MSP TechRep 97-4 Digenetic trematodes of marine fishes from Suva%2C Fiji :: The University of the South Pacific Library

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rine Sttufies

The University of the Soulh Pacific

Technical Report

DIGENETIC TREMATODES OF MARINE FISHES

FROM SUVA, FIJI. FAMILY HAPLOSPLANCHNIDAE

POCHE, 1926: DESCRIPTION OF NEW SPECIES,

A REVIEW AND AN UPDATE.

by

Fuad M. Nahhas

Dolores Y Rhodes

Johnson Seeto

Series

Number

ISSN 1018-2896

97/4

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DIGENETIC TREMATODES OF MARINE FISHES FROM

SUVA, FIJI. FAMILY HAPLOSPLANCHNIDAE POCHE,

1926: DESCRIPTION OF NEW SPECIES,

A REVIEW AND AN UPDATE.

by

Fuad M. Nahhas1, Dolores Y. Rhodes1,

and Johnson Seeto2

1Department of Biological Sciences,

University of the Pacific

Stockton, CA 9521 1 , USA

2Marine Studies Programem,

The University of the South Pacific

Suva, Republic of Fiji

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TABLE OF CONTENTS

I. ABSTRACT .

.

iii

.

II. ACI<.NOWLE])CJrvfENTS . ................................ iv

III. INTRO])UCTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1

IV. HISTORICAL REVIEW . . ·. . . ............................. 2

V. LIFE CYCLE ........ . ............................... 5

VI. rvtATERIALS AN]) rvtETHO])S .. . . . . , ..................... 6

VII. ])ESCRIPTION AN]) ])ISCUSSION OF THE SPECIES ............ 7

Part I - Haplosplnchnids of Fij i

1. Haplosplanchnus pachysomus ( Eysenhardt,1829) L ooss, 1902

7

2.H. purii Srivastava, 1939

16

3. Schikhobalotrema southi n. sp.

21

. 4. Schikhobalotrema sp. #1

22

5. Schikhobalotrema sp. #2

23

6. Hymenocotta mulli rvt anter, 1961

24

PART II - H aplospl anch nids of Other Parts of the W orld

7. Haplosplanchnus mugilis N ahhas and C able, 1964

25

8.H. venezuelensis Fisc hthal and N asir, 1974

26

9. H. bengalensis Ciupta and Puri, 1985

26

10. H vinodtie Ahinad, 1985

27

11. Schikhobalotrema acutum ( Linton, 1910) Skrj. and Ciusc h.,1955

28

12. S. obtusum ( Linton, 1910) Skrj.and Ciusc h., 1955

29

13. S. adacutum ( rvt anter, 1937) Skrj.and Ciusc h., 1955

30

14. S. brackyurum ( rvf anter, 1937) Skrj. and Ciusc h., 1955

31

15. S. pomacentri ( rvf anter, 1937) Skr.j and Ciusc h., 1955

31

16. S. sparisomae ( rvf anter, 1937) Skrj. and Ciusc h., 1955

32

17. S. kyphosi ( rvf anter, 1947) Skr.j and Ciusc h., 1955

33

18. S. girellae ( rvt anter and V an C leave, 1951) Skrj.and Ciusc h., 1955 34

19. S. adbrachyurum Siddiqi and Cable, 1960

34

20. S. manteri Siddiqi and C able, 1960

35

21. S. crassum Pritch ard and rvt anter, 1961

35

22. S. glomerosum Pritchard and rvt ant er, 1961

36

23. S. hawaiiensis Pritchard and rvt anter, 1961

36

24. S. robustum Pritchard and rvt anter, 1961

37

25. S. bivesiculum Nahahs and Cable, 1964

38

26. S. elongatum Nahsha and C able, 1964

39

27. S. acanthuri Yamagut i, 1970

40

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28. S. longivesiculatum Orecchia and Paggi, 1975

40

29. S. magnum Skinner, 1975

41

30. S. solitaria Fernandes and Goulart, 1989

42

3 1 . Pseudoschikhobalotrema heterocotylum (Nahhas and Cable, 1964)

Yamaguti, 197 1

42

32. Haplosplanchnoides hemiramphi Nahhas and Cable, 1964

43

33 . Hymenocotta manteri Overstreet, 1969

43

34 Prohaplosplanchnus diorchis Tang and Lin, 1978

44

35 . Provitellotrema crenimugilis Pan, 1984

45

36. Neohaplosplanchnus ablennis Abdul-Salam and Khalil, 1987

45

37 . Discocephalotrema kyphosi Machida, 1993

47

38. Parahaplosplanchnus cirrusaci (Lu, 1995)

48

VIII. DISCUSSION

50

IX. APPENDIX

1 . Key to the Subfamilies of Haplosplanchnidae

54

2. Key to the Genera of Haplosplanchnidae

55

3. Key to the Species of Haplosplanchnus

56

4. Key to the Species of Schikhobalotrema

57

X. TABLE 1 . Egg sire of Haplosplanchnus pachysomus-

H. caudatus complex

ro

XI. PLATES I-X

61

XII. LITERATURE CITED

81

EDITORIAL COMMITTEE FOR THIS PAPER:

R. A. Bray, Department of Zoology, The Natural .History Museum,

Cromwell Road, London, SW7 5BD, UK.

T. H. Cribb, Department of Parasitology, University of Queensland,

Brisbane, Q. 4072, Australia

ii

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I. ABSTRACT

Six species of haplosplanchnids are reported in this study: Haplosplanchnus

pachysomus (Eysenhardt, 1829) Looss, 1902 was found in 8 of 9 (89%) Mugil

cephalus, and H. purii Srivastava, 1939 in 1 of 8 (12. 5%) Liza vaigiensis and 1 of 9

(11%) M. cephalus; both findings represent a new locality record; Schiklwbalotrema

southi n.sp. is described from a single specimen from Scarus rivulatus. Two species

of Schiklwbalotrema are also reported but not named; Schikhobalotrema sp.# 1 from

S. rivulatus and Schikhobalotrema sp.# 2 from Acanthurus xanthopterus are described,

figured, but not named because of either damage to �e specimen or insufficient data.

Hymenocotta mulli Manter, 1961 from Mugil cephalus and Liza vaigiensis is also

reported, based on one specimen from each host (11% and 12.5% respectively).

Hop/osplanchnus caudatus (Srivastava,1939), H. straightum (Jehan,1973),H. orientalis

Gupta and Ahmad, 1979, H. stunkardi Gupta and Ahmad, 1979 and H. guptai Gupta

and. Ahmad, 1985 are considered conspecific with H. pachysomus, and H. otolithi

Gupta and Ahmad, 1979 with H. purii. Brief information on all other haplosplanchnid

species reported to date is included. Neohaplosplanchnus Lu (1995) nee Abdul-Salam

and Khalil (1987) is renamed Parahap/osplanchnus. The family Haplosplanchnidae and

its subfamilies are redefined; keys to its subfamilies, genera, and to species of

Haplosplanchnus and Schikhobalotrema are included.

