind margins are straight, with posterior tip anterior to axil of pelvic fins. Pelvic fins are composed of a single lobe, triangular, and only moderately expanded. The two dorsal fins are large and well separated. They are of similar shape and size, although the first is slightly larger than the second. Both dorsal fins have strongly concave posterior margins and narrowly rounded apices. The first dorsal fin is located well anterior to the origin of the pelvic fin.

There is no clear division between the trunk and tail regions, the latter being stout and shark-like, with low lateral ridges. The caudal fin is well developed, with a concave rear edge and a short but noticeable lower lobe. Dorsal and lateral surfaces are uniformly brownish, with whitish ventral surface.

Size: The largest specimen examined in the present study was a female of 5790 mm TL (BMNH, uncatalogued, unknown locality). Prater (1939) reported a 6096-mm specimen caught off Mumbai. Large specimens recently reported include a 7000-mm specimen from Brazil ( Almeida, 1999), and a 6000-mm speci- men from Australia ( Peverell, 2005). Carvalho & McEachran (2003) cited 7500 mm as the maximum TL for this species.

Life history: Characterized by late maturity, low fecundity, and slow growth, contributing to a low intrinsic rate of population increase. The breeding season in Lake Nicaragua probably extended from May to July, with parturition taking place from early October into December ( Thorson, 1976). Also in Lake Nicaragua, size at birth ranged from at least 730–800 mm TL, with litter sizes of 1–13 (mean 7.3), following a gestation period of about 5 months ( Thorson, 1976). Thorburn et al. (2007) suggest that in Western Australia individuals of between 800 and 900 mm TL were recently born. In Lake Nicaragua, sexual maturity is reached at about 10 years of age and approximately 3000 mm TL, with a reproductive period lasting about 20 years ( Thorson, 1982). Maturity is attained at lengths greater than 2400 mm in the Indo-West Pacific population ( Compagno & Last, 1999). In Lake Nicaragua, breeding occurs every other year ( Thorson, 1976) and individuals spend much, if not all, of their lives in freshwater, with reproduction of the population occurring primarily in the lake ( Thorson, 1982). In Queensland, Australia, the species appears to pup in freshwater but can move into estuarine and coastal marine habitats ( Peverell, 2005).

Information about age and growth are as follows. In northern Australia and Papua New Guinea, the number of vertebral centra rings varied between 0 and 48, with the first appearing to be formed soon after birth, the second within a few months of birth, and the third over 1 year from birth ( Tanaka, 1991). Therefore, specimens with three rings appeared to be 1 year old ( Tanaka, 1991). If the second and successive rings were formed annually, the largest specimen with 46 rings would have been 44 years old ( Tanaka, 1991). A von Bertalanffy model was fitted to the back-calculated data (BCD) and the observed data (OD), with the following parameters generated: for BCD, L • = 398 cm, K = 0.047 year –1, and t 0 = -5.54 years; for OD, L • = 363 cm, K = 0.066 year –1, t 0 = -4.07 years. The annual growth rate was 180 mm in the first year and 100 mm in the tenth year ( Tanaka, 1991). However, this is in contrast with data from the West Pacific, in which young are born at 500 mm, and an individual grew from 600 to 2600 mm in 3 years ( Thorburn & Morgan, 2005). Thorburn et al. (2007) found the number of annuli, in conjunction with length–frequency data, suggested that in Australia individuals of 1000 mm TL were approximately 1 year old, those between 1400 and 1600 mm TL were approximately 2 years old, those between 1800 and 2200 mm TL were approximately 3 years old, and that the largest ones between 2300 and 2800 mm TL were likely to be at least 4 years old. Preliminary vertebral growth ring analysis estimated a maximum age of 51 years ( Peverell, 2006). Thorson (1982) suggested that specimens in Lake Nicaragua grow 350–400 mm in their first year, 120 mm in their tenth year, and 40–50 mm during each of the last 10 years of life, with a lifespan of over 30 years and maximum size of 4300 mm. On the basis of Thorson’s (1982) data, von Bertalanffy growth parameters were estimated by Simpfendorfer (2000) as L • = 456 cm, K = 0.089 year, and t 0 = -1.98 years. Simpfendorfer (2000) estimated an intrinsic rate of increase of 0.05– 0.07 per year and population doubling times of 10.3– 13.6 years.

