Redescription of Pulchrascaris Chiloscyllii (Johnston and Mawson, 1951) (Nematoda: Anisakidae), with Comments on Species in Pulchrascaris and Terranova

Proc. Helminthol. Soc. Wash. 54(1), 1987, pp. 28-39

Redescription of Pulchrascaris chiloscyllii (Johnston and Mawson, 1951) (Nematoda: Anisakidae), with Comments on Species in Pulchrascaris and Terranova

THOMAS L. DEARDORFF Fishery Research Branch, U.S. Food and Drug Administration, P.O. Box 158, Dauphin Island, Alabama 36528

ABSTRACT: A review of the genus Pulchrascaris Vicente and dos Santos (type species P. caballeroi Vicente and dos Santos) and a new diagnosis are provided. Pulchrascaris differs from the most closely related genus, Terranova, by possessing greatly reduced lips with four toothlike structures, two on the dorsal and one on each subventral lip, on the inner surface and by lacking dentigerous ridges. Three species belonging to the genus Pulchrascaris are recognized: P. caballeroi, P. chiloscyllii, and P. secunda. A redescription of Pulchrascaris chiloscyllii, based on the holotype and supplementary material collected from the lumen of the stomach or within gastric ulcers of the scalloped hammerhead, Sphyrna lewini (Griffith and Smith), showed the species has a single medial preanal papilla, 42-55 pairs of preanal and six pairs of postanal papillae, modified preanal annules, and cuticular plates on the ventral surface of males. Histological observations of the gastric nodules associated with these worms show broad areas where the host tissues had undergone coagulation necrosis. This report extends the geographical range of P. chiloscyllii into the waters offshore from the northern Gulf of Mexico and the Hawaiian Islands. The name Pulchrascaris diazungriai (Vado) is placed in the synonymy of P. chiloscyllii. Pulchrascaris caballeroi (Vicente and dos Santos) is considered a valid species in the genus by possessing only 26 preanal papillae. Five species in the genus Terranova that parasitize elasmobranchs are recognized and discussed: T. antarctica, T. brevicapitata, T. nidifex, T. scoliodontis, and T. pristis. KEY WORDS: Pulchrascaris caballeroi, P. secunda, Terranova antarctica, T. brevicapitata, T. nidifex comb, n., T. scoliodontis comb, n., T. pristis, Acanthocheilus, Pseudanisakis, generic review, taxonomy, morphology, SEM, clasmobranch ascaridoids, gastric ulcers, Sphyrna lewini, sharks.

Mature nematodes were collected from the tube. Gastric ulcers were fixed in 10% phosphate-buff- stomach of a scalloped hammerhead shark, ered formalin, processed, and stained by using standard Sphyrna lewini (Griffith and Smith), caught in procedures (Luna, 1968). Specimens selected for scanning electron microscopy the northern Gulf of Mexico and in waters near (SEM) were dehydrated, critical-point dried in liquid the Hawaiian Islands. Attempts to identify these carbon dioxide, mounted on a specimen stub, coated materials, which are now considered in the genus with 200-300 A of gold-palladium, and examined with Pulchrascaris Vicente and dos Santos, 1972, re- a Cambridge Stereoscan 150 scanning electron micro- scope at 10 kV. vealed that the literature concerning this genus Abbreviations for repositories of examined nema- contained numerous inaccuracies and omissions. todes are BMNH, British Museum (Natural History), Additionally, the generic diagnosis needed clar- London, England; OCI, Oswaldo Cruz Institute, Hel- ification and revision. The purposes of this paper minthology Collection, Rio de Janeiro, Brazil; TAM, The Australian Museum, Sydney, Australia; USNM, are to distinguish Pulchrascaris from other gen- Helminthological Collection, United States National era of ascaridoid nematodes, redescribe a species Museum, Beltsville, Maryland. belonging to the genus Pulchrascaris based on the holotype and supplemental material, discuss Generic Diagnosis other material examined, and make appropriate synonyms and combinations. Pulchrascaris Vicente and dos Santos Pulchrascaris Vicente and dos Santos, 1972 (type Materials and Methods species P. caballeroi). Worms were removed from the host, fixed in glacial Body elongated, reaching greatest width near acetic acid, stored in a solution of five parts glycerin posterior third of body. Cuticle with annulations and 95 parts 70% ethyl alcohol, and examined in glyc- moderately defined. Cuticular alae distinct. Lips erin after evaporation of the alcohol. For spicule ratios, the length of the left spicule was defined as one. All indistinct, greatly reduced, approximately equal measurements are in micrometers unless otherwise in size; smooth, rounded, lacking cuticular flanges stated. Figures were drawn with the aid of a drawing on lateral margins; internal pulp indistinct; dor-

