Marine Aspidogastrids (Trematoda) from Fishes in the Northern Gulf of Mexico

University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln

Faculty Publications from the Harold W. Manter Laboratory of Parasitology Parasitology, Harold W. Manter Laboratory of

10-1977

Sherman S. Hendrix Gettysburg College, [email protected]

Robin M. Overstreet Gulf Coast Research Laboratory, [email protected]

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Hendrix, Sherman S. and Overstreet, Robin M., "Marine Aspidogastrids (Trematoda) from Fishes in the Northern Gulf of Mexico" (1977). Faculty Publications from the Harold W. Manter Laboratory of Parasitology. 487. https://digitalcommons.unl.edu/parasitologyfacpubs/487

This Article is brought to you for free and open access by the Parasitology, Harold W. Manter Laboratory of at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications from the Harold W. Manter Laboratory of Parasitology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. THE JOURNAL OF PARASITOLOGY Vol. 63, No. 5, October 1977, p. 810-817

MARINE ASPIDOGASTRIDS(TREMATODA) FROM FISHES IN THE NORTHERNGULF OF MEXICO*

Sherman S. Hendrixt and Robin M. Overstreett

ABSTRACT: Of the aspidogastrids Multicalyx cristata, Lobatostomaringens, Cotylogaster basiri, and C. dinosoides sp. n., the last two had not been previously known from the Gulf of Mexico. The latter differs from other members of its genus by having relatively large equatorial marginal alveoli in comparison to those at the anterior and posterior ends of the holdfast. It also possesses extensive transverse musculature connecting opposed lateral alveoli. New host records are included for all four species, and we report preadults of what appear to be the first two species.

Trematodes belonging to the family Aspido- (19) elongate transverse alveoli, with prominent and on alveolar gastridae Poche 1907 infect marine and estu- marginal organs papillae ridges; alveoli with glandularcells. Neck arine fishes, but few document the marginal supplied reports retractile, bearing conspicuous flange near base relatively common occurrence of these worms allowing neck to retract, terminating with buccal in the Gulf of Mexico. Of the four we found disc; disc displaying 1 dorsal, 2 lateral, and 2 ven- in Mississippi and adjacent areas, one is new trolateral lobes under appropriate fixation; dorsal lobe when not inverted and form- and one other had never been reported from acutely pointed cleft. Tail retractile, with ratio of portion ex- the Gulf. ing tended beyond holdfast to holdfast-length 1:3 to Described material was removed fresh from 53 depending on length of worm and state of con- the hosts and fixed with hot AFA solution traction; well-contracted and not extended beyond under minimal coverslip pressure. Totomounts holdfast in holotype. Tegument aspinose. Eyespots 5 to 19 (dispersed) long by 3 to 12 were stained with Van Cleave's hematoxylin or pigmented, (dispersed) wide when compacted, often diffuse rarely