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Distribution (mostly preterite) and habitat (see also Material examined): Eastern Pacific: Mexico, Guatemala, Nicaragua, Panama, Ecuador, and Peru. Western Atlantic: USA, Mexico, Belize, Guatemala, Honduras, Nicaragua, Costa Rica, Caribbean Sea, Colombia, Venezuela, Guyana, Suriname, French Guiana, and Brazil. Eastern Atlantic: Mediterranean, Senegal, Republic of Guinea, Guinea Bissau, Gambia, Sierra Leone, Liberia, Ivory Coast, Congo, Democratic Republic of Congo, Angola. Indo-West Pacific: South Africa, Zambia (Zambezi River), Mozambique (Zambezi River), Tanzania, Kenya, Madagascar, Pakistan, Gulf of Aden, India, Thailand, Vietnam, Cambodia, Singapore, Indonesia, Borneo, Philippines, Papua New Guinea, and Australia. Found in coastal, estuarine, and riverine habitats.

The type locality of P. pristis cited by Linnaeus (1758) as ‘Europe’ possibly refers to the Mediterranean Sea. However, no reliable museum specimen nor photographic evidence associated with a definite Mediterranean locality was found by the authors of this study. In fact, to this day, the occurrence of any sawfish species in the Mediterranean remains controversial. Stehmann & Bürkel (1984) argued that sawfish records in the area are questionable. These authors stated that largetooth sawfish records cited in Costa (1850) and Tortonese (1956) were based on museum specimens that had no associated locality data or were mislabelled. Nevertheless, Capapé et al. (2006) cited historical records for southern France. Furthermore, Psomadakis, Maio & Vacchi (2009) reported to have located a largetooth museum specimen stated to be from Italy. Sawfishes have been recorded well out of their year-round ranges, as indicated by the reports of P. pectinata in New Jersey / New York in the USA and Bermuda ( Bigelow & Schroeder, 1953), and of P. pristis in Cape Naturaliste, further south than any other sawfish in Australia ( Chidlow, 2007). This would argue in favour of their possible presence in the region. Nevertheless, evidence suggests that sawfishes have not formed resident, breeding, or core populations in the Mediterranean. Cultural and archaeological data from the Mediterranean are consistent with a long-standing lack of familiarity with sawfishes: no archaeological studies in the region have yielded sawfish remains ( Reese, 1984), there are no depictions of a sawfish in any cultural artifacts ( Boehmer, 2002), and where sawfishes are mentioned by the ancient Greeks and Romans, they are never described anatomically, nor are any details given about their behaviour, habits, or range ( Thompson, 1947: 219). This is in stark contrast with empirical knowledge of elasmobranchs in the ancient Mediterranean. Classical natural historians wrote at length about the behaviour and morphology of smaller and economically important elasmobranch species, such as dogfishes, skates, and torpedo rays [e.g. Aristotle’s Historia Animalium and Generation of Animals [c. 2362 years before present (BP)], Pliny the Elder’s Natural History (c. 1935 BP), and Oppian’s Halieutica (c. 1841 BP)]. If sawfish ever did occur in Mediterranean waters, they would have occurred in low numbers at the periphery of their East Atlantic distribution, which may account for the occasional suggestion of their presence in the region.