28 Copyright © 2011, The Helminthological Society of Washington 29 sal lip with 2 lateral double papillae and 2 tooth- cheilus Molin, 1858 (family Acanthocheilidae), like structures on inner dorsal surface between bears a strong resemblance to Pulchrascaris. Like double papillae; subventral lips each with am- Pulchrascaris, species in the genus Acantho- phid, adjacent mediolateral double papilla, sin- cheilus parasitize elasmobranchs. However, gle lateral papilla, and single toothlike structure Acanthocheilus, by lacking an intestinal cecum, on the inner dorsal surface nearest double pa- is easily differentiated from Pulchrascaris. A pilla. Dentigerous ridges absent. Interlabia ab- reexamination and reevaluation of the species sent. Deirids near nerve ring. Excretory pore be- belonging to the genus Acanthocheilus needs to tween base of subventral lips; with excretory duct be conducted to confirm the presence or absence with nucleus near nerve ring and excretory fila- of the intestinal cecum. It is possible that the ment, extending posteriad within left lateral cord intestinal cecum and/or other characters were past midbody, not present in posterior 14 of worm. not seen by researchers examining the worms, Ventriculus elongate. Intestinal cecum present. and the parasites were erroneously placed in Spicules similar, alate, equal or slightly unequal Acanthocheilus. For example, I examined spec- in length. Gubernaculum absent. Cuticular plates imens purported to belong to Acanthocheilus that present on males immediately posterior to anal are deposited at the USNM Helminthological opening. Modified annules present on ventral Collection. Of these, Nos. 6614 and 35535 (slide) surface of cuticle immediately anterior to anus. definitely had an intestinal cecum, and both lots Vulva anterior to midbody. Uterus didelphic, although in poor condition, had relatively pro- opisthodelphic. Tail conical; tip without orna- nounced lips; and No. 68650 (two vials) were mentation. Phasmids present. Parasites in the third-stage larvae with enough lip formation un- stomach of marine elasmobranchs and teleosts. der the sheath to suggest they were not in the Geographic distribution: amphitemperate and genus. Numbers 34785 and 6534 were specimens tropical seas. of Terranova and are discussed later. Clearly, the COMPARISONS: By possessing an intestinal type species should be critically reexamined. cecum and an excretory pore between the sub- Species belonging to the genus Pseudanisakis ventral lips and lacking a ventricular appendage (Layman and Borovkova, 1926) Mozgovoi, 1951, and interlabia, the genera Terranova Leiper and infect elasmobranchs, and some of these species Atkinson, 1914, and Pulchrascaris are most sim- also have reduced lips when compared with other ilar. In addition to the numerous morphological ascaridoids. These species, however, are easily affinities between these genera, they both have a differentiated from Pulchrascaris by having lips wide range of distribution and their subadults with one continuous dentigerous ridge. and adults principally parasitize elasmobranchs. REMARKS: The genus Pulchrascaris was These genera, however, are differentiated from erected by Vicente and dos Santos (1972) for the each other based on the morphology of their lips: species P. caballeroi, which was collected from Pulchrascaris lacks distinct lips and dentigerous C?)Squatina squatina. The authors' reasons for ridges and possesses toothlike structures. D. I. erecting this genus, however, appeared to be in- Gibson (pers. comm.) examined the female ho- sufficient. They differentiated the genus Pul- lotype of Terranova antarctica deposited in the chrascaris from the most closely related Terra- BMNH and confirmed the presence of distinct nova on the basis of "postanal chitinous apparatus lips and dentigerous ridges and the absence of (=cuticular plates) in the males, little teethlike toothlike structures. structures on the inner face of the lips and a long A toothlike projection similar to those on glandular ventriculus." The first character was species of Pulchrascaris was found on a single present in at least 12 species in the genus Ter- species of Terranova. Sprent( 1979) showed SEM ranova, the second in at least two species, and photomicrographs of "aconical cusps" at the the third present in all species. Deardorff and ventral end of the dentigerous ridge of each sub- Overstreet (1981) pointed out that the presence ventral lip of T. caballeroi, a parasite of snakes. or absence and location of various characters in No such structures, however, were present on the the genus Pulchrascaris needed to be determined. dorsal lip. The generic concept was upheld by Gibson and Considering all the genera recognized by Hart- Colin (1982) for species of Terranova that lacked wich (1974) in his key to the genera of the As- distinct lips. They transferred T. chiloscyllii cariodoidea, the lip morphology of Acantho- Johnston and Mawson, 1951, T. secundum

9 10 11 Figures 1-11. Pulchrascaris chiloscyllii. 1. Dorsal view of lip. 2. Ventral view of lips. 3. En face view. 4. Posterior end of male, showing caudal papillae, spicules, and modified ventral annules, lateral view. 5. Posterior of female tail, lateral view. 6. Body at level of intestinal-ventricular junction. 7. Male tail, showing postanal and

