Zootaxa, Chlamydoselachus africana, a new species ...

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ZOOTAXA

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Chlamydoselachus africana, a new species of frilled shark from southern Africa (Chondrichthyes, Hexanchiformes, Chlamydoselachidae) DAVID A. EBERT1 & LEONARD J.V. COMPAGNO2 1

Pacific Shark Research Center, Moss Landing Marine Laboratories, 8272 Moss Landing Road, Moss Landing, CA. 95039, U.S.A.; ph. 831-771-4427; fax 831-632-4403. E-mail: [email protected] 2 Shark Research Center, South African Museum, Iziko – Museums of Cape Town, P.O. Box 61, Cape Town 8000, R.S.A. E-mail: [email protected]

Abstract Frilled sharks (Chondrichthyes, Hexanchiformes, Chlamydoselachidae), long believed to be a monotypic family and genus, consisting of a single wide ranging species, Chlamydoselachus anguineus (Garman, 1884), is now known to contain at least two species. A new species of frilled shark, Chlamydoselachus africana, sp. nov., is described from five specimens collected from southern Africa. The new species, although difficult to distinguish externally from the well known C. anguineus, differ internally by the structural differences in the chondrocranium, lower total vertebral and spiral valve counts, and pectoral-fin radial counts. The new species, Chlamydoselachus africana, is known from off southern Angola, Namibia, and South Africa. Key words: Chlamydoselachidae, Chlamydoselachus africana, new species, Angola, Namibia, South Africa

Introduction The frilled sharks (Hexanchiformes, Chlamydoselachidae, Chlamydoselachus) are a little known but wide ranging group of deep-water sharks. The family and genus have one living species, with the frilled shark, Chlamydoselachus anguineus Garman, 1884, a medium-sized shark that reaches at least 1.96 m total length (TL), being the only known representative (Compagno, 1984; Ebert, 1990). This species is usually caught on or near the bottom between 120 and 1450 m depth, though it occasionally makes excursions into the midwater (Shiobara et al., 1987). Chlamydoselachus anguineus was first described by Garman (1884) from a 1.5 m TL female specimen purchased by the Harvard Museum of Comparative Zoology (MCZ), Harvard University. The exact location of capture is unknown, but it was likely southeastern Honshu, Japan, due to the close proximity of several deep water submarine canyons. Much of the early interest in this species stemmed from its supposed affinity with the cladodonts (Garman 1884, 1885; Gill 1884a, b). Gudger and Smith (1933) later showed, however, that C. anguineus actually possesses many specialized structural adaptations, while neurocranial studies by Compagno (1977) showed a close similarity between C. anguineus, other hexanchoids and squaloids. The anatomy of C. anguineus has been described in detail by numerous authors (Garman, 1885; Hawkes, 1907; Goodey, 1910; Allis, 1923; Gudger & Smith, 1933; Smith, 1937), but these studies were based on Japanese specimens, since their capture outside Japan is uncommon and most non-Japanese specimens have been deposited intact in museums and academic institutions. Smith (1967), based on two Namibian specimens, pointed out that not only did a certain degree of sexual dimorphism exist within the species, but that within each sex there is a wide variation in form. South Africa’s Marine and Coastal Management (MCM; formerly Sea Fisheries Research Institute) research ship FRS Africana has, since 1983, conducted cruises along the west coast of southern Africa aimed Accepted by MR. de Cavalho: 18 Jun. 2009; published: 31 Jul 2009

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at determining the biomass and recruitment of the Cape hakes (Merluccius capensis and M. paradoxus). Those two species are the target of a major demersal fishery. Since 1986, chondrichthyan samples for life history and systematic studies have been collected as a matter of course during these cruise surveys. During one of these Africana cruises, Cruise 059, in February 1988 a small, adult male Chlamydoselachus species was caught off Lüderitz, Namibia (26°38'S, 15°10'E). The small size at which maturity was attained in this specimen prompted closer examination of Chlamydoselachus material from this region and elsewhere. After anatomical, meristic and morphological examination it was determined that Chlamydoselachus species from the southeastern Atlantic Ocean were not conspecific with C. anguineus (described from Japan) and in fact represents an undescribed Chlamydoselachus species.