Alternatively, the ‘Europa’ locality in the P. pristis original description could refer to sawfish accounts in other parts of the continent’s coast arising from a mistaken view that sawfishes had a circumglobal marine distribution, including temperate and even arctic waters. The examples are several: (1) Linnaeus (1746) once included sawfishes as part of the Swedish fauna; (2) in The History of Fish, the sawfish is said to inhabit the northern seas of Iceland, Greenland, and Spitsbergen (Anon., 1818?); (3) according to an encyclopedia, ‘[sawfish] inhabit all seas, from the polar ice to the equatorial regions’ ( Lieber, 1851); Fox (1868: 684) asserted that ‘The saw-fish is amongst the most widely distributed of fishes, belonging to the arctic, antarctic, and tropical seas’; (4) a newspaper article called narwhals captured in Norway ‘sawfish’ ( Anon, 1902). This view of sawfishes as cosmopolitan animals may have its root in language. The etymology of the word pristis could derive from the Greek word for ‘saw’, or alternatively, to ‘blowing’ or ‘spouting’. Some classical texts group the fish the Greeks called pristis or pristes, and the Romans called serra, among the elasmobranchs, but just as often, these fishes are grouped with the whales. Furthermore, through the Renaissance period (1450–1600), sawfishes, orcas, swordfishes, and narwhals were popularly referred to as ‘sword-fish’ in various European languages. Consequently, sawfishes were erroneously assumed to: (1) inhabit Arctic seas, like narwhals (e.g. references cited above); (2) spout like whales (see the drawing in Rondelet 1554); (3) hunt like orcas and swordfishes, based on reports of ‘sawfish’ rostra (likely from swordfish) being taken from the flesh of whales ( Révoil, 1865).

POPULATION STRUCTURE

Population structuring among and within ocean basins was evident for all four sawfish species studied, based on either or both NADH-2 and the number of rostral teeth per side. Overall, these species exhibit a typical pattern of tropical coastal elasmobranchs, in which the dispersal of females, at least, might occur along coastlines, whereas great oceanic expanses and cold waters work as effective barriers ( Duncan et al., 2006). Two recent genetic studies using mitochondrial markers on A. cuspidata and P. pristis corroborate the hypothesis of structured populations. Across northern Australia both species were structured on a much smaller geographical scale ( Danastas, 2010; Phillips et al., 2011; respectively), suggesting that structuring occurs along coastlines.

Results suggesting a very low level of gene flow between the Indian Ocean and Western Pacific populations of A. cuspidata seem consistent. This pattern was obtained by both qualitative (exclusive haplotypes) and quantitative NADH-2 analyses (Fst), and the regional variation of the number of rostral teeth per side. In sharks, exclusive Indian Ocean and Western Pacific haplotypes were found for: the blacktip shark, Carcharhinus limbatus ( Keeney & Heist, 2006) ; the scalloped hammerhead, Sphyrna lewini ( Duncan et al., 2006) ; and the zebra shark, Stegostoma fasciatum ( Dudgeon, Broderick & Ovenden, 2009) . Historical and contemporary barriers may be involved in these patterns. The region has a complex geological history, and several biogeographical regions have been identified for marine fishes ( Blum, 1989). Periods of lowered sea levels in the last 3 Myr almost closed the sea connection between the Indian and Pacific oceans by a land connection between South- East Asia, New Guinea, and Australia, temporarily isolating marine organisms ( Benzie, 1998).

Furthermore, the exclusive haplotypes suggestive of the further substructuring of A. cuspidata into Indonesian and New Guinean–Australian groups are consistent with a major marine faunal break in the region. The chondrichthyan fauna of South-East Asia and the South-West Pacific differ considerably, based primarily on demersal species ( Last & Séret, 1999). This break has also been effective at the sister species and population levels for several marine organisms, including sharks (see discussion in Dudgeon et al. 2009). Three shark species have been shown to be genetically structured between Indonesia and Australia: the zebra shark, Stegostoma fasciatum ( Dudgeon et al., 2009) ; the spottail shark, Carcharhinus sorrah ; and the dusky shark Carcharhinus obscurus ( Ovenden et al., 2009) . Strong currents and deep trenches may restrict gene flow or isolate species or populations from these regions. Furthermore, the lack of differentiation of haplotypes between Australia and New Guinea suggests that the shallow waters that separate them may serve as a dispersal corridor, as hypothesized for Stegostoma fasciatum ( Dudgeon et al., 2009) .