Key words: Digenetic trematodes, Haplosplanchnidae, Haplosplanchnus

pachysomus, H. purii, Schiklwbalotrema southi, Schikhobalotrema sp. l,

Schikhobalotrema sp.2, Hymenocotta mulli,Parahaplosplanchnus, parasites, Mugil

cepha/.us, lil.ll vaigiensis, Sparisoma rivulatus, AcanthulUS xanthopterus,marine fishes,

Fiji.

iii

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II. ACKNOWLEDGMENTS

The authors are thankful to the faculty and staff of the Marine Studies

Programme (formerly Institute of Marine Resources), The University of the South

Pacific, Suva, Republic of Fiji for their assistance. Special thanks are extended to

Professor G. Robin South, Professor of Marine Studies, for making the facilities

available to the senior author to conduct this study, and Professor Rodney A. Bray of

the British Museum of Natural History, London, England, for examination of some of

the specimens, and supplying us with some literature. Professors Bray and T. H. Cribb

of the University of Queensland also served as reviewers of the manuscript; for their

valuable comments we are grateful. We thank Dr. J . Ralph Lichtenfels, Biosysternatic

Parasitology Laboratory, United States Department of Agriculture, Beltsville,

Maryland, and Professor Mary Hanson Pritchard and Dr. M. Sterner of the University

of Nebraska, Lincoln, for the loan of specimens. We also thank Christina Ninalga,

Ambre Parrish, Enjoli Gayle and Bounthavong Rasaphangthong for their assistance in

the preparation of this manuscript. The partial financial assistance of California Cedars

Products, the University of the Pacific Research Committee and the Francis R. Hunter

Fund is also gratefully acknowledged.

iv

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Ill. INTRODUCTION

The present paper, the third in a series (see Amin and Nahhas, 1994; Nahhas

and Wetzel, 1995) is, in part, a report of six species of haplosplanchnids, family

Haplosplanchnidae Poche, 1926, collected by the senior author between 13 January and

7 February 1992 while on sabbatical leave at the Marine Studies Programem , The

University of the South Pacific, Suva, Republic of Fiji. The Fijian species are

described in Part I of this article. Part II is a review and an update with pertinent data

on all haplosplanchnid species described to date including brief and relevant remarks.

Not included are various reports of . undescribed Haplosplanchnus and

Schikhobalotrema spp.

Two previous collections of parasites of marine fishes from the Fiji Islands have

been made, the first by Manter in 1951 (see Manter 1953, 1961, 1963a, 1963b, 1963c;

Manter and Prince, 1953), and the second, between 1979 and 1982, by the Hatsutori

Maru and other fishing boats on charter to the government of New Zealand (see Lester

et al., 1985). Manter (1961) reported one species of haplosplanchnid, Hymenocoua

mulli1 from an unidentified mullet (Mugilidae).

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IV. HISTORICAL REVIEW

The family Haplosplanchnidae, one of the smallest families of digenetic

trematodes, was established by Poche in 1926 to accommodate Haplosplanchnus

pachysomus (Eysenhardt, 1829) Loso s, 1902, a species characterized by a single cecum

and a single testis.

..

•

In 1910, Linton described Deradena acuta from Tylosurus marinus, D. obtusa

from Acanthurus coeruleus and Paracanthurus (Acanthurus) hepatus, and D. ovalis

from Scarus coeruleus and S. croicensis. Linton (1910) recognized a superficial

resemblance to Haplosplanchnus Looss, but noted that the vitellaria are diffuse instead

of dendritic. Manter (1931: 386) added that

"... the genus Deradena possesses a single cecum and is

therefore very similar to Haplosplanchnus Looss."

Further study by Manter (1937) led to the transfer of D. acuta and D. obtusa

to the genus Haplosplanchnus . Manter also recognized a similarity between D. ovalis

and Hapladena varia Linton, 1910 which led him to consider the former a synonym

of the latter. Manter (1937: 381) also noted

"... some constant differences between all the Tortugas

forms (H. acuta and H. obtusa) and H. pachysomus

(Eysenhardt), the type. The vitellaria are much more

extensive especially posteriorly. the prostatic cells much

less developed (unless Loso s interpreted the "neck

gland" of Linton as prostatic cells), the eggs are

definitely larger and the cecum at least somewhat

longer."

He considered these as specific rather than generic differences, redescribed H.

acutum and H. obtusum and added four new species: H. sparisomae, H. brachyurum,

H. pomacentri, and H. adacutum from various herbivorous species of fish from

Tortugas, Florida.

Srivastava (1939) described 2 new haplosplanchnids, Laruea caudatum from

Mugil (li.a)i vaigiensis from Puri, Bay of Bengal and Haplosplanchnus purii from the

same host species and locality and from Karachi, Arabian Sea. Laruea was

distinguished from Haplosplanchnus by its body shape (plump, roughly Y-shaped,

semi-spiral posterior end), the ventral sucker (long, club-shaped, tubular, more

muscular), and the position of the gonads (more anterior, just below mid-level rather

than posterior).

Manter (1947) described H. kyphosi from Kyphosus sectatrix and K. incisor

from Tortugas, Florida, and Manter and Van Cleave (19Sl) added H. girellae from

Girella nigricans from La Jolla, California.

2

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Skrjabin and Guschanskaja (1955) disagreed with Manter (1937) and considered

the differences, cited above, between the American species of Haplosplanchnus and H.

pachysomus to be significant enough to justify a new genus which they named

Schikhobalotrema and to which all the American species of Haplosplanchnus were

transferred. Skrjabin and Guschanskaja (1955) also did not recognire the genus Laruea

which they considered a synonym of Haplosplanchnus. They created two subfamilies,

Haplosplanchninae and Schikhobalotrematinae to accommodate Haplosplanchnus and

Schikhobalotrema respectively. Sogandares-Bemal and Sogandares ( 1 961) recognired

Schikhobalotrema as a subgenus of Haplosplanchnus.

S.

odbraScihdyduiqriuamndfrComabSlepa(r1i9s6o0m)aadsdpe. datnwdoSn. emwasnpteecriie·f�rotomthae

genus Schikhobalotrema:

"reef fish with a collar".