with Semichon's carmine and sections especially in large individuals. Ring of prominent with Harris' or Heidenhain's iron hematoxylin, outer longitudinal and inner circular muscles com- and often with eosin. Figures were drawn with the partmentalizingalimentary reproductiveorgans from level of midneck to aid of a camera measurements are in approximately postequa- lucida; torial level; less dense musculature extending to micrometers unless stated otherwise. near tip of tail. Groups of cells underlying dorsal anucleate tegument. Prepharynx195 to 494 (255) 465 93 to 255 Cotylogaster basiri Siddiqi and Cable 1960 long. Pharynx 180 to (299) long by to 1/3 with dense concentric (Figs. 1, 2, 5, 6) (223) wide; anterior1/4 circular muscle fibers; central area of posterior Redescription (based on 15 whole mounts, 2 sec- portion filled with nucleated cells. Esophagus non- tioned later; values for holotype in parentheses): epithelialized, short, indistinct when contracted. Body 1,554 to 7,336 (4,650) long by 870 to 2,278 Cecum a simple epithelialized sac; termination (1,871) at widest level of ventral holdfast. Ven- variable within gonadal level; posterior portion in tral holdfast organ 1,451 to 4,007 (3,530) long, atypical specimen with 1 simple and 1 bilobed occupying all of ventral surface of body excluding pedunculated outpouching. neck and "tail" (= terminal muscular dorsal cone), Testes 2, tandem to diagonal, rarely symmetrical, possessing one continuous marginal row of 60 to usually separated from each other, postequatorial; 66 (56) cuplike alveoli and medial row of 19 to 23 anterior testis 105 to 806 (339) long by 135 to 488 (235) wide; posterior testis usually sinistral to one when 128 to 626 Received for publication 28 January 1977. anterior diagonal, (335) long 102 to 603 wide. Seminal vesicle * This study was conducted in cooperation with by (273) sinuous, the U.S. of often swollen at ends or elsewhere. Prostatic ves- Department Commerce, NOAA, 742 49 to 322 National Marine Fisheries Service, under PL icle elongate, 263 to (568) long by No. 2-262-R and Office (145) wide, lined internally with membrane-bound 88-309, Project NOAA, surrounded con- of Sea Grant, under Grant No. 04-6-158-44060. anucleate bodies, externally by The U.S. Government is authorized to spicuous layer of prostatic cells approximating produce Cirrus and cirrus sac and distribute for governmentalpurposes width of vesicle. lacking. reprints duct and notwithstandingany copyright notation that may Ejaculatory variably-shaped genital hereon. atrium surroundedby glandular cells. Genital pore appear to forward t of Biology, Gettysburg College, median, usually immediately posterior Department into defined Gettysburg, Pennsylvania 17325. margin of holdfast organ, opening t Gulf Coast Research Laboratory,Ocean Springs, cavity external to compartmentalizingmusculature Mississippi 39564. but internal to holdfast organ or tegument at neck 810 HENDRIXAND OVERSTREET-ASPIDOGASTRIDSFROMNORTHERN GULF OF MEXICOFISHES 811