Methods Morphometric measurements follow Ebert (1990) and Compagno (2001) and meristic counts were taken on the holotype and five paratypes of C. africana and from 32 specimens of C. anguineus from Australia (n = 7), California, U.S.A. (1), Japan (9), New Zealand (5), the North Atlantic (4), Suriname (3) and Taiwan (3). Meristic counts were taken from skeletal material from Namibia, New Zealand, and Taiwan, and from literature accounts. Skeletal material was prepared through dissection and hot-water maceration. The material was rinsed in cold water to remove any extraneous tissue and to prevent the more delicate structures from falling apart from overcooking. The entire vertebral column, paired and unpaired appendages and crania were prepared by this method. Counts included those of the fin radials, vertebral column and cranium. Radial fin counts included those of the pectoral, pelvic, dorsal and anal fins. Due to poor centrum calcification, vertebral counts were taken by counting the basidorsals. The vertebral counts include monospondylous (MP), diplospondylous (DP) and caudal diplospondylous (DC) vertebrae. The position where the haemal arch formed in relation to the monospondyly-diplospondyly transition was recorded. Cranial measurements follow those of Compagno (1988) and Ebert (1990). Once all skeletal material had been cleaned, counted and measured it was place in 50% n-propyl or isopropyl alcohol for storage. Comparable morphometric and meristic measurements were also taken from the literature. Principal Components Analysis (PCA) was used to determine if Chlamydoselachus africana and C. anguineus individuals could be reliably distinguished based on morphometric variables. Only specimen data containing the full complement of measurements (50 variables) were included. In addition, because elasmobranch morphology often changes with ontogeny (Compagno, 1988), data were further limited to include only specimens of C. anguineus (916-1266 mm TL, n = 10) that were of similar size to those of C. africana (915-1170 mm TL, n = 5). Euclidean distance was used as a measure of dissimlarity to create a resemblance matrix between Chlamydoselachus individuals. A BEST analysis was subsequently conducted in PRIMER 6 (v. 6.1.6, 2008, PRIMER-E Ltd., Plymouth, England) to determine what variables best explained the morphological variation among individuals by maximizing a Pearson rank correlation between their respective resemblance matrices (Clarke & Gorley, 2006). Ninety-nine percent of the variability could be explained by 28 of the variables. PCA was conducted on these variables using a correlation matrix with Multivariate Statistical Package software (MVSP; version 3.13, Kovach Computing Services, Wales, UK). Case scores of the first (PC1) and second (PC2) principal component axes were interpreted and statistically evaluated to determine magnitude and sources of morphometric variability between Chlamydoselachus congeners. Data were first evaluated for normality and homoscedasticity using Kolmagarov-Smirnov and two–tailed variance ratio (F) tests, respectively (Zar, 1999). If data were determined to be normally distributed and of equal variance, two–tailed t–tests were applied to test the hypothesis that mean cases scores of C. africana and C. anguineus did not differ significantly ( = 0.05). If data did not meet the assumptions of normality or homoscedasticity, they were evaluated using two–tailed non–parametric Mann–Whitney U tests (Zar, 1999). Institutional acronyms following Leviton et al. (1985) and abbreviations for personal field numbers for

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the material examined are as follows: Australian Museum Sydney (AMS); British Museum Natural History (BMNH); California Academy of Sciences (CAS); Commonwealth Scientific and Industrial Research Organization (CSIRO), Tasmania, Australia; D.A. Ebert field number (DAE); Far Seas Fisheries Research Laboratory Shimizu (FSFRLS), Japan; Museum of Comparative Zoology (MCZ); Moss Landing Marine Laboratories (MLML), Moss Landing, California; National Science Museum Tokyo (NSMT), Japan; Rhodes University, South African Institute of Aquatic Biodiversity (formerly the J.L.B. Smith Institute of Ichthyology, RUSI), Grahamstown, South Africa; South African Museum (SAM); United States National Museum of Natural History (USNM).

Chlamydoselachidae Garman, 1884 Family Chlamydoselachidae Garman, 1884: 8. Type genus: Chlamydoselachus Garman, 1884.

Diagnosis. Hexanchoids with a slender, eel-like body, and prominent tropeic folds on the abdomen. The head has six paired gill openings, with the lower ends of the first gill extending across the throat. The snout is extremely short and truncated, the mouth being greatly elongated and terminal on the head. The teeth are alike in the upper and lower jaws, with three strong cusps and a pair of intermediate cusplets. The anal fin is larger than the single dorsal fin and the caudal fin lacks a subterminal notch.

Chlamydoselachus Garman, 1884 Chlamydoselachus Garman, 1884: 8. Type species: C. anguineus Garman, 1884, by original designation. Didymodus Cope, 1884a:275; 1884b: 412–413; 1885: 878. Chlamydoselache Günther, 1887: 22.

Chlamydoselachus africana sp. nov. Southern Frilled Shark (Figures 1, 2, Table 1) Chlamydoselachus anguineus: Smith 1951, 87; Smith 1965, 511, Fig. 3b; Smith, 1967: 105, pl. 19–23; Trunov, 1968, 137, fig. 3; Bass et al., 1975, 16, text fig. 9, pl. 6; Domanevskiy, 1975: 1117; Timokhin, 1980, 125; Allue et al. 1984, 124; Compagno 1984, 14, ill.; Bass 1986, 47, Fig. 3.1; Lloris, 1986, 87, figs. 17–18; Compagno et al., 1989, 19, pl. 2; Ebert 1990, 30, Fig. 3.1, Tab. 2.1; Compagno et al. 1991, 51, Fig. 3a (distribution map). Chlamydoselachus "sp. A" Ebert, 1990, 217, Fig. 3.12. Chlamydoselachus "sp. A" Compagno et al., 2005, 65, Plate 1