In P. pristis , the fixation index (Fst) values obtained for major ocean basin comparisons revealed a significant restriction of gene flow between Atlantic, Indo- West Pacific, and Eastern Pacific populations. Three biogeographical barriers may be responsible for this: (1) the Isthmus of Panama (IOP), isolating the Eastern Pacific and Atlantic ( Coates & Obando, 1996); (2) the cold waters of the Benguela upwelling system, isolating tropical organisms of the Atlantic and Indian oceans ( Shannon, 1985); and (3) the immense expanse and deep waters of the Pacific Ocean, making dispersal between the western and eastern portions of this ocean difficult and unlikely for sawfishes, which have a mostly continental shelf distribution ( Robertson, Grove & McCosker, 2004; Wiley & Simpfendorfer, 2010). Other shark populations are also structured in similar patterns, along each of these barriers as follows: (1) IOP for the lemon shark, Negaprion brevirostris ( Schultz et al., 2008) , and the nurse shark, Ginglymostoma cirratum ( Karl, Castro & Garla, 2011a) ; (2) the Benguela current for the scalloped hammerhead shark, Sphyrna lewini ( Duncan et al., 2006) ; (3) the Eastern Pacific barrier for Sphyrna lewini ( Duncan et al., 2006) , the blacktip shark, Carcharhinus limbatus ( Keeney & Heist, 2006) , and lemon sharks Negaprion acutidens ( Schultz et al., 2008) .

Moreover, a finer scale level of structuring of P. pristis populations within the Atlantic was suggested by quantitative (phylogenetic) and qualitative (exclusive haplotypes) NADH-2 analyses, and regional variation of the number of rostral teeth per side. Corroborating this, other shark species also show some level of isolation between the Western and Eastern Atlantic: the blacktip shark, Carcharhinus limbatus ( Keeney & Heist, 2006) ; the lemon shark, N. brevirostris ( Schultz et al., 2008) ; and the nurse shark, G. cirratum ( Karl et al., 2011a) . These populations might be completely or at least partially isolated because of the mid- Atlantic Ocean’s deep and cold waters.

Results for the structuring of P. pristis in the Indo- West Pacific were inconclusive. First, the markers were not congruent for gene flow within this ocean basin: the restriction of gene flow between the Indian Ocean and the Western Pacific was suggested by quantitative (phylogenetic) and qualitative (exclusive haplotypes) NADH-2 analyses, but no geographical variation was found for the number of rostral teeth per side. Interpreting this pattern is difficult, as the variability of non-genetic traits is usually of unknown nature, being the product of complex environmental and genetic influences ( Grant, Garcia-Martin & Utter, 1999). Second, the geographical distribution of haplotypes in the Western Pacific did not follow the pattern shown for A. cuspidata and other coastal sharks in the region (present study and references cited above).

Lastly, the lack of geographical variability of NADH-2 sequences for P. pectinata and P. zijsron may not be interpreted as gene flow between populations of each of these species. This is because a lack of geographical structure suggested by any given molecular marker may result from several reasons, including at least: (1) sufficient gene flow to maintain panmixia; (2) sporadic recruitment from distant areas; (3) recent divergence of the compared populations; and (4) inadequate marker or sample size ( Carvalho & Hauser, 1995). Furthermore, Grant et al. (1999) suggested that evidence of geographical structuring based on nongenetic traits, such as meristic data, may indicate separate stocks, even when not apparent based on molecular data. Therefore, if we follow their concept, the significant difference in number of rostral teeth observed may indeed be sufficient information to indicate that each species is composed of separated populations: (1) Western/Eastern Atlantic populations for P. pectinata and (2) Indian Ocean/Western Pacific populations for P. zijsron .

Figures

Figure 4. The largetooth sawfish Pristis pristis. A, dorsal view of specimen from north-western Australia (photo: W. White); B, line drawing from FAO Species Catalogues.