level in extended specimens; cavity widening an- original description are that a true cirrus sac teriorly, opening to environment at or immediately is lacking, a point already made by Frederick- anterior to forward margin of holdfast, regulated sen (1972), and that the excretory system is by contractionof flange. bivesiculate rather than having an I-shaped Ovary anteriomedial and often contiguous to bladder. Depending on the contractionof the anterior testis, smooth, 132 to 546 (342) long by the vesicles 75 to 425 tail, open separately or into an (220) wide. Laurer's canal passing at the the dorsally along less dense extension of muscular invagination tip, giving appearance compartmentalizationand opening to surface sub- of a V-shapedbladder. terminally and dorsally near posterior tip of tail. An important feature of C. basiri and all Seminal receptacle of uterine type. Ootype usually other species of Cotylogaster Monticelli 1892 adjacent to ovary, relatively small. Oviduct re- is the circularand mus- curved. cylindrical longitudinal Vitelline reservoir usually posterior to cle that encircle much of the ootype, receiving 2 vitelline ducts laterally from layers alimentary continuous or occasionally interrupted inverted U- tract and reproductive system (Figs. 5, 6). shaped band of follicles; posterior level of band Most aspidogastridspossess a transverseseptum lying within testicular level, less extensive in holo- that divides the dorsal portion containing the type since right branch extending to ovarian level tract and terminal from a one to alimentary genitalia and left anterior that; anteriorlevel variable; ventral the follicles 21 to 165 long by 15 to 90 wide. Uterus portioncontaining gonads. Cylindri- voluminous in large specimens, extending anteriorly cal compartmentalizationdiffers among species to anterior loop of vitellaria and occasionally as as will be seen in the following species having far anterior as midlevel of prostatic complex, oc- gonads externalto the compartment. cupying most of posterior 1/2 of worm including All the listed hosts new records. metraterm wider represent tail; muscular, usually distally the was than proximally, longer than prostatic vesicle, sin- Previously, parasite known only from istral to prostatic complex, usually entering genital the porgies Calamus calamus (Valenciennes) atrium at same level as ejaculatory duct, sur- and C. bajonado (Bloch and Schneider). rounded by glandular cells occurring most con- Those infections occurredin Puerto Rico (Sid- spicuously at distal end. Eggs numerous, 53 to 78 and and long by 27 to 41 wide, containing biocellate larvae; diqi Cable, 1960) Jamaica (Nahhas larvae often hatching within uterus. and Cable, 1964). Thus, our records extend Excretory system bivesiculate; collecting tubules the parasite'sgeographical range to the north- recurving posteriorly near anterior of buccal disc; ern Gulf of Mexico. pore terminal or dorsal and subterminal depending Based on the of both small on state of contraction of both vesicles presence preadult tail; empty- and mature in the ing into tegumental cavity at same point as opening large specimens fish, largest of Laurer'scanal, surroundeddistally by numerous being in fish well offshore, we assume fish compacted cells. normally aid in completing the life history of New host records: Archosargusprobatocephalus the worm and that the worm grows in fish. (Walbaum), sheepshead, Sparidae; Micropogonias Specific fish act as faculative undulatus (Linnaeus), Atlantic croaker, Sciaeni- apparently only dae; Menticirrhusamericanus (Linnaeus), southern hosts for C. occidentalisNickerson 1902. Dick- kingfish, Sciaenidae; Trachinotus carolinus (Lin- erman (1948) was able to establish worms naeus), Florida pompano, Carangidae; T, falcatus from snails in only one of two challenged fish. (Linnaeus), permit, Carangidae. He that worms from snails con- Sites: and reported large Intestine rectum. tained and Wootton Localities: Mississippi and Louisiana. eggs, (1966) presented Specimen deposited: USNM Helm. Coll. No. preliminarydata on infecting bivalves experi- 74462. mentally with larvae hatched from bivalve- worms. However, as pointed out by Cable DISCUSSION (1974), few specimens of C. occidentalis in a of snail studied Siddiqi and Cable (1960) originally de- species by him for more than scribed Cotylogaster basiri on the basis of three 30 years possessed eggs, and no eggs or larvae specimens. Isseroff and Cable (1968) added ever occurred in dishes with isolated snails. a notation on the larva and its eyespots. With Cotylogasterpresently includes four species, our additional specimens we have supple- C. michaelis Monticelli 1892, the type-species, mented the species' description considerably C. occidentalis, C. basiri, and C. barrowi Hueh- as well as extended the ranges for measure- ner and Etges 1972, but Fredericksen (1972) ments and corrected a few minor measure- considered the latter a synonym of C. occiden- ments. Two important corrections to the talis. We found immaturespecimens of another 812 THE JOURNAL OF PARASITOLOGY,VOL. 63, NO. 5, OCTOBER1977