Holotype. SAM 31028, 1170 mm TL, immature female, off the Cunene River, Namibia, 19° 59'S, 11° 48'E, 409 m deep, trawled by RV Benguela. Paratypes. 4 specimens. RUSI 2423, 915 mm TL mature male, off Walvis Bay, Namibia; RUSI 2424, 1010 mm TL, immature female, off Walvis Bay, Namibia; SAM 36076, 916 mm TL, mature male, off Lüderitz, Namibia, 26°38'S, 15°10'E, 425 m deep, 19 February 1988; USNM 203466, 990 mm TL, mature male, Bahia Farta, Angola, 12°36'S, 13° 12'E, 5 April 1968. Diagnosis. An external morphologically similar looking, smaller-sized Chlamydoselachus (to at least 1170 mm TL) with a proportionally long head length 17.3–17.9% TL, prepectoral length 15.1–17.7% TL, predorsal fin length 62.6–64.5% TL, head height 6.2–8.6% TL and width 6.6–8.9% TL, broad interorbital width (5.7–6.4% TL) and internarial width (3.9–4.8% TL), mouth broad (6.0–8.1% TL), gill openings long, analcaudal fin space (0.2–1.3% TL), pectoral fin length (8.8–9.6% TL), pelvic fin length (11.6–15.4% TL), mean

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number of upper tooth rows (x = 28.8), pectoral mesopterygial radial counts (7), metapterygial radial counts (8), anal fin radials (30), total vertebral counts (147), MP vertebral count (18), DP count (76), DC count (52), MP/DP transition just posterior to the pelvic fins, spiral intestinal valve counts 26–28.

FIGURE 1. Lateral view of Chlamydoselachus africana, female, 1170 mm TL, holotype (SAM 31028).

FIGURE 2. Lateral view of Chlamydoselachus africana, male, 916 mm TL, paratype (SAM 36076), specimen now skeletonized. Illustration by L.J.V. Compagno.

Description. Proportional measurements expressed as a percentage of the total length are given for the holotype followed by the four paratypes in parentheses (Table 1). Skeletal description and clasper morphology based on adult male paratype (SAM 36076). Body long, slender, eel-like, compressed behind the pelvic fins. Pectoral-pelvic space is moderately long with a noticeable difference between males 23.0–24.1% and females 26.8 (24.6–27.7)% of total length. Head broad, flattened, wider than high, slightly convex; head length 17.3 (17.4–17.9)% TL. Preoral snout length 0.1 times mouth width. Snout tip broadly rounded. Nostrils lateral, width 5.9 in internarial width, 2.2 in eye length, and 0.2 in third gill opening. Eyes large, rounded, length approximately 10.1 times in head length. Spiracle present or absent and when present about 13.3 times in eye length and located about 3.3 eye lengths behind posterior margin of eye. Distance from snout tip to sixth gill opening 1.5 times in pectoral-pelvic space. Height of gill openings descending in length, with the sixth being about 1.4 times height of first; first gill opening extends across throat; width of third gill opening about 2.4 times in head length and 4.3 times eye length. Mouth broadly rounded, large, distensible, length is about 0.9 times in mouth width; the width is about 2.7 times in head length, and 1.0 of head width at mouth corners. Teeth are similar in both upper and lower jaws. Each tooth has three long, slender, smooth-edged cusps. Between each cusp is a small pointed cusplet. Upper medial teeth paired, form similar to anterolateral teeth, but noticeably reduced. Lower jaw with a single medial tooth that is undifferentiated from the anterolaterals. The teeth on upper and lower jaws are curved inwards and set on a broad base that projects behind and interlocks with the tooth base posterior to it. Tooth count for holotype is 14-2-14/13-1-13 (Tables 1 & 2). There was no sexual dimorphism observed between the teeth of male and female sharks. Lateral trunk denticles lanceolate, single cusped, with flattened bases. Crown slightly projected above the body with four longitudinal ridges extending from the base to the cusp. Denticle crowns widely spaced. Pectoral fins are broad, rounded and low on body. Both anterior and posterior margins are convex. Pectoral length 9.2 (8.8–9.6)% TL and 1.0 times into anterior margin length; pectoral fins much smaller than pelvic fins; pectoral origin is posterior to sixth gill opening. Pectoral fin skeleton radials (SAM 36076) extend about 3.6 times into length of pectoral anterior margin; radials divided into a maximum of six segments (Figure 3). Propterygium small with no radials, mesopterygium with 7 radials, and metapterygium with 4 radials on basal segment and 4 on metapterygial axis; total radial counts were 15 (Table 3).

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TERMS OF USE This pdf is provided by Magnolia Press for private/research use. Commercial sale or deposition in a public library or website is prohibited. TABLE 1. Proportional measurements expressed as a percentage of the total length for the type series of Chlamydoselachus africana.



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TERMS OF USE This pdf is provided by Magnolia Press for private/research use. Commercial sale or deposition in a public library or website is prohibited. TABLE 1. (continued)

TABLE 2. Regional tooth counts for Chlamydoselachus species. Source: 1. present study; 2. Bass, 1979; 3. Lozano Rey, 1928; 4. Garman, 1885; 5. Gudger and Smith, 1933; 6. Günther, 1887; 7. Hawkes, 1907; 8. Jordan and Fowler 1903; 9. Nakaya and Bass, 1978; 10. Collett, 1897; 11. Bertrand, 1926.

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TERMS OF USE This pdf is provided by Magnolia Press for private/research use. Commercial sale or deposition in a public library or website is prohibited. TABLE 3. Pectoral, pelvic, dorsal, and anal fin radial counts for Chlamydoselachus species. Source: 1. present study; 2. Braus 1902; 3. Deinega 1909; 4. Garman 1885; 5. Goodey 1910.