Chandler, 1935, and T. diazungriai Vado (as shaped, curving slightly ventrad, terminating with Vada), 1972, to Pulchrascaris and considered P. bluntly rounded process (Figs. 5, 7); process caballeroi as a junior synonym of P. chiloscyllii. slightly wrinkled. Based on the type specimen of P. chiloscyllii MALE (based on 12 specimens): Body 16-32 (TAM W3551) deposited by Johnston and Maw- mm long by 203-350 wide at greatest width; ratio son, as well as on supplemental material, the of greatest width to length 1:55-100. Lips 22-45 following redescription is provided. long by 45-55 wide. Nerve ring with center 290- 350 from anterior extremity, 24-42 in breadth. Pulchrascaris chiloscyllii Esophagus 1.3-1.7 mm long by 112-150 wide. (Johnston and Mawson) comb. n. Ventriculus 1.3-1.7 mm long by 90-150 wide; (Figs. 1-17) ratio of ventricular to esophageal lengths 1:0.9- Terranova chiloscyllii Johnston and Mawson, 1.1. Intestinal cecum 1.5-1.9 mm long by 81- 1951:291-292, figs. 1-4 (original description; 150 wide; ratio of cecal to esophageal lengths type host Chiloscyllium punctatum; type lo- 1:0.8-1.0; ratio of cecal to ventricular lengths cality Halfway Island, Central Queensland 1:0.8-0.9. Spicules similar, alate, 2.4-4.4% of coast, Australia). body length (Fig. 4), equal in length in 1 speci- Terranova diazungriai Vado, 1972:487-489, fig. men; right spicule 470-910 long by 22-36 wide; 5 (original description; type host Sphyrna lew- left spicule 481-930 long by 22-36 wide, greater ini; type locality Isla de Margarita Juan Griego, in length in 11 of 12 specimens; spicule to spicule Edo Nueva Esparrta, Venezuela). ratio 1:0.9-1.0. Gubernaculum lacking. Caudal Pulchrascaris diazungria: Gibson and Colin, papillae 47-60 pairs; preanal pairs 42-55, 50 on 1982:xxxvi-xxxvii (new combination). average, becoming more lateral and irregularly Pulchrascaris chiloscyllii Gibson and Colin, 1982: spaced as progressing anteriad (Figs. 4, 12, 14); xxxvi-xxxvii (new combination; with P. ca- medial preanal papilla conspicuous, located im- balleroi as junior synonym). mediately above anterior anal lip, 1 in number (Figs. 8, 12); postanal pairs 6, with pairs 2, 4, 5, Redescription and 6 from posterior located more ventral than GENERAL: Body reaching greatest width at pairs 1 and 3, and with pair 5 doubled and con- posterior % of worm. Cuticle with inconspicuous spicuously larger than others (Figs. 7, 8, 13, 17); annulations. Lips approximately equal in size, adanal papillae lacking. Cuticular plates 3, ven- widest at base, all wider than long; dorsal lip with tral, immediately posterior to anus, with serrated lateral double papillae and 2 toothlike projec- edges, each 11-22 long by 11-27 wide (Figs. 7, tions (Figs. 1, 16); subventral lips each with single 8, 12, 13). Modified annules on ventral surface mediolateral papilla, adjacent amphid, and me- beginning near anus, extending anteriorly be- diolateral double papilla and 1 toothlike struc- yond preanal papillae (Figs. 4, 12, 14). Tail flexed ture (Figs. 2, 3, 15); internal pulp round, indis- ventrad, 123-180 long, with blunt process at pos- tinct. Interlabia absent. Dentigerous ridges absent. terior extremity; process 11-22 long. Esophagus 4.7-9.2% of body length. Ventriculus FEMALE (based on 12 specimens): Body 27- longer than wide. Intestinal cecum equal to or 30 mm long by 406-481 wide; ratio of greatest greater than ventriculus (Fig. 6) except in 2 spec- width to length 1:62-67. Lips 36-45 long by 56- imens. Nerve ring located within anterior 18- 67 wide. Nerve ring with center 340-370 from 25% of esophagus. Cervical papillar pair near anterior extremity, 32-42 in breadth. Esophagus level of nerve ring. Excretory pore opening be- 1.7-2.0 mm long by 160-200 wide. Ventriculus tween base of subventral lips; excretory canal 1.7-2.0 mm long by 130-150 wide; ratio of ven- single, extending posteriorly along left lateral cord tricular to esophageal lengths 1:1.0. Intestinal beyond midbody; not present in posterior 1A of cecum 1.0-2.0 mm long by 140-260 wide; ratio worm. Lateral cords V-shaped and conspicuous of cecal to esophageal lengths 1:0.9-1.0; ratio of in cross section (Figs. 9-11, 19). Tail conically cecal to ventricular lengths 1:0.8-0.9. Vulva

medial papillae, lateral view. 8. Male tail, showing postanal papillae and cuticular plates, ventral view. 9-11. Lateral ala at anterior (9), midbody (10), and posterior (11) of worm.