Pritchard and Manter (1961) added four- more: S. crassum from Stegastes fasciolatus

( = · Pomacentrus jenkenst), S. glomerosum from Acanthurus achilles and A.

sandvicensis, S. hawaiiensis from Ctenochaetus strigosus, and S. robustum from

Stegastes fasciolatus (=Pomacentrus jenkinsi), Acanthurus sandvicensis, Chaetodon

frembii and 7-ebrasoma flavescens. Manter ( 1 961) described a new genus,

Hym�npcotta, to accommodate H. multi from an unidentified mullet (family

Mugilidae). Nahash and Cable (1964) described Schkikhobalotrema bivesiculum from

Abudefduf saxatilis, S. elongatum from Mugil cephalus and M. curema, and S.

heterocotylum from Pseudoscarus guacamaia. They also reported the first species of

Haplosplanchnus from the Caribbean which they named H. mugilis from M. curema,

and described an amphistomatous haplosplanchnid from Hemiramphus brasiliensis

which they called Haplosplanchnoides hemiramphi. Overstreet ( 1969) added a second

species to the genus Hymenocotta, H. manteri, from M. cephalus from Biscayne Bay,

Florida. Yamaguti ( 1 970) described Schikhobalotrema acanthuri from Acanthurus

sandvicensis, A. nigrofuscus, and 7-ebrasoma flavescens.

Yamaguti ( 1 97 1 ) revised the family recognizing the genus Haplosplanchnus

with 3 species and Schikhobalotrema with 17. He rejected Skrjabin and Guschanskaja's

synonymy of Laruea with Haplosplanchnus. He also transferred Schikhobalotrema

heterocotylum Nahhas and Cable, 1964 to a new genus Pseudoschikhobalotrema, and

Hymenocotta manteri Overstreet, 1 969 to Hymenocottoides.

Zhukov (1971 ) described Haplosplanchnus bivitellosus from Mugil cephalus and

M. soiuy from the basins of the Japan and Yellow Seas. In 1973, Jehan described

Laruea straightum from Pseudosciaena diacanthus and Rachycentron canadus.

Fischthal and Nasir ( 1974) added H. venezuelensis from Antennarius multiocellatus

from Los Roques Islands, Venezuela. Orecchia and Paggi ( 1 975) described

Schikhobalotrema longivesiculatum from Blennius sanguinolentus from the Gulf of

Gaeta, Italy. Skinner ( 1 975) added S. magnum from M. cephalus from Biscayne Bay,

Florida. Tang and Lin ( 1978) described Haplosplanchnus cuneatus and H. elongatus

from M. cephalus, and Prohaplosplanchnus diorchis from Liza haematochilus and M.

cephalus all from the Min River, Fujian, China. Gupta and Ahmad (1979) described

Haplosplanchnus indicus from M. vaigiensis, H. orientalis from llisha elongata

( =Pellona elongata), H. otolithi from Otolithus ruber, and H. stunkardi from

3

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Acanthurus sandvicensis all from the Bay of Bengal, at Puri, Orissa. Pan (1984) added

a new genus and species Provitellotrema crenimugilis from Crenimugil crenilabis.

Ahmad (1985) described Haplosplanchnus guptai and H. vinodae from M. cephalus

from the Panjim Coast, Goa, India. Gupta and Puri (1985) described H. bengalensis

from Acanthurus sandvicensis from the Bay of Bengal, at Puri , Orissa. Abdul-Salam

and Khalil (1987) added a new genus and species, Neohaplosplanchnus ablennis, from

Ablennes hians from the Kuwaiti coast, Arabian (Persian) Gulf. Fernandes and

Goulart(1989) described Schikhobalotrema solitaria from Stephanolepis hispidus from

Praia de Copacabana, Rio de Janeiro; Machida (1993) added a new genus

Discocephalotrema to accommodate D. kyphosi from Kyphosus cinerascens and created

for it a new subfamily Discocephalotrematinae; Lu (1995), unaware of the description

of Nephaplo-splanchnus ablennis Abdul-Salam and Khalil, 1987 from Kuwait, used the

same generic name as a new genus to accommodate N. cirrusaci from Engraulis

japonica from Shallow Sea, Guandong Province, China.

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V. LIFE CYCLE

Two life cycles have been described in the family Haplosplanchnidae Poche,

1926. Cable (1954) described a partial life cycle involving sporocyst stages within the

marine snail Cerithium variable (Gastropoda, Cerithiidae), the development of the

cercariae within the snail and their encystment on vegetation in water as metacercariae.

Whether the haplosplanchnid egg is eaten by the snail or hatches in water and later

penetrates the snail intermediate host was not determined. A redial stage is apparently

absent. Cable (1954) suggested that these developmental stages were most likely the

larval forms of Schikhobalotrema acutum (Linfon, 1910) Skrjabin and Guschanskaja,

1955, the most common haplosplanchnid in Caribbean and adjacent waters.

Fares and Maillard (1975) d.escribed the life cycle of Haplosplanchnus

pachysomus (Eysenhardt, 1829) Looss, 1902. They had found natural infections in Liza

auratus, L. ramada, Mugil cephalus and Chelon labrosus, and haplosplanchnid

cercariae emerging from naturally infected Hydrobia ventrosa (Gastropoda:

Hydrobiidae) in littoral waters of Languedoc-Roussillon, French Mediterranean coast.

Fares and Maillard used laboratory-raised H. ventrosa snails, and mullets that had bene

collected at a young age and kept in aquaria, to demonstrate a complete life cycle.

Their experiments showed that ciliated miracidia, which had emerged from the uterus

of adult H. pachysomus, penetrate the snails, develop in the gonads into sporocysts

which give rise to rediae which, in tum, produce cercariae. The phototropic cercariae

swim to the surface and encyst as metacercariae in the surrounding environment (milieu

ambient). Only 4-5 day old metacercariae were infective, which when eaten by mullets,

develop into adults in the anterior part of the intestine of the fish. Fares and Maillard

(1975) also gave a detailed description of the anatomy of the adult.

Recently Abdul-Salam and Sreelatha (1995) described Cercaria kuwaitae VI,

y a new haplosplanchnid cercaria which develops in sporocysts in Cerithidea cingulata.

The onl known adult haplosplanchnid from the Arabian Gulf is Neohaplosplanchnus

ablennz's Abdul-Salam and Khalil, 1987.

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VI. MATERIALS AND METHODS

A total of 236 fishes were obtained from several sources in Laucala Bay, Suva

including traps, nets, spear fishing, and commercial fishermen. Except for a few fishes

that were purchased, all were captured live on reefs and lagoons of Laucala Bay, Suva,

a few miles from the laboratory of the Marine Studies Programme (formerly Institute

of Marine Resources). Fifty species, representing 32 genera and 20 families were

collected. Four species: Acanthurus xan thop terus (Acanthuridae), Li za vaigiensis and

Mugil cephalus (Mugilidae), and Scarus rivulatus (Scaridae), harbored

haplosplanchnids. The fish were kept alive in tanks until shortly before examination.

After removal from the host, the digeneans were washed in 0.7% saline, many studied

alive before they were fixed with alcohol-formalin-acetic acid (A.F.A.) under slight

coverslip pressure. The worms were then transferred to a dish, left in the fixative

overnight, then stored in 70% ethanol. After washing with three changes of 50%

isopropanol, the specimens were stained with Semichon's acetocarmine (Carolina

Biological Supply Company), destained in 0.5% acid alcohol, dehydrated in ascending

series of isopropanol, cleared in methyl salicylate, rinsed in xylol, and mounted in

Kleermount (Carolina Biological Supply Company).