Pelvic fins large and broadly rounded, with anterior margin 1.0 times pectoral anterior margin; anterior and posterior margins convex; inner margin sexually dimorphic with males being somewhat longer than females. Inner margin of male paratypes do not form a clasper scroll. Pelvic fin skeleton (SAM 36076) is a flattened band of cartilage, slightly concave dorsally and enlarged at the ends; a long basipterygium with three segments from which 20 radials extend diagonally from its axis (Table 3). Pelvic radials with four segments each, except for the last two that are unsegmented. The claspers from one of the male paratypes (SAM 36076) consist of an elongated axial cartilage connected to the basipterygium by an intermediate segment followed by the beta cartilage. In the adult condition the end-style is joined by a terminal cartilage. Anal fin very large, broadly rounded, its height is 2.0 times dorsal fin height, base length 1.7 in dorsal base. Anterior and posterior fin margins are rounded and convex; an acute angle forms at the tip of the posterior and inner margins. Fin height 2.3 to 2.7 times into base and 2.0 to 4.2 times inner margin. Anal fin skeleton (SAM 36076) composed of an elongated basal cartilage with 30 radial cartilages (Table 3) extending diagonally from it; each radial has 4 segments. The dorsal fin is set far back, about 64.2 (62.6–64.5)% TL from snout tip, and low, only 1.9 times anal fin height. Anterior margin is rounded and convex with posterior margin. Base is short, 0.5 times dorsal-caudal space, height 3.1 times in base, and inner margin 0.9 times in height and 3.1 in base. The dorsal fin skeleton (SAM 36076) has a basal cartilage that is elongate, slightly convex distally and flattened proximally. Basal cartilage radials number 15 with each having four segments (Table 3). Caudal fin elongated, subtriangular, and without a subterminal lobe; length of dorsal margin 2.6 times in precaudal length. Total vertebral column count from SAM 36076 was 147. The MP-DP counts were 18 MP and 76 DP for a total precaudal count of 94 (Table 4). The transition between the MP and DP vertebrae occurred just posterior to the pectoral fins at the 18th vertebra. The caudal count (DC) was 53. The cranium of one paratype (SAM 36076) was dissected out and measured (Table 5). Neurocranium (Figure 4) short, with a blunt rostral cartilage, not hypercalcified in adult. Medial rostral cartilage length is about 19 times into nasobasal length. Width across lateral rostral cartilage bases about 4.9 times in length of medial rostral cartilage. Nasal capsules longer than wide, with rounded edges. Width of cranium across nasal capsules 1.7 in nasobasal length. Nasal apertures moderately large and transversely oval, separated by a space 1.8 times there widths. Anterior fontanelle large, rounded anteriorly, sub-triangular posteriorly, slightly longer than wide. Cranial roof 1.3 times orbital length. Orbital notches 1.3 times orbital length. Suborbital shelves 0.7 times orbital length. Otic capsules 0.9 times orbital length. The number of spiral valve turns was 27 for the holotype and ranged from 26–28 for the paratypes (Table 6). The liver is large and extremely oily, consisting of two lobes, one on each side of the body, extending the entire length of the abdominal cavity. The lobes are of equal size and alike in form. Coloration. In life a dark chocolate brown, but with a thin membranous mucous covering the shark that upon being rinsed off after death revealed a dark gray color beneath the membrane. Color after preservation varies from light brown to gray. A NEW SPECIES OF FRILLED SHARK


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TERMS OF USE This pdf is provided by Magnolia Press for private/research use. Commercial sale or deposition in a public library or website is prohibited. TABLE 4. Vertebral counts for Chlamydoselachus africana and C. anguineus. Monospondylous precaudal vertebrae (MP); Diplospondylous precaudal vertebrae (DP); Diplospndylous caudal vertebrae (DC).

TABLE 5. Cranial measurements expressed as a percentage of the nasobasal length for a C. africana, 916 mm TL, from Namibia (SAM 36076) and a C. anguineus, 1252 mm TL, from Taiwan (DAE 881204).

Etymology. The species name africana is in allusion to the Marine and Coastal Management research vessel “Africana” in recognition of the excellent research surveys this vessel has conducted over the past several decades. It is also the vessel that collected the paratype SAM 36076. Distribution. In the southeastern Atlantic, C. africana is confirmed only from off southern Angola southwards to southern Namibia (Figure 5). Although Indian Ocean records are scarce, Chlamydoselachus species have been caught in oceanic waters off the Transkei coast, Eastern Cape Province, South Africa (Timokhin, 1980) and off the kwaZulu-Natal coast (R. White, fishermen, kwaZulu-Natal, South Africa, pers. comm.). Specimens caught from off the Transkei coast were taken in depths of between 1230 and 1400 m (Timokhin 1980), while the kwaZulu-Natal specimen was caught in about 300 m depth by a ski boat fisherman (R. White, pers. comm.). One additional Eastern Cape record worth noting was reported by Smith (1951) of an angler who supposedly caught a Chlamydoselachus species from off a pier at Port Alfred.