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FIGURES 1-4. Aspidogastridsfrom the Gulf of Mexico; 1, 2. Cotylogaster basiri from Micropogonias undulatus. 1. Whole mount, dorsal view. 2. Terminal genitalia, ventral view. 3. Cotylogaster dinosoides from Pogonias cromis, holotype, ventral view. 4. Multicalyx cristata from Pristis pectinata, marginal organ, lateral view.

filamen- species, and, because they clearly represent a ment lacking. Tegument having dense, anucleated, portion occasionally distinct species and most characters are evi- tous, aspinose over 15 thick; underlain by distinct parenchymal we describe it below. dent, layer supporting groups of nucleated cells or cell portions associated with external layer by ducts; Cotylogaster dinosoides sp. n. parenchymallayer overlying basal lamina followed (Figs. 3, 7) by longitudinal muscle bundles, parenchymal cells, and extensive transversefibers connecting marginal Description (based on 5 immaturewhole mounts, alveoli. Ring of prominent outer longitudinal and 1 subsequently sectioned): Body 2,721 to 3,492 inner circular muscles compartmentalizingalimen- long. Ventral holdfast 2,226 to 2,837 long by 1,104 tary tract and most of terminal genitalia but not to 1,580 wide, occupying ventral surface of entire gonads, extending between midpharyngeal level body excluding neck and posterior extension, pos- and immediately beyond testes where muscles be- sessing one continuous marginal row of 40 to 42 coming diffused. Prepharynxmuscular, variable, 54 cuplike alveoli and medial row of 17 elongate to 128, capable of forming lips, ventral to promi- transverse alveoli; marginal organs distinct on nent transverse commissure of nervous system. alveolar ridges with associated papillae short and Pharynx 263 to 339 long by 216 to 275 wide; inconspicuous;marginal alveoli relatively large near anterior 1%/to 1/4 with dense concentric circular equator of worm compared with progressively muscle fibers; central area of posterior portion smaller ones anteriorly and posteriorly, supplied filled with nucleated cells. Esophagus nonepithe- with glandular cells; posterior extension up to 2% lialized, short and indistinct when contracted. of body length; neck retractile, bearing inconspicu- Cecum a simple epithelialized sac, extending pos- ous flange near base allowing neck to retract, teriorly to between 23 and 30% of body length terminating as simple retractile buccal funnel from posterior end. possessing no lateral lobes but single acutely- Testes 2, postequatorial,usually tandem but oc- pointed retractile dorsal lobe. Eyespots with pig- casionally diagonal, rarely contiguous; anterior HENDRIXAND OVERSTREET-ASPIDOGASTRIDSFROMNORTHERN GULF OF MEXICOFISHES 813

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FIGURES5-8. Cross-sectionsof aspidogastrids; 5, 6. Cotylogaster basiri. 5. Section at pharyngeal level near anterior margin of ventral holdfast; note prominent musculature separating neck from body proper, Heidenhain's iron hematoxylin, X 206. 6. Section at level of prostatic vesicle (next to narrow cecum); note that musculature is less well developed than in Fig. 5 but still easily visible, Heiden- hain's iron hematoxylin, X 173. 7. Cotylogasterdinosoides, alveolus of twisted worm showing marginal organ and peripheral aspect of attached transversemusculature, Heidenhain's iron hematoxylin, X 166. 8. Lobatostoma ringens, section at level of prostatic vesicle; darkly stained organ in middle of worm at margin is testis, Harris' hematoxylin and eosin, X 106. testis 207 to 442 long by 154 to 367 wide; posterior follicles of inverted U-shaped loop dorsal to an- testis at or anterior to termination of cecum, 217 terior testis in one specimen and between anterior to 413 long by 160 to 318 wide. Posttesticular uterine extension of coil and testis in another. space 20 to 28% of body length. Seminal vesicle Excretory system bivesiculate; pore dorsal, sub- sinuous, never extending as far posterior as testes terminal, emptying into thickened tegumental at least in immature specimens; vas deferens join- cavity 8 to 13% of body length from posterior end; ing vasa efferentia about midway between seminal separate vesicles often extending posterior to pore vesicle and testes. Prostatic vesicle elongate, lined before emptying, joining each other immediately internally with membrane-boundanucleate bodies, proximal to pore and adjacent to Laurer's canal, surrounded externally by numerous prostatic cells. with distal portions surroundedby compacted cells; Cirrusand cirrus sac lacking. Ejaculatoryduct rela- anterior paired collecting tubules recurving pos- tively long, sinuous, surroundedby compact clump teriorly anterior and dorsal to transverse nerve of glandular cells. Genital atrium approximatelyas commissure. long as length of underlying alveolus, surrounded Type host: Pogonias cromis (Linnaeus), black by glandular cells. Genital pore approximately drum, Sciaenidae. median, near level of anterior holdfast margin. Site: Intestine. Ovary dextral to and either contiguous with or Locality: Marsh Point in Mississippi Sound, separated from anterior testis, 83 to 210 long by Ocean Springs, Mississippi. 45 to 116 wide. Laurer's canal opening dorsally Holotype: USNM Helm. Coll. No. 74463; para- near posterior of worm. Uterus looping well an- type: No.74464. terior to forward testis and coiled posterior to rear Etymology: The specific name dinosoides, from one; metraterm sinistral to prostatic complex, with the Greek dinos (a drinking bowl) and oides distal portion surrounded by glandular cells. Eggs (resembling), refers to each of the several large not present. Vitellaria anlagen having anterior alveoli. 814 THE JOURNAL OF PARASITOLOGY,VOL. 63, NO. 5, OCTOBER1977

TABLE I. Teleost host for Lobatostoma ringens.