Measurements are expressed in millimeters except for eggs which are in

micrometers (µm). Sucker ratio was calculated from the mean of the length (depth) and

width and is expressed with the oral sucker taken as 1. Drawings of specimens obtained

in this study were prepared by microprojection and details filled in through microscopic

observations. Drawings of other species were made by tracing original diagrams. One

asterisk* indicates a new synonym. The number of specimens recovered from each

infected fish and the number of fish examined are indicated next to each host species

listed in the description of the Fijian species. Discussions or remarks, where necessary,

are also presented with each species.

Holotypes are deposited in the Parasite Collection of the United States National

Parasite Collection (USNPC), Beltsville, Maryland; voucher specimens of some species

are in the British Museum of Natural History, BM(NH), London, and Harold W .

Manter Laboratory (HWML), University of N ebraska State Museum, Lincoln. Fishes

were identified by the third author, Johnson Seeto. References used included an

unpublished manuscript on fishes of the Fiji Islands, Nelson ( 1984), Myers ( 1989), and

Randall et al. (1990).

6

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VII. DESCRIPTION AND DISCUSSION OF THE FIJIAN SPECIES

Part I - Haplosplnchnids of Fiji

GENUS HAPLOSPLANCHNUS Looss, 1902

To date 16 species of Haplosplanchnus have been reponed; four of these are

listed in Yamaguti ( 197 1): H. pachysomus (Eysenhardt, 1829) Looss, 1902, H.

caudatus (Srivastava, 1939) listed as Laruea caudatum, H. purii Srivastava, 1939 , and

H. mugilis Nahhas and Cable, 1964 . Twelve others were described after 197 1 , and are

b19ri7e3t1)yAdhismcuasds,ed19i8n5t,hHis .pvaepneer:zuHel.ebnisvisiteFliloscshutsh· aZlhaunkdo.vN, a1s9ir7,

1, H.

1974,

straightum (Jehan,

H. cuneatus Tang

and Lin, 1978, H. elongatus Tang and Lin, 1978, H. indicus Gupta and Ahmad, 1979 ,

H. orientalis Gupta and Ahtnad, 1979, H. otolithi Gupta and Ahtnad, 1979, H.

stunkardi Gupta and Ahmad, 1979 , ii. bengalensis Gupta and Puri, 1985, H. guptai

Ahmad, 1985, and H. vinodae Ahmad, 1985 .

There seems to be a correlation between the presence or absence of muscular

acetabtilar lips, the ratio of the oral sucker to the ventral sucker, and the length-width

ratio of the ventral sucker. The 16 species of HaplosjJlanchnus can be separated into

two groups. Group 1 is characteriz.ed by the presence of muscular acetabular lips, a

. ventral sucker at least twice the oral sucker and its length at least twice its width. Six

species are included in this group: H. pachysomus, H. caudatus, H. straigh tum, H.

orientalis , H. stunkardi, and H. guptai. Group 2 is characteriz.ed by absence of

muscular acetabular lips, a sucker ratio of 1 :2 or less, and ventral sucker length not

much greater than its width. This group consists of 10 species: H. purii, H. mugilis,

H. bivitellosus, H. venezuelensis, H. cuneatus, H. elonga tus, H. indicus, H. otolithi,

H. bengalensis, and H. vinodae.

Two of the 16 species, H. pachysomus and H. purii were encountered in this

study. ' ,

1.

Haplosplanchnus pachysomus (Eysenhardt, 1829) Looss, 1902

Figs. 1-5 Plate I

Figs. 1 1- 15 Plate III

SYNONYMS:

Distoma pachysoma Eysenhardt, 1829

Podocotyle pachysomus (Eysenhardt, 1829)

Stossich, 1898

* Laruea caudata Srivastava, 1939

*L. straightum Jehan, 1973

*Haplosplanchnus caudatus Srivastava, 1939

*H. straightum (Jehan, 1973) Ahmad, 1985

*H. orientalis Gupta and Ahmad, 1979

*H. stunkardi Gupta and Ahmad, 1979

*H . guptai Ahmad, 1985

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HOST:

Mugil cephalus (Mugilidae)

3/4/8/8/9/11115/19 in 8 of 9

SITE:

Intestine

DATE O F

COLLECTION : Jan.19, 1992

Feb. 3, 1992

DEPOSITE D

SPECIMENS : USNPC 83982

BM(NH)l993.4.2.81 . 84

HWML 37842

Description (based on 77 specimens, including several live ones; measurements

on 16). Body brownish-yellow in life, Y-shaped or somewhat triangular, tapering

posteriorly, ventrally rolled up in some, dorsally in others, and rounded in a third

group, 0.800-1. 200 long, 0.475-0.875 wide at acetabular level. Cuticle aspinose, eye

spot pigment diffuse. Oral sucker ovoid, 0. 110-0. 200 long, 0.089-0.240 wide; ventral

sucker elongated, 0.450-0 . ()()() long, 0. 180-0.370 wide, with two muscular lips,

situated in the longer arm of the Y-shaped body; ventral sucker length (depth) 2-4

times width. Prepharynx shon; pharynx ovoid, 0. 073-0.120 long, 0. 070-0. 110 wide;

esophagus shon; cecum 0. 140-0.400 long, extending to posterior level of ventral

sucker. Testis single, ovoid, 0 . 140-0. 310 long, 0. 100-0.250 wide in posterior half of

body; seminal vesicle tubular, extending to anterior level of ventral sucker; prostatic

duct surrounded by prostate cells; ejaculatory duct shon. Ovary globular or ovoid,

anterior or anterolateral to, often contiguous with testis in fixed specimens, 0. 070-

0.190 long, 0. 070-0. 140 wide; seminal receptacle variable in position and size, usually

anterolateral to, smaller, same size, or larger than ovary, 0. 078-0.250 long, 0.050-

0.180 wide; vitelline follicles 10-15, poorly developed, distributed from ovary to near

posterior level of ventral sucker. Uterus variable in its posterior extent, usually to

anterior level of testis, and in a few, extending beyond its posterior level; eggs

containing developing miracidia with prominent eye-spots, 45-67 long, 27-35 wide;

Genital atrium tubular; genital pore midway between oral sucker and ventral sucker.

Excretory bladder Y-shaped or sac-like with wide arms, containing a large concretion

like structure, with several smaller ones in one or both of the excretory arms.

H. pachysomus has been reported by several authors (see Bray, 1984) and from

various species of mullets belonging to the Mugil-Liza group, Crenimugil crenilabis,

artd Chelan labrosus (Mugilidae).