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Unfortunately, the specimen was discarded before its identity could be confirmed. One of us (DAE) spoke with Margaret M. Smith (now deceased), former director J.L.B. Smith Institute of Ichthyology, Grahamstown, South Africa in December 1986 who knew the angler personally that caught this specimen and considered him to be very reliable in fish identification. Given that the continental shelf is very broad in this area it seems unlikely that this deepwater species would occur so far out of its normal range. It may be that this particular specimen was ill, disabled, or at least disoriented when caught. Thus, this record is only tentatively included here. Identification of these latter specimens as to whether they represent the new species, C. africana, or C. anguineus is unknown as these specimens were unavailable for examination. Size. The largest female on record, an immature specimen, is the holotype that measured 1170 mm TL. Males reach a maximum length of at least 990 mm TL.

FIGURE 3. Pectoral fin skeleton of (a) C. africana paratype SAM 36076 and (b) Taiwan C. anguineus (DAE 881204).

FIGURE 4. Illustration of Chlamydoselachus africana cranial skeleton with dorsal, lateral, and ventral views (paratype SAM 36076). Illustration by L.J.V. Compagno.



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FIGURE 5. Distribution of Chlamydoselachus africana. The star represents the location of the holotype, the closed triangles represent the capture locations of two paratypes, and the open triangle represents two paratypes caught at the same location. The open circles represent records of Chlamydoselachus specimens whose species identification could not be confirmed.

Biological notes. Based on the degree of calcification of the terminal cartilage elements it is concluded that male southern frilled sharks mature at a minimum size of 915 mm TL. The epididymis of adult male C. africana were enlarged and coiled and sperm could be expelled by applying pressure along the posterior portion of the genital papilla. Tanaka et al. (1990) concluded that the onset of maturity for male C. anguineus occurred at approximately 1100 mm TL. The smallest adult male recorded by Tanaka et al. (1990) was 1178 mm TL. Claspers of the Chlamydoselachidae are not enclosed within a scroll formed by the pelvic fin inner margin as in the Hexanchidae, but a hexanchid-like clasper sac is present in adult males of both C. africana and C. anguineus. No adult female C. africana were examined during this study. However, it is assumed that development is viviparous without placenta. Litter size is at least three based on an observation made by Dr. A.I.L. Payne (pers. comm., Cefas, Suffolk, England) of a specimen caught off Namibia, but not retained. Maturity in female C. anguineus has been variously reported from 1256 mm TL (Tanaka et al., 1990) to approximately 1500 mm

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TL (Gudger, 1940). A 1398 mm TL specimen illustrated by Gudger (1940) was immature while a 1550 mm TL specimen was mature. Tanaka et al. (1990) in an extensive study of C. anguineus found the minimum size of maturity in females to be 1256 mm TL. Fecundity has been reported as between 2 and 12 (Gudger, 1940; Tanaka et al., 1990).

FIGURE 6. Cranial skeleton, including dorsal, ventral, and lateral views of (a) Chlamydoselachus africana (SAM 36076) and (b) C. anguineus from Taiwan (DAE 881204).

FIGURE 7. Euclidean bi-plot of Principal Component 1 (PC1) and Principal Component 2 (PC2) case scores calculated from 28 morphological variables measured for Chlamydoselachus africana (n = 5) and C. anguineus (n = 10) individuals.

Examination of the holotype and paratypes of C. africana yielded some dietary information on this species. One paratype (SAM 36076), measuring 916 mm TL, contained a partially digested Apristurus sp., measuring approximately 265 mm from the cranial base to the caudal region and weighing 98.8 gm. Another



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paratype (RUSI 2424), 1010 mm TL, contained the skeletal remains of a digested cartilaginous fish, possibly a member of the family Scyliorhinidae. A 990 mm TL specimen (USNM 203466) from southern Angola had a squaloid spine embedded in its stomach. The 1170 mm TL holotype (SAM 31028) had a nearly intact Galeus polli measuring 342 mm TL and weighing 97.7 gm in its stomach. On the basis of the limited available data, it would appear that both species of frilled sharks prey primarily on scyliorhinid sharks though they probably feed on other items of an appropriate size. Taniuchi (1987) reported the remains of an Apristurus japonicus in a Japanese specimen. A North Atlantic specimen examined during this study was also found to contain the remains of an Apristurus sp. in its stomach. Unfortunately, very little else is known about the feeding habits of Chlamydoselachus species to confirm their suspected prey preference. However, predation on scyliorhinids and possibly squaloids, as well as other smaller deepwater sharks, would coincide with suspected movement patterns of both predator and its potential prey. Evidence has shown that Chlamydoselachus species are commonly caught in midwater trawls (Shiobara et al., 1987). Similarly, members of the genera Apristurus and Parmaturus are known to migrate vertically into the water column (Lee, 1969; Cross, 1988; Ebert et al., 1996). TABLE 6. Spiral valve counts for Chlamydoselachus species. Source: 1. present study; 2. Günther 1887; 3. Hawkes 1907; 4. Smith, 1937; 5. Collett, 1897.

TABLE 7. Hydrographic data for C. africana (SAM 36076) caught off Namibia at 26º 38' S, 15º 10' E on 19 February 1988. Key: salinity, S o/oo; dissolved oxygen, O2; nitrogen, N; silicates, Si; phosphates, P; chlorophyll A, Chl A.