Host Locality Reference

Carrangidae-pompanos Trachinotus carolinus North Carolina Linton, 1905; MacCallum and MacCallum, 1913 East and west coasts of Present study Florida; Alabama; Mississippi; Louisiana Louisiana Sparks, 1958 Veracruz, Mexico Caballero y Caballero and Bravo Hollis, 1966 Trachinotus falcatus West coast of Florida Present study Sciaenidae-drums Menticirrhus americanus Mississippi Present study Micropogonias furnieri Jamaica Nahhas and Cable, 1964 Micropogonias opercularis Argentina Suriano, 1966 Micropogonias undulatus North Carolina Linton, 1905; Diaz and Johnson, 1974; Present study Mississippi; Louisiana; Present study Georgia

Sparidae-porgies Calamus bajonado Florida Manter, 1947 Bimini Sogandares-Bemal, 1959 Calamus calamus Florida Manter, 1947 Stenostomus chrysops Bermuda Rees, 1970

Ephippidae-spadefishes Chaetodipterus faber Florida MacCallum, 1921 Labridae-wrasses Halichoeres radiatus Bermuda Linton, 1907

Pleuronectidae-righteye flounders Oncopterus darwini Puerto de Quequen, Szidat, 1961 Argentina

Exocoetidae--halfbeaks Hyporhamphus roberti Veracruz, Mexico Caballero y Caballero and Bravo Hollis, 1966

Pomatomidae-bluefishes Pomatomous saltatrix Bermuda Hanson, 1950

DISCUSSION dinosoides because the preadult and short adult, as well as the larva, have conspicuous Cotylogaster dinosoides can be separated eyespots and because its gonads occur in from all other members of the genus by its rel- the cylindrical muscular compartment. Cotylo- atively large equatorial marginal alveoli in gaster occidentalis, a freshwater species, has comparison to those alveoli at the anterior and been reported from the freshwater drum in posterior of the holdfast. It also possesses ex- nearby Lake Pontchartrain in Louisiana (So- tensive transverse musculature connecting op- gandares-Bernal, 1955), which is brackish in posing lateral alveoli (Fig. 7), allowing a areas; the elongated adult possesses 79 to 273 cylindrical aspect of the living worm, nearly marginal alveoli, but even when fewer alveoli as well as a buccal funnel without simple occur in immature specimens, alveoli are all lateral lobes. The Mediterranean species, C. similar in size. michaelis, appears to be most similar. It differs Lobatostoma (Linton 1907) further from C. dinosoides by having vitelline ringens (Fig. 8) follicles that extend anteriorly near the anterior Teleost hosts and their localities: See Table I. The C. margin of the holdfast. sympatric New molluscan host: Donax roemeri protracta basiri can be easily differentiated from C. Conrad, coquina. HENDRIXAND OVERSTREET-ASPIDOGASTRIDSFROMNORTHERN GULF OF MEXICOFISHES 815