Several characteristics have bene used to distinguish the six species of

Haplosplanchnus with an elongated ventral sucker (group 1). These included body

shape, topography of the gonads, whether the gonads are contiguous or separated from

each other, extent of the uterus relative to the testis, size and position of the seminal

receptacle in relation to the ovary, length of the cecum, number and distribution of the

vitellaria, nature of the prostatic complex, and egg size.

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The Fijian specimens were initially identified as H. caudatus. It was noted,

however, that they also have many similarities to H. pachysomus; furthermore, when

the various reports of H. caudatus and H. pachysomus were reviewed, it became

evident that there is complete overlap between the two species not only in terms of

organ topography but also in measurements. It was also noted that there are very few

reports in which the two species were compared. The following historical review and

comparison led to the conclusion that H. caudatus is not distinct from H. pachysomus;

furthennore, several other species (H. straightum, H. orientalis, H. stunkardi, and H.

guptm) should also be considered synonyms of H. caudatus and by extension of H.

pachysomus.

·

A brief review of these species follows:

Haplosplanchnus caudatus (Srivastava, 1939) Skrj. and Gusch., 1955

Figs. 6-10 Plate II

SYNONYM: Laro.ea caudatum Srivastava, 1939

Three reports describe or discuss H. caudatus. Srivastava collected 3 specimens

from Mugil (Liza) vaigiensis Quoy arxl Gaimard, at Puri, Bay of Bengal in 1935, gave

a brief description in 1937 and a more detailed one in 1939 under the generic name

Laruea. In comparing the new genus to Haplosplanchnus, Srivastava (1939: 70) stated

"The new genus, Laruea differs remarkably from

the type genus in the peculiar shape of its body

and of the ventral sucker, and in the position of

its gonads and vitellaria. In all other important

features the two genera are alike."

Madhavi (1979: 239) stated that her 14 specimens from the same host species

and from M. cephalus from Waltair coast, Bay of Bengal

"... showed considerable variation in body shape. The

fully gravid specimens have a shape identical to that

represented for type specimen. They have a

characteristic Y-shaped body with a curved tail like

structure near posterior end arxl the long disc like ventral

sucker situated on a lateral extension. In some specimens

the posterior tail like portion retracted into the body

proper and such specimens had a blunt posterior end.

The younger specimens had a diff�rent body shape which

is almost triangular without any tail like portion near

posterior end. The specimens also showed variation in

the extent of the cecum, some had a longer cecum

almost reaching the level of ovary, in others it is much

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smaller. Eggs measured 39 to 43 in length and 18 to 23

in width."

Madhavi accepted the synonymy of Laruea with Haplosplanchnus as suggested

by Skrjabin and Guschanskaja (1955) and concluded that

" ... the present observation also supports this view as it

is clearly seen that the body shape is variable, and cannot

be used as a reliable taxonomic character. The only

feature that separated the two genera is the shape of the

ventral sucker which has no more than any specific

significance. "

The 77 Fijian specimens obtained from eight M. cephalus, ranging in sire from

10-15 centimeters and captured on two different dates, are in agreement with the

several descriptions and measurements of both H. pachysomus and H. caudatus as

reported in the literature. The Fijian material shows similar variations as described by

Madhavi for H. caudatus. The elongated, curved posterior end described by Srivastava

(1939) was seen in the live material when the worms were placed in a dish on ice and

became fully stretched. When the worms were fixed at room temperature, that shape

changed to triangular, roughly Y-shape, or elongate as seen in figures 1-5 (Plate I).

Many worms took a circular fonn when the posterior end was grabbed by the powerful

muscular acetabular lips of the ventral sucker.

Figures 1, 2, 3, and 5 also show variations in the si.ze and location of the

seminal receptacle. The gonads and the seminal receptacles are usually close together,

but their position in the body depends on degree of contraction of the worms and the

shape they take.

Neither Srivastava (1939) nor Madhavi (1979) described muscular acetabular

lips on the ventral sucker of H. caudatus. Ahmad (1985) had requested Dr. Madhavi

to reexamine her slides of H. caudatus for the presence of these structures, and she

confirmed their presence. Figures 1-5 show the muscular acetabular lips and the

different shapes that the ventral sucker may take as a result of its contraction,

extension, and to a lesser extent influence of cover slip pressure during fixation.

H. caudatus was also reported by Bray (1984) from M. cephalus from

Sodwana, Natal, South Africa. He gave no detailed description or measurements, but

at our request (personal communication: FMN) he measured and reported egg siz.e of

42-48 X 26-28 µm.

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Bray (1984: 278) noted that:

" . . . it (H. caudatus) is very similar to the type of the

genus, Haplosplanchnus pachysomus (Eysenhardt, 1829)

Looss, 1902 and may be synonymous. . . the difference

between H. caudatus and H. pachysomus is in the degree

of development of the ventral sucker for although

elongate in both species, this condition is apparently

greatly more exaggerated in H. caudatus. "

His figures of H. caudatus as well as those of Srivastava and Madhavi are shown in

figures 6-10 (Plate II). Bray (1984) compared the ventral sucker of H. caudatus with

H. pachysomus as figured by various authors including that of Stossich which shows

" .. . an elongate sucker similar to that of H. caudatus,

although the specimen is from the Mediterranean."

This suggested to him

, " .. :that both species occur in the Mediterranean or that

there is but one variable species. "

Dr. Bray examined six specimens we sent him and he was in agreement with

our preliminary identification of the Fijian specimens as H. caudatus. However, further

review of the literature led us to reconsider our original identification and to conclude

that the two species are conspecific. Bray (1984) al8o pointed out the similarity of

Laruea straightum Jehan, 1973, H. orientalis Gupta and Ahmad, 1979, H. stunkardi

Gupta and Ahmad, 1979, all from non-mullets, to H. caudatus, and suggested that they

may be synonyms of the latter. To this group, which we shall call the 'H. caudatus

complex, we add H. guptai Ahmad, 1985 from M. cephalus. All these species,

including ,L. straightum, which was later transferred to Haplosplanchnus by Ahmad

(1985),. are known to have muscular acetabular lips, and their body size, internal

organs, and other measurements overlap. Their eggs are fully developed with eye

spotted miracidia. The variations that we have seen, during live observations and in

fixed specimens, lead us to agree with Bray's insight and suggestion. A brief sumam ry

of each and the justification given by their authors follow.

Haplosplanchnus straightum (Jehan, 1973) Ahinad, 1985

Fig. 16, Plate IV

SYNONYM: Laruea straightum Jehan, 1973

Specimens of this species were collected from Pseudosciaena diacanthus

(Sciaenidae) and Rachycentron canadus ( Rachycentridae).

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The similarity of H. straightum to some Fijian specimens ( Figures 3 and 5,

Plate I) is quite evident. H. straightum is considered a synonym of H. caudatus, and

by extension, of H. pachysomus.