The epipelagic ommastrephid squids found in the stomachs of Suruga Bay C. anguineus are fastswimming, highly active and relatively large species (Kubota et al., 1991). It was suggested that Chlamydoselachus may not be sufficiently swift to catch healthy fast squids but might prey on spent, post

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reproductive squids and injured individuals. Unfortunately the squid prey of C. anguineus examined by Kubota and colleagues were highly digested and could not be examined for reproductive condition or injuries. Chlamydoselachus species may indeed select spent or injured squids, but the possibility also exists that perfectly healthy epipelagic squid could fall prey to these sharks. The long mouth of the Chlamydoselachus species can accommodate relatively large prey, and their snakelike heads and firm, muscular bodies suggest that they may be able to slowly approach fast epipelagic squids, or might be approached closely by squid investigating or attacking them, and make a sudden snakelike lunge to snag them with their relatively strong, tooth-studded jaws. The mouth of Chlamydoselachus bears a functional resemblance to a squid jig, with many needle-sharp, inward and diagonally-directed curved points on its teeth which is enhanced by the outward rotation of the tooth rows when the jaws are protruded. Even a glancing strike by a shark on a squid or other soft-bodied prey could readily snag it. Squid might also jig themselves by grabbing at the conspicuous whitish tooth rows. Live Chlamydoselachus have been photographed swimming in captivity with mouth agape and with tooth bands highlighted by the dark mouth, but whether this lures squids into striking at the teeth and hooking themselves is speculative at present. Examination of fresh caught specimens of C. africana from southern Africa and C. anguineus from Taiwan revealed that the jaws and buccal cavity are highly distensible, suggesting that these sharks are capable of ingesting quite large prey items. The inwardly projecting, needle-sharp teeth further indicate that this is a highly specialized feeder. In addition, the abdomen is elongate and the stomach distensible, further indicating that this predator is capable of ingesting fairly large prey. Given these morphological characteristics, e.g. the elongated abdomen, anguiform tooth arrangement, terminal mouth, and highly distensible jaws, these sharks appear to have a rather specialized body arrangement reminiscent of gulper eels (Saccopharyngidae) or viperfish (Chauliodontidae). Furthermore, Chlamydoselchus species are capable of swallowing relatively large prey items ranging from 1/3 to at least 1/2 their own body length, in much the same way as gulper eels and viper fish are able to engulf large prey items. The Apristurus sp. found in the 916 mm TL Namibian specimen measured 29% of the predator's TL. However, this was only a partial measurement since most of the head and half the tail region had been digested. Forensic examination of the prey item indicated that it had been ingested whole. In life, it would probably have measured closer to 35 or 40 % of this shark's TL. The unique body shape of the Chlamydoselachidae is optimal for grasping and engulfing prey and their ability to forage in both demersal and midwater habitats indicate a highly evolved life style that is not remotely primitive. Thus, the Chlamydoselachidae appear to be highly specialized predators. Habitat. Hydrographic and substratum data are virtually unknown for Chlamydoselachus records published to date. Hydrographic data on a paratype (SAM 36076) caught at a depth of 425 m off southern Namibia indicate that it was in a low oxygen, high nutrient zone (Table 7), with a soft bottom substratum.

Comparison of Chlamydoselachus Species Comparison of proportional measurements from Chlamydoselachus species from different regions revealed a high degree of differences in proportional measurements between regions. It may be that in addition to the southern African C. africana there may be one or more different Chlamydoselachus species involved or the group may eventually prove to be a species complex. However, we identified a subset of measurements that showed consistent proportional differences between the new species and Chlamydoselachus species from elsewhere. These included a greater head length of 17.3–17.9% for C. africana versus 13.1–16.2% for C. anguineus, a greater prepectoral length, 17.0% versus 13.6–15.9%, a broader interorbital width of 6.0% versus 4.2–5.5%, greater internarial width of 4.4% versus 3.1–3.9%, a broader mouth width of 7.0% versus 4.0–6.3%, and proportionally longer gill openings. Direct comparison of Japanese (including the holotype of C. anguineus) and Taiwanese material revealed a further subset of measurements including differences in the anal-caudal space; shorter in C. africana 0.8% versus C. anguineus at 1.5–1.6%, a broader head height (7.3% versus 5.4–6.5%) and head width (7.5% versus 5.0–5.8%), a greater caudal peduncle height (4.5% versus A NEW SPECIES OF FRILLED SHARK