Localities of clam: Horn Island, Mississippi; clam's identity is actually D. roemeri roemeri Alabama Point, Baldwin County, Alabama. Philippi. USNM Helm. Coll. Specimens deposited: Nos. Rohde found no of L. 74465-74466. (1973) specimens manteri with eggs in snails. He was unable, DISCUSSION except for limited doubtful success, to infect a sea turtle or fishes other than Trachinotus Lobatostoma ringens has been reported more blochi (Lacepede) with adult or preadult speci- often than any other marine aspidogastrid. mens. That fish, related to the pompanos host- Table I lists those records as well as our find- ing L. ringens, L. kemostoma (MacCallum and ings. The worm has been adequately described MacCallum 1913), and L. pacificum Manter for most features, most recently by Caballero y 1940, presumably represents the primary verte- Caballero and Bravo Hollis (1966). Its range brate host of the two-host cycle. According to extends from at least North Carolina to Argen- Szidat (1970), an immature specimen of L. tina. pacificum infected a snail from freshwater in Some of the musculature of L. ringens and Rio de la Plata, Argentina. of species of Cotylogaster show similarities and differences. A thick cylindrical ring extends to Multicalyx cristata (Faust and Tang 1936) near the worm's posterior end and encircles the (Fig. 4) tract and terminal but not alimentary genitalia, New host records: Pristis pectinata Latham, the gonads (Fig. 8). This feature is thinner smalltooth sawfish, Pristidae; Dasyatis sayi (Le- and not cylindrical in cross-sections of L. man- seur) bluntnose stingray, Dasyatidae; Cephaloscyl- lium ventriosum teri Rohde 1973 illustrated by Rohde (Garman), swell shark, Scylio- (1973) rhinidae. and Rohde and Sandland (1973). Rather than Site: Bile ducts. having dense fibers traversing the dorsal por- Localities: Off Mississippi in Gulf of Mexico tion of the body as in Cotylogaster dinosoides, and Santa Barbara,California. L. ringens possesses a dense concentration of Specimens deposited: USNM Helm. Coll. No. 74467 attached fibers along most of the dorsal mid- (2 slides). line. These attached rather than con- fibers, DISCUSSION spicuously extending to the marginal alveoli as the unattached transverse ones do in C. dino- Our specimens, 28 to 101 mm in length, soides, spread out with the majority attaching compare favorably with descriptions and sup- along the lateral portions of the medial alveoli. plemental data (Faust and Tang, 1936; Doll- The groups of cells which in C. dinosoides pri- fus, 1958a, b; Stunkard, 1962). Additionally, marily occur confined to a parenchymal layer they possess marginal organs like other aspido- subjacent to the anucleate tegument exist, but gastrids (Fig. 4). These organs associate with not in such a band and often ventral to the short broad papillae on lateral ridges between transverse muscle fibers. Anterior concentric individual alveoli and extend from the anterior circular muscles of the pharynx occur just as in alveolus to those preceding incompletely de- L. manteri and the two species of Cotylogaster veloped alveoli near the posterior end; they described here. also occur in the holotype. Lobatostoma ringens probably requires a Extremely striking in appearance, living teleost to complete its life cycle. Preadult and worms have reddish alveoli contrasting with a small adult specimens occurred frequently in pale yellow body proper. Even though we Florida pompano feeding on the clam Donax found the worms residing in the bile duct, roemeri protracta. An immature specimen oc- conspicuously operculated eggs 116 to 128 long curred in 1 of 865 clams examined from Missis- by 73 to 78 wide with well-developed typical aspidogastrid larvae occurred attached to the sippi and another in 1 of 50 from Alabama. epithelium of the gall bladder. Stunkard and Both locations consist of high-energy, high- Dollfus both cited the gall bladder as the loca- salinity beaches bordering the Gulf of Mexico. tion of adults in their reports. Faust and Tang Lobatostoma Hopkins (1958) reported sp. (1936) originally described it from a single from D. variabilis in and Texas, Sparks (1960) worm listed from the spiral valve, but we agree considered that worm to be L. ringens. The with Stunkard (1962) in questioning that site. 816 THE JOURNAL OF PARASITOLOGY,VOL. 63, NO. 5, OCTOBER1977