Haplosplanchnus orientalis Gupta and Ahmad, 1979

Fig. 17 Plate IV

H. orientalis, described from a single specimen taken from one /lisha elongata

( =Pellona elongata) (Clupeidae) out of 53 examined from Puri, Orissa, Bay of Bengal,

is probably the same species reported by Gupta and Ahmad in 1975 as Laruea

orientalis.

Gupta and Ahmad ( 1979:187) stated that

"the new form has a close resemblance with H.

caudatum Srivastava, 1939 in having ventral sucker

long, club-shaped and genital pore at bifurcation of Y

but differs from it in having testis, ovary and

receptaculum seminis separated from each other by

uterine coils instead of close together, in having testis

near hind end of body instead of behind first half of

body, in the extension of uterus up to hind end of body

instead of up to testis, in the extension of intestinal

cecum up to a little posterior to ventral sucker instead of

up to a little anterior to receptaculum seminis, in the

extension of vitellaria between ovary and blind end of

intestinal cecum instead of between testis, the ovary and

blind end of intestinal cecum and in having ovary in

posterior third of body instead of in middle third of

body. Accordingly it is regarded as a new species with

the specific name H. orientalis sp. n. "

Since this description is based on a single specimen, the constancy of these

characteristics is hard to determine. The Fijian specimens exhibit variations in all the

characteristics cited by the authors. Bray ( 1984) suggested that differences involving

the distribution of the uterus

" may be of little importance and, in geographical terms,

an intermediate form may occur. "

In view of M adhavi's findings and the variations seen in the Fijian material, H.

orientalis is reduced to a synonym of H. caudatus and by extension of H. pachysomus.

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Haplosplanchnus stunkardi Gupta and Ahmad , 1979.

Fig. 18 Plate IV

H. stunk:ardi was described from two specimens in one Acanthurus sandvicensis

out of 4 1 examined at Puri.

Gupta and Ahmad ( 1979: 188)) acknowledged its similarity to H. caudatus

stating that

"the new form has a close resemblance with H.

caudatum Srivastava, 1939 and H. orjentalis sp. n. in

having long, club-shaped ventral sucker and genital pore

at bifurcation of Y but differs from both these forms in

the extension of ventral.sucker posteriorly up to anterior

to testis, in the extension of intestinal cecum up to

middle of ovary, in the extension of vitellaria between

middle of testis and blind end of intestinal cecum and in

having posterior end rounded. The new form further

. differs from H. caudatum in the extension of uterus

between middle of testis and middle of ventral sucker

instead of between testi s and ventral sucker. The new

form can further be distingui shed from H. orientalis in

having testis and ovary close together instead of

separated from each other by uterine coils and in the

extension of uterus between middle of testis and middle

of ventral sucker instead of between hind end of body

and one third length of ventral sucker. Accordingly it is

regarded as a new species with the specific name H.

stunkardi sp. n."

The characteristics cited by Gupta and Ahmad as distinguishing features of H.

stunkardi are evident in several of the 77 Fijian specimens particularly in the length of

the ventral sucker relative to total body length . Gupta and Ahmad's figure of H.

stunkardi reproduced in figure 18 (Plate IV) is clearly very similar to a Fijian specimen

shown in figure 4 (Plate I). We consider this species also a synonym of H. caudatus,

and by extension, a synonym of H. pachysomus.

H. stunkardi was also reported, but not described or figured, by Ezz El-Dien

et al. ( 1990) from M. cephalus and M. chelo from the Suez Canal , Egypt. These

authors also indicate that Al-Bassel found it in M. capito at Lake Quarun, Nile River

in 1987.

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Haplosplanchnus guptai Ahmad, 1985

Fig. 19 Plate IV

This species was described from nine specimens from the intestine of M.

cephalus from the Panjim Coast, Goa, India.

According to Ahmad (1985: 193)

"the new species most closely resembles H. caudatum

(Srivastava, 1939) , H. straightum (Jehan, 1973) , H.

orientalis Gupta and Ahmad, 1979 and H. stunkardi

Gupta and Alunad, 1CJ79 in the shape of body and in the

structure of ventral sucker. The new species differs from

H. caudatum, H. straightum and H. stunkardi in the

extension of uterus posteriorly up to hind end of body

instead of uterus extending only up to anterior margin of

testis. The new species closely resembles H. orientalis in

the extension of uterus up to posterior end of body but

differs from it in having gonads close together instead of

well separated from one another, in having seminal

receptacle lateral to ovary instead of anterior to ovary, in

having testis elongate and of larger size instead of testis

oval and of smaller size, in having seminal receptacle

contiguous with ovary instead of well anterior to it, in

having eggs of larger size instead of smaller size (35-42

X 18-20 µm) , vitellaria consisting of 7-10 follicles,

postovarian, grouped together instead of vitellaria

consisting of numerous small follicles which are

confined between ovary and blind end of cecum, in

having seminal vesicle of smaller size and stopping much

anterior to testis instead of seminal vesicle of larger size

and stopping near testis."

The only feature that was not observed in the Fijian material is an elongated

testis. This characteristic was emphasized by Ahmad as separating H. guptai from H.

orientalis. In some Fijian specimens, the uterus extends slightly posterior to the testis

but not to the posterior end of the body. The larger eggs (50-65 X 26-37) of H. Guptai

are within the range found in the Fijian specimens, and those given for H. pachysomus.

They also represent an intermediate range between the H caudaJus complex and H.

pachysomus (Table I). We do not consider the shape of the testis significant enough to

justify a new species; in all other respects it is similar to H. pachysomus.

In contrast with the few records on H. caudaJUS, there have bene at least 12

reports of H. pachysomus in recent years from mullets of the Adriatic , Black, and

Mediterranean seas, and the Nile River.

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Yamaguti (1934:361)) was the first to report H. pachysomus from outside these

bodies of water. He recovered this species from young and adult M. cephalus from the

Inland Sea of Japan, stating:

"This species has been dealt with by Looss with

such accuracy that there is no need of redescription, but

I may take this opportunity to supply some details which

are missing in Looss' description.

In the first place the living worm is brownish

yellow throughout, although the alcoholic specimens are

entirely colorless.

The excretory vesicle is divided into two parts;

the posterior is an elongated sac extending to near the

testis, but the anterior is relatively narrow and bifurcates

just behind the testis into lateral arms passing forwards

along the lateral borders of the testis.

The vas deferens forms an elongate oval vesicula

seminalis at its distal end. The terminal portion of the

uterus is distended with embryonated eggs, some hatched

in . the uterus. The empty shells in the uterus measure

about

0.051

X

0.027

mm

.