Figures 12-14. Scanning electron micrographs of Pulchmscaris chiloscyllil. Numbers in parentheses indicate scale lengths. 12. Posterior end of male, showing preanal papillae and medial (med) and modified ventral annules

Figures 15, 16. SEM micrographs of Pulchrascaris chiloscyllii. 15. En face view of male, showing papillae, amphids, and excretory pore (arrow). Bar = 100 pm. 16. En face view, showing toothlike structures (small arrows) and excretory pore (large arrow). Bar = 100 /am. opening 7.6-9.4 mm or 28-31% of body length from P. chiloscyllii by lacking three cuticular from anterior extremity. Uterus didelphic, opis- plates on the ventral surface of the male. thodelphic. Eggs 33-42 in diameter. Phasmids located laterally. Tail 170-240 long. Remarks HOSTS: Sphyrna lewini (Griffith and Smith), In addition to adding new locality records, new scalloped hammerhead; S. zygaena (Linnaeus), synonyms, and new combinations, minor mor- smooth hammerhead (Sphyrnidae). phological variations, descriptions of previously SITES OF INFECTION: Free in lumen of stom- unreported structures, and observations on pa- ach, within gastric ulcers. thology associated with this species are provided. LOCALITIES: Kaneohe Bay, Oahu, Hawaii (S. I have been unable to locate and examine spec- lewini); offshore from Alabama (S. lewini}; South imens of T. diazungriai that were described by Africa (S. lewini, S. zygaena, and "shark"). Vado (1972) from Sphyrna lewini caught in waters SPECIMENS DEPOSITED: USNM Helm. Coll. near Isla de Margarita Juan Griego, Venezuela. No. 79483 (pair); University of Nebraska State Based on the original description, however, these Museum No. 23632 (pair). specimens are conspecific with P. chiloscyllii. COMPARISONS: The primary distinguishing Pulchrascaris chiloscyllii, then, is the senior syn- characteristic of Pulchrascaris chiloscyllii is the onym. presence of 42-55 pairs of preanal papillae. This Two male and two female nematodes (BMNH species is most similar to P. caballeroi, which Nos. 1982.2256-2260) from a "shark" and males has at least 26 papillae (see later discussion of P. (BMNH Nos. 1982.2261-2270) from S. zygaena caballeroi). Pulchrascaris secunda, the only other that were all caught off South Africa were ex- species belonging to this genus, is differentiated amined. They all appear to be P. chiloscyllii. One

(mva) (100 fim). 13. Male tail, showing postanal papillae and three cuticular plates (20 /mi). 14. Close-up of preanal papillae and modified ventral annules; note that some annules (arrows) do not completely encircle worm (20 Mm).

least four adult worms were counted (Fig. 18). Aggregates of worms were surrounded by broad areas where the host tissues had undergone coagulation necrosis. The periphery of these zones of necrosis was heavily infiltrated with lympho- cytes and mononuclear cells (Fig. 19). No nematode was attached to the host tissue. One other anisakine nematode, T. nidifex, has been reported within similar fibrous stomach nodules in a shark (see Linton, 1900, 1901. 1907. 1934). This gastric ulcer (USNM No. 6534) (Fig. 20) was 2.1 cm at its greatest width, 1.7 cm at its greatest opening, and approximately 0.5 cm in height. Whether P. chiloscyllii or T. nidifex caused the gastric ulcers or whether the ulcers were caused by some other source, in which case the worms lodged themselves within the ulcer and further aggravated it, is uncertain. Figure 17. Ventral view of tail of male P. chiloscyllii, showing pairs of postanal papillae. Bar =100 /xm. Pulchrascaris caballeroi (Vicente and dos Santos) Pulchrascaris caballeroi Vicente and dos Santos, male and three female worms (BMNH Nos. 1972:17-19, figs. 1-6 (original description; type 1976.2284-2299) that were removed from the host Squatina squatina; type locality Macae, mesentery of S. lewini also appeared to be P. State of Rio de Janeiro, Brazil). chiloscyllii, but these specimens were not mature. A sheath over the anterior end suggests that these I examined the holotypes of P. caballeroi (OCI worms may be fourth-stage larvae. Apparently, 30.649a, male; OCI 30.649b, female), which were this parasite occurs throughout the range of mounted on glass slides, and found most struc- sphyrnids. tures, measurements, and ratios to be very sim- Not all worms identified as Pulchrascaris chi- ilar to those reported by Vicente and dos Santos loscyllii and deposited in the BMNH can be re- (1972). Additionally, I counted 26 preanal, one ferred to the genus Pulchrascaris. At least two medial, and six postanal pairs of papillae, which mature males (BMNH Nos. 1982.2175-2177) differs from the 24 preanal, one adanal, and four that were collected from a black marlin, Makaira postanal pairs reported by Vicente and dos San- indica (Cuvier), near Ballito, South Africa, can- tos. Present on the male, but not reported or not. These specimens have salient lips with den- measured previously, were modified ventral an- tigerous ridges, and four ventral cuticular plates. nules, a 2.5-mm-long intestinal cecum, and lat- They appear to belong to the genus Terranova. eral alae. Pulchrascaris caballeroi may possess Based on the original description of Baylis (1931) more than 26 pairs of preanal papillae, but it is and the paratypes (BMNH Nos. 1938.7.15.13- impossible to determine if more are present be- 24), T. scoliodontis is the only species in the ge- cause the male holotype is permanently mounted nus with four cuticular plates. The importance on a slide. Based only on the original description of cuticular plates as a taxonomic character is of Vicente and dos Santos (Gibson, pers. comm.), discussed later. Gibson and Colin (1982) considered P. cabal- In addition to the 14 specimens of P. chilo- leroi a junior synonym of P. chiloscyllii. How- scyllii found free in the lumen of the stomach of ever, although very similar, the holotype of P. the infected shark caught near Hawaii, several caballeroi is best separated from its congener P. specimens were firmly encysted within two fi- chiloscyllii by having 26 pairs of preanal papillae. brous ulcers in the gastric wall of the host. Each It, therefore, must be considered a valid species. ulcer was open to the lumen of the stomach and Generally, the synonymy question for P. ca- nematodes within them were visible. Two male balleroi could be answered by examining sup- worms were dissected from one ulcer and, upon plemental specimens collected from the type host histological examination of the other ulcer, at and type locality; but, in this case, that would be