All three hosts that we report representnew ACKNOWLEDGMENTS records. The of M. cristata in presence Ceph- We are grateful to F. G. Hochberg, Jr., ventriosum from Santa Barbara, aloscyllium Charles E. Brown, John H. Finucane, Tom California, extends the range to the Pacific Mattis, and Marine Life, Inc. of Gulfport, Mis- Ocean. Stunkard (1962) stated, "Dr. Laurie sissippi, for donating or loaning aspidogastrids reported (in littoris) that according to Dr. or unexamined hosts. Lichtenfels al- James E. Lynch, 'Macraspisis fairly abundant Ralph in the ratfish (Hydrologus colliei) in Puget lowed us to examine material from the Belts- Sound.'" Examination of Lynch's specimens ville Parasitological Laboratory of the U.S. in the U.S. National Museum,however, reveals National Museum, and Ronnie G. Palmer, Ed- them to be Taeniocotyleelegans (Olsson 1869). ward C. Whatley, Jr., and Ann St. Andrie pro- Previously, Faust and Tang (1936) reported vided technical assistance. M. cristatafrom Rhinopterabonasus (Mitchill) (= R. quadriloba) in Mississippi; Stunkard LITERATURECITED (1962) reported it from Dasyatis centroura Y AND BRAVO in Massachusetts; and Dollfus CABALLERO CABALLERO, E., M. (Mitchill) HOLLIS.1966. TrematodaRudolphi, 1808 de (1958a) reported it from Mustelus canis peces marinos del litoral mexicano del Golfo (Mitchill), Rhizoprionodon(= Scoliodon) ter- de Mexico y del Mar Caribe. I. Rev Biol raenovae (Richardson), and Rhinobatoscemi- Trop 13: 297-301. R. M. 1974. and of culus Hilaire) in Senegal, in western CABLE, Phylogeny taxonomy (St. trematodes with reference to marine species. Africa. In W. B. Vernberg (ed.), Symbiosis in the We encountered immature aspidogastrids Sea. University of South Carolina Press, Co- from the gall bladder of the checkered puffer, lumbia, South Carolina, p. 173-193. Sphoeroides testudineus (Linnaeus) (in Bis- DIAZ, A., AND C. A. JOHNSON, III. 1974. The and from the intestine of effect of season and salinity on the distribution cayne Bay, Florida), of parasites of estuarine fishes from North Menticirrhus americanus (off Horn Island, Carolina. ASB Bull 21: 15. Mississippi) (deposited as USNM Helm. Coll. DICKERMAN, E. E. 1948. On the life cycle and Nos. 74468-74469) that are most likely M. systematic position of the aspidogastridtrema- cristata. Manter also an im- tode, Cotylogaster occidentalis Nickerson, (1931) reported 1902. Parasitol34: 164. mature from the intestine of M. J aspidogastrid DOLLFUS, R. PH. 1958a. Sur Macraspis cristata americanus,but consideredit as possibly Taen- (E.-C. Faust et C.-C Tang 1936) H.-W. Man- iocotyle (= Macraspis) elegans. Whether our ter 1936 et sur une emendation necessaire a specimens are immature M. cristata and ma definition de la famille des Aspidogastridae accidentalor trans- (Trematoda). Ann Parasitol Hum Comp 33: whether the fishes represent 227-231. fer hosts remain uncertain. Most of the diverse 1958b. Cours d'helminthologie. I.- elasmobranchhosts, however, do feed on tele- Trematodes sous-classe Aspidogastrea. Ann osts. Parasitol Hum Comp 33: 305-395. Some nomenclatural have involved FAUST, E. C., AND C.-C. TANG. 1936. Notes on problems with a considera- Faust and erected new aspidogastrid species, M. cristata. Tang (1936) tion of the phylogeny of the group. Parasitol- Multicalyxas a subgenus of Stichocotyle Cun- ogy 28: 487-501. ningham 1884 when describing the species. FREDERICKSEN, D. W. 1972. Morphology and Since the usually had been con- taxonomyof Cotylogasteroccidentalis (Trema- then, species 1110- cristata Manter's toda: Aspidogastridae). J Parasitol 58: sidered Macraspis following 1116. (1954) transfer,until Stunkard(1962) pointed HANSON, M. L. 1950. Some digenetic trematodes out that Macraspis Olsson 1869 was preoccu- of marine fishes of Bermuda. Proc Helmin- Macraspis MacLeay 1819, an insect, thol Soc Wash 17: 74-89. pied by of and resurrected with M. cristata as HOPKINS, S. H. 1958. Trematode parasites Multicalyx Donax variabilis at Mustang Island, Texas. the type species; he created Taeniocotyle for Publ Inst Mar Sci, Univ Tex 5: 301-311. M. elegans, which he considered generically ISSEROFF,H., AND R. M. CABLE. 1968. Fine of in larval trema- different. Both species probablybelong to the structure photoreceptors todes. A comparative study. Z Zellforsch same genus, but that problem will not be MikroskAnat 86: 511-534. treated here. LINTON, E. 1905. Parasites of fishes of Beaufort, HENDRIXAND OVERSTREET-ASPIDOGASTRIDSFROMNORTHERN GULF OF MEXICOFISHES 817