The

elliptical

free

miracidia

are 0.06-0.07 X 0. 027 -0. 03 mm and covered with short

cilia all over; they have a large x-shaped eye-spot with

a lens on each concave side; at the extreme anterior end

there is a very small sharply pointed stylet"

It should be ooted that neither Srivastava (1939) nor Madhavi (1979) made any

reference to Yamaguti's 1934 report of H. pachysomus from Japan. The presence of

muscular lips in H. pachysomus (Figure 11, Plate Ill) was not described by Looss but

several investigators including Fares and Maillard (1975) reported them (Figure 14,

Plate Ill). Our examination of Fischthal and Kuntz's specimens (Figures 12 and 13,

Plate III) deposited at USNPC also confirms their presence.

Loso s's description of this species was based on specimens from M. cepha.lus

and M. chelo from Trieste, the Adriatic Sea. In addition to the reports of Fischthal and

Kuntz (1963) from M. cephalus and M. (Liza) ramada from Egypt, and Fares and

Maillard (1975) from Liza aurota, L. ramada, M. cephalus and Che/on labrosus from

the French Mediterranean coast, there were several others including Papema ( 1964)

from M. cephalus, M. auratus, M. labeo, and M. chelo from Israel, from the Nile

River and the Mediterranean by several Egyptian parasitologists and in the last 1O years

those of Garippa et al. (1988) from M. cephalus in Italy, and Brglez and Paradiznik

(1988) from M. cephalus in the Adriatic. H. pachysomus was also found in L. ramoda

by Orecchia et al. (1988) in the Mediterranean, and by Radujkovic et a/.(1989) and

Radujkovic and Raibaut (1989) in the Adriatic. Gaevskaya and Dmitrieva ( 1992)

redescribed H. pachysomus from M. cephalus, L. ourata and L. saliens from the Black

Sea; their report and that of Bray ( 1984), as far as we can determine, are the only two

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that compared H. pachysomus with H. caudatus. Bray's conclusion, that the only

difference between the two species is the degree of development of the ventral sucker,

has already been referred to. Gaevskaya and Dmitrieva, on the other hand,

distinguished the two species by egg size which is somewhat greater for H. pachysomus

( 39-57 x 1 8-30) than for H. caudotus ( 39-43 x 18-22). Table I lists egg size range for

H. pachysomus-H. caudatus complex as reported in the literature. The table suggests

that eggs from the Adriatic, Black, and Mediterranean specimens of H. pachysomus

tend to have a slightly larger size compared with those of the H. caudatus complex of

the Indian, southern Atlantic oceans and the Arabian Sea, but the overlap is clear. On

the basis of egg size, the Fijian material must be identified as H. pachysomus; when

shape, topography of organs, and suckers are considered, the only conclusion that can

be made, to paraphrase Bray ( 1984), is either all six species occur in Fijian waters or

there is but one variable species.

In group 2 of the genus Haplosplanchnus no muscular acetabular lips are

present, the ventral: oral sucker ratio and the ventral sucker length compared to its

width is less than 2: 1 . This group includes H. purii Srivastava, 1939, H. mugilis

Nahsha and Cable, 1964, H. bivitellosus Zhukov, 197 1 , H. venezuelensis Fischthal and

Nasir, 1974, H. cuneatus Tang and Lin, 1 978, H. elongatus Tang and Lin, 1978, H.

indicus Gupta and Ahtnad, 1 979, H. otolithi Gupta and Ahmad, 1979, H. bengalensis

Gupta and Puri, 1 985, and H. vinodae Ahmad, 1985.

2. Haplosplanchnus purii Srivastava, 1939

Figs. 24-29 Plate V

SYNONYMS:

H. bivitellosus (Zhukov, 1 97 1) Bray, 1984

H. cuneatus (Tang and Lin, 1978) Bray, 1984

H. elongatus (Tang and Lin, 1 978) Bray, 1984

H. indicus (Gupta and Ahmad, 1 979) Bray, 1 984

*H. otolithi Gupta and Ahmad, 1 979

HOSTS:

Liza vaigiensis (Mugilidae) 7/l of 8

Mugil cephalus (Mugilidae) 11 1 of 9

SITE:

Intestine

DATE OF

COLLECTION: Jan. 19, 1992

Jan. 3 1, 1992

DEPOSITED

SPECIMENS: USNPC 83983

BM(NH) 1994.6. 14. 1

HWML 37843

Description and measurements based on eight specimens. Body somewhat Y

shaped, rounded posteriorly, 0.725- 1.425 long, 0.400-0.650 wide at acetabular level.

Cuticle aspinose, eye-spot pigment diffuse. Oral sucker ovoid, 0. 1 10-0. 1 90 long,

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0.150-0.200 wide; ventral sucker without acetabular lips, somewhat cylindrical, 0.250-

0.350 long, 0.170-0.230 wide; sucker ratio 1:1.6-1.8 ; ventral sucker length ( depth):

width about 1.5:1. Prepharynx short; pharynx spherical, 0.060-0.080 in diameter;

esophagus very short; cecum 0.230-0.350 long, extending to posterior end of ventral

sucker. Testis single ovoid0.110-0.2<50 long, 0.100-0.200 wide, close to posterior end

of body; seminal vesicle a narorw, tubular structure opening anteriorly into small pars

prostatica surrounded by prostate glands. Ovary globular, 0.100-0.160 long, 0.100-

0.120 wide, anterior to and overlapping testis; seminal receptacle dorsal to ovary,

0.063 -0.150 long, 0.043-0.110 wide; vitelline follicles number 10-15 extending

dorsolaterally from seminal receptacle to near posterior level of ventral sucker; uterus

extending from anterior level of testis to near prostatic duct, occupying all the area in

between; eggs 42-58 in length, 25-33 in width, containing developing miracidia with

p rominent eye-spots; in some specimens no eye-spots were observed in any of the eggs

and .in one specimen miracidia were seen in the uterus. Genital pore lies half way

between suckers, and in some, two prominent conical papillae are evident. Excretory

bladder sac-like, with two main canals extending anteriorly to at least level of ventral

sucker.

This is the fifth report of H. purii. Srivastava (1939) desc ribed it from "about

a dozen specimens" from M. (I.ha) vaigiensis, at Puri, Bay of Bengal. Madhavi (1979)

collected14 speciffiens from the same host species and from M. cephalus from Waltair

coast, Bay of Bengal. Wang (1982) reported it from M. cephalus from Fujian

Province, China, but gave neither measure ments nor a drawing. Bray (1984) recovered

it from Liza tricuspidens from Swarthops River estuary, Algoa Bay, Cape Province,

South Africa. N either Madhavi nor Bray reported any measurements of their

specimens. Mehra (1980) lists it in his book on fauna of India, but without explanation,

considered it a synonym of H. pachysomus.