18 a

Figures 18, 19. Sections through ulcer in stomach of Sphyrna lewini. 18. Specimens of Pulchrascaris chiloscyllii surrounded by necrotic host tissue. Bar = 400 /urn. 19. Close-up of worms with nodule; note ala (a) and excretory canal (ex). Bar = 400 pm. difficult. Vicente and dos Santos reported the xxxvi-xxxvi (new combination; validation of type host to be the angel shark Squatina squatina genus). (Linnaeus, 1758). Their identification of the host is undoubtedly erroneous. According to Com- Lent and Teixeira de Freitas (1949) collected pagno (1984), S. squatina is only found in the and described what they believed to be mature eastern North Atlantic. Only the Argentine angel adults of Porrocaecum secundum Chandler, 1935, shark S. argentina (Marini, 1930) and the sand at La Paloma, Uruguay, from the intestine of an devil S. dumeril LeSueur, 1818, have been re- Atlantic cutlassfish, Trichiurus lepturus Lin- ported along the eastern coast of South America, naeus. I examined a male (OCI 31.356a) and two but neither species has a geographical range near females (OCI 31.656c, e) that were stained and Macae, Brazil. One of these two species is prob- permanently mounted on individual slides. The ably the host examined by Vicente and dos San- morphology of the lips differed slightly from the tos. The parasites of both S. argentina and S. illustrations (figs. 45, 46) and description of Lent dumeril should be critically examined. and Teixeira de Freitas. Each lip had the standard number and arrangement of papillae and Pulchrascaris secunda (Chandler) amphids seen on other anisakine worms; thus, Porrocaecum secundum Chandler, 1935:145 these characters contrast with the authors' de- (original description; type species Trichiurus scription and illustration of only two papillae. lepturus; type locality Galveston Bay, Texas). Neither the toothlike structures illustrated in their Porrocaecum secundum: Lent and Teixeira de figure 46 nor dentigerous ridges could be seen. Freitas, 1949:28-34 (description of adult and The cuticle appeared to be damaged or missing larval stages). from portions of the male anteriad of the anus, Terranova secundum: Olsen, 1952:188-189 (new making it difficult to determine the number of combination). preanal papillae and the presence of modified Pulchrascaris secunda: Gibson and Colin, 1982: ventral annules. Cuticular plates posterior to the

Figure 20. Photograph of syntype of Terranova nidifex deposited in the National Museum (Helm. Coll. No. 6534) by Linton, showing nematode coiled within ulcer in stomach of Galeocerdo tigrinus; worm not attached to tissue. Bar = 2 cm.