North Carolina. Bull U S Fish Comm (1904) Rico. Sci Surv Porto Rico and Virgin Islands 24: 321-428. 17: 257-369. .1907. Notes on parasites of Bermuda SOGANDARES-BERNAL, F. 1955. Some helminth fishes. Proc U S Nat Mus 33: 85-126. parasites of fresh and brackish water fishes MACCALLUM, G. A. 1921. Studies in helmin- from Louisiana and Panama. J Parasitol 41: thology. Part 1. Trematodes. Part 2. Ces- 587-594. todes. Part 3. Nematodes. Zoopathologica1: .1959. Digenetic trematodes of marine 135-284. fishes from the Gulf of Panama and Bimini, ,AND W. G. MACCALLUM. 1913. On British West Indies. Tulane Stud Zool Bot 7: Aspidogaster ringens (Linton) and A. kemo- 71-117. stoma n. sp. Zool Jahrb Abt Syst Oekl Geogr SPARKS,A. K. 1958. Some digenetic trematodes Tiere, Jena 34: 245-256. of fishes of Grand Isle, Louisiana. Proc La MANTER, H. W. 1931. Some digenetic trema- Acad Sci 20: 71-82. todes of marine fishes of Beaufort, North Caro- 1960. Some aspects of the zoogeography lina. Parasitology23: 396-411. of the digenetic trematodes of shallow-water 1947. The digenetic trematodes of fishes of the Gulf of Mexico. Lib Hom E. marine fishes of Tortugas, Florida. Am Midl Caballeroy C.: 285-298. Nat 38: 257-416. STUNKARD,H. W. 1962. Taeniocoytle nom. nov. 1954. Some digenetic trematodes from for Macraspis Olsson, 1869, preoccupied, and fishes of New Zealand. Trans R Soc N Z systematic position of the Aspidobothrea. Biol 82: 475-568. Bull 122: 137-148. NAHHAS, F. M., AND R. M. CABLE. 1964. Dige- SURIANO, D. M. 1966. Estudio de la fauna para- netic and aspidogastrid trematodes from sitaria de Micropogon opercularis en relacion marine fishes of Curacao and Jamaica. Tulane con problemas zoogeograficos del Atlantico Stud Zool Bot 11: 169-228. Sur. Parasitologia1: 31-47. REES, G. 1970. Some helminth parasites of fishes SZIDAT, L. 1961. Versuch einer Zoogeographie of Bermuda and an account of the attachment des Sud-Atlantik mit Hilfe von Leitparasiten organ of Alcicornis carangis MacCallum, 1917 der Meeresfische. Parasitol Schriftenr 13: (Digenea: Bucephalidae). Parasitology 60: 1-98. 195-221. .1970. [Further studies on the marine ROHDE, K. 1973. Structure and development of relict fauna of the Plate River system.] In K. Lobatostoma manteri sp. nov. (Trematoda: S. Singh and B. K. Tandan (eds.), H. D. Aspidogastrea) from the Great Barrier Reef, Srivastava Commemoration Volume. Indian Australia. Parasitology 66: 63-83. VeterinaryResearch Institute, Izatnagar,U. P., , AND R. SANDLAND. 1973. Host-parasite p. 637-653. relations in Lobatostoma manteri Rohde WOOTTON,D. M. 1966. The cotylocidium larva (Trematoda: Aspidogastrea). Z Parasitenkd of Cotylogasteroides occidentalis (Nickerson, 42: 115-136. 1902) Yamaguti 1963 (Aspidogasteridae As- SIDDIQI,A. H., AND R. M. CABLE. 1960. Dige- pidocotylea Trematoda). Proc 1st Int Congr netic trematodes of marine fishes of Puerto Parasitol 1964: 547-548.