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3.2–3.5%), a greater pectoral fin length (9.2% versus 7.0–8.1%), and a greater pelvic fin length (13.2% versus 11.5–11.6%). The total mean number of upper jaw tooth counts is slightly higher in the four Namibian C. africana specimens (x = 28.8) relative to all C. anguineus examined from other regions. The upper jaw tooth count for the Angolan specimen fell within the range of C. anguineus (Table 2). The lower tooth counts were slightly higher in the Namibian specimens, with the exception of the North Atlantic specimens. The Angolan C. africana fell within the mid-range of the C. anguineus examined (Table 2). The pectoral fin radials of C. africana are slightly higher for the mesopterygium (7 versus 5–6) and lower (8 versus 9–12) for the metapterygium relative to C. anguineus (Table 3). The number of pelvic fin radials was similar to those of specimens from Japan and Taiwan as were the number of dorsal fin radials (Table 3). The number of anal fin radials is also slightly higher in C. africana (30) relative to C. anguineus (r = 20–28). Chlamydoselachus africana and C. anguineus strongly differ from each other in total vertebral counts, precaudal vertebral counts, and in the position of the MP/DP transition (Table 4). Total vertebral counts were 147 for a Namibian specimen of C. africana while New Zealand and Taiwanese specimens of C. anguineus were 160 and 171, respectively. The variability in the MP-DP counts was especially high. Two C. anguineus, one each from New Zealand and Taiwan, had an MP range of 72–75 and a DP precaudal count range of 21–27, while a C. africana had an MP of 18 and a precaudal DP of 76. The caudal counts (DC) differed widely, with C. anguineus having 58–78 and C. africana having 52. The transition between the MP and DP for C. anguineus was over the pelvic fins between the 72–75 vertebrae, while the transition in C. africana was just posterior to the pectoral fins at the 18th vertebrae. The crania of the two Chlamydoselachus species exhibit a number of morphological differences (Figure 6). These include the entire ethmoid region of the Taiwanese C. anguineus specimen (DAE 881204) being more elongated, and with a longer rostrum that is more ventrally thrust or angled, and has a slightly greater bend in the subethmoid fossa when compared to the C. africana paratype (SAM 36076). Other differences include the ventral edge of the rostrum in C. anguineus is opposite the mid-nasal capsule in the Taiwanese specimen, and in illustrations of Japanese C. anguineus (e.g. Allis, 1923), and is quite distinct when compared to the opposite dorsal surface in the Namibian C. africana. The ectethmoid processes are more elongate, broader, and more posteriorly expanded in the C. anguineus cranium, to the point of obscuring the front end of groove for orbital process in lateral, whereas in the C. africana cranium one can see space in front of these grooves, such that the basal angle is obvious. The subethmoid fossa is more antero-posteriorly elongated in C. anguineus, where as it is more laterally expanded and broad in C. africana. Comparison of the nasal fenestrae between the two species reveals that it is much smaller in C. anguineus when compared to C. africana. The orbital process grooves on the basal plate is more anterior in C. africana, but more posterior in C. anguineus. The basal plate between anterior grooves for the orbital processes is much more ventrally arched, convex and ridged in C. anguineus, but nearly flat in C. africana. The basal plate is more waisted behind the grooves in C. africana than in C. anguineus. The orbits are more upthrust and are slightly raised above the cranial roof in C. africana, but about opposite that in C. anguineus. The postorbital processes of C. africana are more elongated and bent or twisted, although not extreme in dorsal-ventral view; in lateral view it is less ventral, but higher than in C. anguineus, in which they extend to the ventral edge of the hyomandibular facet. The otic processes of C. africana are more laterally projecting (or sphenopterotic ridges less laterally expanded). The sphenopterotic ridge is higher in C. africana. The otic processes by comparison in C. anguineus are more angled posteriorly, and with a notch. The occiput is much more elongate and with greatly elongated occipital condyles in C. africana, but much shorter in C. anguineus (Figure 6b; Allis, 1923). Spiral valve counts are significantly lower in C. africana than in C. anguineus. The range of spiral valve turns for C. africana was fairly narrow, between 26 and 28, while the number of turns for C. anguineus ranged between 35 and 49 (Table 6). Chlamydoselachus africana individuals were clearly distinguished from those of C. anguineus based on PCA results. Principal components (PCs) 1 and 2 were interpretable and accounted for a considerable proportion (PC 1 = 38.6%, PC 2 = 17.2%) of total variation in morphological data. Principal component 1 was

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strongly bipolar (i.e., influenced by the differential contribution of two variables), with dorsal fin length (0.575) and, to a lesser extent, anal fin anterior margin (0.32) loading heavily to the positive. Conversely, several variables contributed similarly to negative loadings. Foremost among them were anal fin posterior margin (-0.358) and head length (-0.343). Results of the t-test conducted for PC1 case scores revealed highly significant differences between species (t = 4.859, P < 0.001), indicating that they could be reliably distinguished by the indicated variables (Figure 7). Species did not separate on PC2 (t = 0.632, P = 0.538; Figure 7). Chlamydoselachus anguineus individuals tended to load more positively, however, based primarily on proportional longer anal-caudal (0.137), dorsal-caudal (0.127), and head width (0.88) measurements.

Key to Species of Chlamydoselachus 1a. Total vertebral centra 160–171, MP-DP transition between the 72nd and 75th vertebral segment and occurs about over the pelvic fins. Spiral intestinal valve counts 35–49. Head length 13.1–16.2% of total length ..................................... ............................................................................................................. Chlamydoselachus anguineus Garman, 1884. 1b. Total vertebral centra 147, MP-DP transition at 18th vertebral segment just behind the posterior end of the pectoral fins. Spiral intestinal valve counts 26–28. Head length 17.3–17.9%......... Chlamydoselachus africana, new species.