anal opening were lacking. Other material (OCI larvae between these genera is problematical. No 16.602f, e) was all fragments of portions of fe- larvae have yet been described as belonging to male worms. These slides were badly yellowed the genus Pulchrascaris. Rather, larvae of both and of little value. The third-stage larva (OCI genera apparently are considered as Terranova 16.603) was as described by Lent and Teixeira sensu lato. Based on the ratio between the lengths de Freitas. of the intestinal cecum and ventriculus, for ex- Because the specimens of Lent and Teixeira ample, P. chiloscyllii closely corresponds with de Freitas possessed indistinct lips with what the larval type designated as Terranova Hawaii appeared in their illustrations to be toothlike type B (Deardorffet al., 1982, 1984). This larval projections, I consider them in the genus Pul- type was generally found in the abdominal vis- chrascaris, as did Gibson and Colin (1982). Pul- cera of pelagic fishes such as carangids, lutjanids, chrascaris secunda differs from the other two scombrids, and serranids, and is probably the species in the genus by lacking cuticular plates same as T. secundum (as Porrocaecum) of Chan- on the male and by parasitizing a teleost. dler (1935) from Trichiurus lepturus in Galves- Whether or not the third-stage larva reported ton Bay, Texas, and Terranova type I of Cannon by Chandler (1935) is actually the juvenile stage (1977) from many marine fishes offshore from of the worm described by Lent and Teixeira de southeastern Queensland. Based on similar re- Freitas remains uncertain. Finding larval and lationships of the cecum and ventriculus, Can- adult stages, although similar, in the intestine of non suggested the Terranova type I larva was the same host does not necessarily suggest that most similar to P. chiloscyllii (as Terranova chi- they are the same species. Only life cycle studies loscyllii). The finding of these larvae in the same can solve such problems. localities as adult P. chiloscyllii further supports Although species of Pulchrascaris may be dif- Cannon's speculations. Until further life cycle ferentiated from those of the genus Terranova on studies are conducted, however, I refrain from the basis of lip morphology—features not pres- positively identifying P. chiloscyllii as the adult ent on larval stages—separation of third-stage stage of Terranova Hawaii type B.

Terranova brevicapitata (Linton) gion, was originally described by Linton (1900). Ascaris brevicapitata Linton, 1901:425, pi. Ill, Although in poor condition, the syntypes (USNM figs. 19-22 (original description; type host Ga- No. 6534) of T. nidifex deposited by Linton in leocerdo tigrinus; type locality Woods Hole, 1900 possessed comparatively salient lips, an Massachusetts region). elongated ventriculus, and an intestinal cecum Porrocaecum brevicapitatum: Baylis, 1931:97 in one specimen. Dentigerous ridges may be (new combination). present on the small, immature worm; however, Terranova brevicapitata: Mozgovoi, 1951 :vol. II, the poor condition of the lips makes confirma- p. 541 (new combination). tion difficult. This material appears to belong in Terranova brevicapitata: Gibson and Colin, 1982: the genus Terranova. Owing to the incomplete xxxvi-xxxvii (new combination; with T. sco- description of T. nidifex, Olsen (1952), Gibson liodontis as junior synonym). and Colin (1982), and others regarded it as species inquirenda. I agree. Corresponding males are Linton (1901) described Terranova brevicapi- necessary. Johnston and Mawson (1945) sug- tata (as Ascaris brevicapitata) based on four spec- gested that this species may belong to Terranova imens that he collected from Galeocerdo tigrinus and that T. galeocerdonis may be a junior syn- and one specimen "belonging to the National onym. This species, however, was never formally Museum." It appears that the single specimen placed in the genus, even though it is commonly Linton referred to was USNM No. 6382. Because referred to it. Therefore, A. nidifex (Linton) is no holotype was designated, I designate USNM transferred to the genus Terranova, as T. nidifex No. 6382 as the lectotype of T. brevicapitata comb. n. (Linton). Although the poor condition of the lectotype obstructed much of the internal structure, Terranova scoliodontis (Baylis) comb. n. the lip morphology was not diagnostic of Pul- Porrocaecum scoliodontis Baylis, 1931:95-97, chrascaris. No cuticular plates were seen. In 1920, figs. 1-3 (original description; type host Sco- MacCallum deposited additional material liodon sp.; type locality ?Cleveland Bay, (USNM No. 34584) of T. brevicapitata (as As- Townsville, Australia). caris brevicapitata) that he collected from the Terranova scoliodontis: Johnston and Mawson, same host and locality as the original specimens. 1945:111 (new combination). Of the five specimens with visible lips, three were Terranova brevicapitata: Not of Linton. Gibson similar to Pulchrascaris and two were similar to and Colin, 1982:xxxvi-xxxvii (in part; new Terranova. I counted 51 preanal and six postanal combination with T. scoliodontis as junior papillae and three cuticular plates on one of the synonym). male specimens lacking distinct lips. The two specimens belonging to Terranova were females. Although I agree with Gibson and Colin (1982) As it now stands, based on the original descrip- in their placement of T. brevicapitata, I do not tion, T. brevicapitata is distinguished from most believe that T. scoliodontis is a junior synonym other species in Terranova by lacking cuticular of the former. The paratypes of T. scoliodontis plates. (BMNH 1938.7.15.13-24) possess four ventral, cuticular plates, which distinguish this species Terranova nidifex (Linton) comb. n. from all other species in this genus. Further, within the genus, only T. scoliodontis has an ex- Acanthocheilus nidifex Linton, 1900:303, pi. 43, cretory system that has both a right and left fil- figs. 116-119 (original description; type host ament (Gibson, 1983). I consider Terranova sco- Galeocerdo tigrinus; type locality Woods Hole, liodontis, therefore, a valid species belonging to Massachusetts, region). the genus Terranova. Porrocaecum nidifex: Wulker, 1930:9 (new combination). Discussion Terranova nidifex: Johnston and Mawson, 1945: I recognize three species belonging to Pulchras- 111 (first inference as belonging to Terranova; caris. Both Pulchrascaris caballeroi and P. chi- new combination not stated). loscyllii parasitize elasmobranchs. If specimens Terranova nidifex (as Acanthocheilus nidifex), of P. caballeroi from the type host and type lo- which also was collected from the tiger shark, cality are critically examined, this species may Galeocerdo tigrinus, from the Woods Hole re- be found to be a synonym of P. chiloscyllii. The

Copyright © 2011, The Helminthological Society of Washington 38 PROCEEDINGS OF THE HELMINTHOLOGICAL SOCIETY wide distribution of P. chiloscyllii, as well as the evidenced in the genus Terranova. In addition wide distribution of larvae with similar mor- to T. pristis and T. scoliodontis, which infect elas- phology, suggests that the intermediate hosts have mobranchs, four other species— T. crocodili a wide geographic range. It is reasonable to as- (Taylor), T. lancellata (Molin), T. caballeroi Ba- sume that these intermediate hosts are restricted rus and Coy Otero, and T. draschei (Stossich)— to open-water fishes. Sharks probably acquire the have been reported to have cuticular plates. The infection throughout their geographical range. first three species are found in reptiles. The three Pulchrascaris secunda is the only species in the cuticular plates on these species are semilunar in genus known to parasitize teleosts. shape and directed posteriad. This contrasts This report recognizes five species belonging sharply with the condition in the two species to the genus Terranova that infect elasmo- parasitizing elasmobranchs. The edges of each branchs. Terranova brevicapitata, T. scoliodon- cuticular plate on T. crocodili and T. lancellata tis, and T. nidifex have been previously dis- are serrated; those on T. caballeroi are smooth. cussed. Terranova antarctica Leiper and Atkinson, Terranova draschei is the only species in the ge- the type species, was collected from the stomach nus that has semilunar-shaped plates and does of Mustelus antarcticus in Bay of Islands, New not parasitize a reptile; rather, it has been re- Zealand. This species is known from only female ported in the primitive fish Arapaima gigas from specimens. The fifth species, T. pristis, was de- the Amazon (see Baylis, 1927; dos Santos et al., scribed by Baylis and Daubney (1922) from the 1979). According to Sprent (1979), T. caballeroi, intestine of a sawfish, Pristis perotteti. I examined T. crocodili, and T. lancellata differ from T. dras- paratypes (BMNH 1982:2172-2174) and con- chei in the morphology of their spicules. cur with the original description with the excep- tion that the males have three cuticular plates Acknowledgments immediately posterior to the cloacal opening and I gratefully acknowledge David I. Gibson at at least 54 pairs of preanal and six pairs of post- the British Museum (Natural History), J. Ralph anal papillae. Gibson and Colin (1982) synon- Lichtenfels at the U.S. National Museum Hel- ymized T. galeocerdonis (Thwaite), T. rochali- minthological Collection, J. Julio Vicente and mai (Pereira), and T. ginglymostomae Olsen into Delir Correa Gomes at the Oswaldo Cruz Insti- T. pristis. I believe T. cephaloscyllii, which was tute, and Patricia Hutchings at The Australian found in the stomach of a cat shark, Cepha- Museum for loaning museum specimens. loscyllium unbratile Jordan and Fowler, from Nagasaki, should also be combined with T. pris- Literature Cited tis because, based on the description by Yama- Baylis, H. A. 1927. Some parasitic worms from Ar- guti (1941), these species cannot be differentiat- apaima gigas (teleostean fish) with a description ed. The holotype of T. cephaloscyllii could not of Philometra senticosa n. sp. (Filarioidea). Par- be obtained to corroborate the original descrip- asitology 19:35-47. tion. Terranova pristis is differentiated from all . 1931. On some Ascaridae from Queensland. Annals and Magazine of Natural History, series species in the genus by the males having three 10, 8:95-102. cuticular plates. -, and R. Daubney. 1922. Report on the para- The presence of cuticular plates appears to be sitic nematodes in the collection of the Zoological unique to these ascaridoids. Although the func- Survey of India. Memoirs of the Indian Museum 7:263-347. tion of the cuticular plates on the males is un- Cannon, L. R. G. 1977. Some larval ascaridoids from certain, the presence or absence, number, and south-eastern Queensland marine fishes. Inter- morphology of these plates on species belonging national Journal of Parasitology 7:233—243. to both Terranova and Pulchrascaris may have Chandler, A. C. 1935. Parasites of fishes in Galveston evolutionary implications. Cuticular plates ap- Bay. Proceedings of the United States National Museum 83:123-157. pear to be a primitive character, based on the Compagno, L. J. V. 1984. FAO Species Catalogue. fact that species that have similar cuticular plates Sharks of the World. An Annotated and Illustrated generally infect primitive hosts (elasmobranchs). Catalogue of Shark Species Known to Date. Part Hence, it is likely that the two genera are evo- 1. Hexanchiformes to Lamniformes. FAO Fish- eries Synopsis No. 125. Vol. 4. 249 pp. lutionarily very close. Deardorff, T. L., M. M. Kliks, M. E. Rosenfeld, R. A. Further, the morphology of these cuticular Rychlinski, and R. S. Desowitz. 1982. Larval plates is useful for identification to species, as ascaridoid nematodes from fishes near the Hawai-