Comparative material Chlamydoselachus anguineus: Australia (7 specimens): AMS 124101-09, 1360 mm TL, female, 33º 47’S, 151º 55’E, off Sydney, New South Wales, Australia; CA 4546, 1226 mm TL, adult male, New South Wales, Australia; CA 4488, 1370 mm TL adult male, New South Wales, Australia; CA 4540, 1435 mm TL, female, New South Wales, Australia; CSIRO H 5258-01, 807 mm TL, immature female, Sandy Cape, Tasmania, Australia; CSIRO H 5005-01, 853 mm TL, immature male, Tasmania, Australia; CSIRO H 286, 1140 mm TL, immature male, 39º 01’S, 148º 39’E, Bass Strait, Tasmania, Australia. California (1 specimen): CAS 20265, 1630 mm TL, female, 34º 23'N, 121º 03'W, 22 miles west of Pt. Arguello, California, U.S.A. Japan (9 specimens): Holotype, MCZ 800, 1527 mm TL, female, S.E. Honshu, Japan, only four pieces remaining from specimen; heart, immature gonads including ovaries and oviducts, and four vertebral segments; AMS I. 7698, 1346 mm TL, adult male, Suruga Gulf, Japan; BMNH 1887.3.19.4, 1220 mm TL adult male, Sigamya Bay; BMNH 1887.3.19.1, mature male, Japan; CAS SU 12923, 1468 mm TL female, Misaki, Japan; CAS SU 12922, 984 mm TL juvenile female, Misaki; MCZ 34247, 1150 mm TL, female, Yokohama, Japan; MLML 158 (0329), 178 mm TL, embryonic male, Japan; USNM 161522, 542 mm TL juvenile male, Shimizu, Japan. New Zealand (5 specimens): MLML uncat., 1424 mm TL, female, 42º 35’S, 170º 10’E, Hokitika Canyons, west coast, South Island, New Zealand; MLML uncat., 1325 mm TL, male, 42º 35’S, 170º 10’E, Hokitika Canyons, west coast, South Island, New Zealand; DAE 030011, 1390 mm TL, immature female, 43º 08’S, 174º 04’E, South Island, New Zealand; FSFRLS EI 523, 1410 mm TL, female, New Zealand; FSFRLS EI 861, 1130 mm TL, adolescent male, New Zealand. North Atlantic (4 specimens): BMNH 1961.5.11:1, 1508 mm TL adult male, 59º 50'N, 06º 30'W, eastern North Atlantic; BMNH 1962.7.17:1, 1750 mm TL adult female, 40–45 miles N.W. of Butt of Lewis, eastern North Atlantic; BMNH 1931.5.27:1, 1700 mm TL adult female, 59º 10'N, 07º 04'W, Brierly Bank, WyvilleThomson Ridge, eastern North Atlantic; MCZ 63259, 1320 mm TL, adolescent female, western North Atlantic off New England, U.S.A. Surinam (3 specimens): NSMT P40003, 671 mm TL immature or early adolescent male, Surinam, 7º 45.0’N, 53º 49.0’W to 7º 46.0’N, 53º 53.0’W, 758 m; National Science Museum Tokyo, NSMT P40090, 680 A NEW SPECIES OF FRILLED SHARK


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mm female, Surinam, 7º 51.0’N, 54º 15.0’W to 7º 52.0’N, 54º 21.0’W, 810 m; National Science Museum Tokyo, NSMT P40989, 1184 mm adult male, Surinam, 7º 50.0’N, 54º 17.0’W to 7º 49.0’N, 54º 13.0’W, 790 m. Taiwan (3 specimens): DAE 881204, 1252 mm TL, adult male, 24º 50'N, 121º 22'E, Ta-Chi, Taiwan; DAE 882104, 1571 mm TL, adult female, 23º 06'N, 121º 22'E, Cheng-Kung, Taiwan; DAE 882304, 1410 mm TL adult male, 22º 26'N, 120º 30'E, Tung-Kang, Taiwan.

Acknowledgements We would like to thank Andrew Payne (Cefas), C.J. Augustyn, Rob Leslie (Marine and Coastal Management, Cape Town, South Africa), the late Capt. D. Krige and the officers and crew of FRS Africana, Paul Cowley (South African Institute for Aquatic Biodiversity, formerly the J.L.B. Smith Institute of Ichthyology JLBSII, Grahamstown, South Africa), Tom Hecht (Department of Ichthyology and Fisheries Science, Rhodes University, Grahamstown, South Africa), Barrry Rose (Irvin and Johnson, Cape Town), the late Martina A. Compagno-Roeleveld, Cedric Hunter, Sidney Kannemeyer, Cedric Goliath, Mike Bougaardt, Michelle van der Merwe and Elizabeth Hoensen (Iziko - South African Museum, I-SAM), Nigel Merrett (British Museum Natural History), Susan Jewett (United States National Museum), Shoou-Jeng Joung (National Taiwan Ocean University, Kee-lung, Taiwan), Karsten Hartel (Museum of Comparative Zoology, Harvard University), John Paxton and Mark McGrouther (Australian Museum, Sydney), Andrew Stewart (Museum of New Zealand), Malcolm Francis (National Institute of Water and Atmospheric Research), Keiichi Matsuura (National Science Museum, Tokyo, Japan), Peter Last and Alastair Graham (CSIRO Marine and Atmospheric Research, Hobart, Tasmania) and Jenny Kemper (Pacific Shark Research Center, Moss Landing Marine Laboratories). We would especially like to acknowledge Joseph Bizzarro (Pacific Shark Research Center, Moss Landing Marine Laboratories) for performing the PCA analysis and writing the corresponding methods and results sections. DAE thanks NOAA/NMFS for their support of the National Shark Research Consortium and Pacific Shark Research Center, and the South African National Research Foundation (NRF). LJVC’s research funding was provided by the South African Council for Scientific and Industrial Research, NRF, JLBSII, and I-SAM.

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