ian Islands with comments on pathogenicity ex- colecao de nematodeos, parasites de vertebrados, periments. Pacific Science 36:187-201. do Museu de Historia Natural de Montevideo. —, and R. M. Overstreet. 1981. Review of Hys- Memorias do Institute Oswaldo Cruz 46:1-71. terothylacium and Iheringascaris (both previously Linton, E. 1900. Fish parasites collected at Woods = Thynnascaris) (Nematoda: Anisakidae) from the Hole in 1898. Bulletin of the United States Fish northern Gulf of Mexico. Proceedings of the Bi- Commission (1899) 19:267-304. ological Society of Washington (1980) 93:1035- . 1901. Parasites of fishes of the Woods Hole 1079. region. Bulletin of the United States Fish Com- -, R. B. Raybourne, and R. S. Desowitz. 1984. mission (1899) 19:405-492. Description of a third-stage larva, Tetranova type . 1907. Preliminary report on animal parasites Hawaii A (Nematoda: Anisakinae), from Hawai- collected at Tortugas, Florida, June 30 to July 18, ian fishes. Journal of Parasitology 70:829-831. 1906. Carnegie Institution of Washington, No. 5 dos Santos, E., J. J. Vicente, and C. R. Jardim. 1979. (1906), Washington. 112-118 pp. Helmintos de peixes de Rios Amazonicos da co- . 1934. Some observations on the distribution lecao helmintologica do Institute Oswaldo Cruz. of helminth Entozoa of fishes of the Woods Hole II. Nematoda. Atas Sociedad Biologia de Rio de region (Massachusetts, U.S.A.). Transactions of Janerio20:ll-19. the American Microscopical Society 52:121-131. Gibson, D. I. 1983. The systematics of ascaridoid Luna, L. G., ed. 1968. Manual of Histologic Staining nematodes—a current assessment. In A. R. Stone, Methods of the Armed Forces Institute of Pa- H. M. Platt, and L. F. Khalil, eds. Concepts in thology, 3rd ed. New York. The Blakiston Divi- Nematode Systematics 22:321-338. Academic sion, McGraw-Hill Book Co., 258 pp. Press, London and New York. Olsen, L. S. 1952. Some nematodes parasitic in ma- , and J. A. Colin. 1982. The Terranova enig- rine fishes. Publications of the Institute of Marine ma. Parasitology 85:xxxvi-xxxvii. Science at the University of Texas 2:173-215. Hartwich, G. 1974. Keys to the genera of the As- Sprent, J. F. A. 1979. Ascaridoid nematodes of am- caridoidea. 15 pages in R. C. Anderson, A. G. phibians and reptiles: Terranova. Journal of Hel- Chabaud, and S. Wilmott, eds. CIH Keys to the minthology 53:265-282. Nematode Parasites of Vertebrates. No. 2. Com- Vado, E. Y. 1972. Etude de huit nematodes parasites monwealth Agricultural Bureaux, Farnham Royal, de vertebres du Venezuela et de la Colombie. Bul- Buckinghamshire, England. letin of the Museum of Natural History, Paris, Johnston, T. H., and P. M. Mawson. 1945. Parasitic series III, no. 41:476-498. nematodes. B.A.N.Z. Antarctic Research Expe- Vicente, J. J., and E. dos Santos. 1972. Sobre um dition 1929-1931 Reports, series B (Zoology and nova genero da subfamilia Filocapsulariinae Ya- Botany) 5:73-160. maguti, 1961 (Nematoda, Ascaridoidea). Atas So- , and . 1951. Report on some parasitic ciedad Biologia de Rio de Janeiro 16:17-19. nematodes from the Australian Museum. Records Yamaguti, S. 1941. Studies on the helminth fauna of of the Australian Museum, Sydney 22:289-297. Japan. Part 33. Nematodes of fishes, II. Japanese Lent, H., and J. F. Teixeira de Freitas. 1949. Uma Journal of Zoology 9:343-396 + pis. 4-7.