The single Fijian specimen, recovered from M. cephalus, was among 19 others

that were identified as H. pachysomus. All 8 specimens agree with the desc ription of

Srivastav':l (1939) and Madhavi (1979). Srivastava (1939) desc ribed the ventral sucker

as being "bowl-shaped" ( Figure 27 , Plate V); the ventral sucker in our collection is

somewhat more cylindrical. Madhavi's drawing (Figure 28 , Plate V) shows a more

globular ventral sucker. In Madhavi's specimens, the seminal receptacle is shown

between the ovary and testis, but in Bray's (Figure 29 , Plate V) the seminal receptacle

isanterodorsal to the ovary. Also to be noted is the difference in length of the intestinal

cecum.

Bray's (1984) synonymy of the four species of Hoplosplanchnus: H. bivitellosus

Zhukov, 1971 from Sea of Japan and Liao H o River, Yellow Sea, H. cuneatus Tang

and Lin, 1978 from Min River, Fujian, China, H. elongatus Tang and Lin, 1978 from

Min River, Fujian, China, and H. indicus Gupta and Ahmad, 1979 from Puri, Orissa,

Bay of Bengal with H. purii is accepted. To this group, we add H. otolithi Ahmad,

1985.Other species of Hoplosplanchnus group 2 , based on Bray's analysis, may also

be synonymous with H. purii but the 8 Fijian specimens of H. purii do not show the

variations that were observed in the Fijian specimens of H. pachysom us. A brief

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description of species considered synonyms of H. purii by Bray and by us, with

comments, follows:

Haplosplanchnus bivitellosus Zhukov, 1971

Fig. 31 Plate VI

H. bivitellosus was described from 15 specimens recovered from the intestine

of M. cephalus and M. soiuy, from Poyset Bay, Sea of Japan and the Liao River in the

Yellow Sea Basin.

Zhukov (1971:192) stated that

" ... the described species is more similar to H. purii

Srivastava, 1939 from Mugil vaigiensis . . . howev,cr it

differs from it by the presence of paired branches of yolk

glands."

Bray (1984:280) reduced H. bivitellosus to a synonym of H. purii stating that

H. bivitellosus

" ...possess a poorly developed vitellarium in the shape

of two twisted ribbons reaching anteriorly from the

testis. This arrangement needs confirmation, and as the

worm is in every other feature so similar to H. purii, it

is here considered a synonym. "

Haplosplanchnus cuneatus Tang and Lin, 1978

Fig. 32 Plate VI

H. cuneatus from M. cephalus from the Min River, Fujian China, was

described from several specimens (number not indicated).

Tang and Lin (1978:210) differentiated this species

" ... from its most closely related H. purii Srivastava,

1939 by its more prominent vasa efferentia, shorter

vesicula seminalis, much shorter intestinal caecum and

more profuse vitellaria."

Bray (1984) considered these features as variable and reduced H. cuneatus to

a synonym of H. purii. It should be pointed out that in the genus Haplosplanchnus, the

vas deferens is usually not well differentiated from the tubular seminal vesicle; cecal

length is variable.

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Haplosplanchnus elongatus Tang and Lin, 1 978

Fig. 33 Plate V

This species from the intestine of M. cephalus also from the Min River, was

described from a single specimen.

H. elongatus has a ventral sucker that looks more like that of H. purii rather

than H. caudatus. The authors, however, compared it only with H. caudatus.

According to Tang and Lin ( 1 978: 2 1 1) this .

" . . . species differs from its closely related form, H.

caudatus Srivastava, 1939 in several characters such as

the size of eggs, length of the intestinal caecum, and the

form and position of ventral sucker, etc . . . "

Bray ( 1 984: 280) indicated that

" . . ·� none of the features invoked by these authors, and in

particular the vitellarium, appear in view of Madhavi ' s

work to separate these species satisfactorily from H.

purii. H. elongatus is probably only a more fully

developed specimen of H. purii than had been previously

described . "

Haplosplanchnus indicus Gupta and Ahmad, 1979

Fig 34 Plate VI

This species was described from a single specimen from Liza vaigiensis, from

Puri, Orissa, Bay of Bengal .

Gu,pta and Ahmad ( 1 979: 1 9 1 ) stated

"the new form has a close resemblance with H. purii

Srivastava, 1939 in having genital pore on a conical

papilla but differs from it in having vitellaria poorly

developed and extending between receptaculum seminis

and blind end of intestinal cecum instead of scythe

shaped and extending between receptaculum seminis and

opposite body wall, in the extension of uterus up to

anterior margin of testis instead of up to vitellarium, in

the extension of intestinal cecum up to anterior third of

body instead of nearly up to middle third of body and in

having body Y-shaped instead of triangular. Accordingly

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it is regarded as a new species with the specific name H.

indica sp. n. "

Bray ( 1 984:280) suggested that H. indicus

" . . . is clearly a synonym of the latter (H. puri1). Apart

from minor supposed differences in the uterine

distribution, length of cecum and body-shape, the

vitellarium is again described and evoked as a specific

character. "

Haplosplanchnus o tolithi Gupta and Ahmad, 1979

Fig 36 Plate VI

This species was described from two specimens recovered from the intestine of

one Otolithus ruber (Sciaenidae) out of 42 examined from Puri, Orissa.

According to Gupta and Ahmad ( 1979: 190)

"the new form differs from an the known forms of the

genus Haplosplanchnus Looss, 1902 in having body

ovoid, in the extension of intestinal cecum up to middle

of testis, in the extension of vitellaria between a little

posterior to testis and blind end of intestine cecum, in

the extension of uterus between posterior margin of testis

and pharynx and in the disposition of ventral sucker.

Accordingly it is regarded as a new species with the

specific name H. otolithi sp. n."

The ventral sucker of H. otolithi (Figure 38, Plate VI) is very similar to that

seen in a number of Fijian specimens of H. purii (Figures 24-26, Plate V). There is

also a strong similarity in the topography of the gonads. Gupta and Ahmad emphasized

the ovoid shape of the body. It is evident that this body shape may result from lateral

expansion at the midbody-acetabular level as in figure 24 (Plate V). All other

characteristics mentioned by Gupta and Ahmad are variable. For these reasons we

consider H. otolithi a synonym of H. purii.

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GENUS SCHIKHOBALOTREMA Skrjabin and Guschanskaja, 1955

To date 20 species have bene reported : S. acutum (Linton, 1910), S. obtusum

(Linton, 1910), S. adacutum Manter ( 1937) , S. brachyurum (Manter, 1937), S.

pomacenJri (Manter, 1937), S. sparisomae (Manter,. 1937), S. kyphosi (Manter, 1937),

S. girellae (Manter, 1937) , S. adbrachyurum Siddiqi and Cable, 1960, S. manteri,

Siddiqi and Cable, 1960, S. crassum Pritchard and Manter, 1961 , S. glomerosum

Pritchard and Manter, 1961 , S. hawaiiensis Pritchard and Manter, 196 1 , S. robustum,

Pritchard and Manter, 196 1 , S. bivesiculum Nahhas and Cable, 1964, S. elongatum

Nahhas and Cable, 1964, S. acanthuri Yamaguti, 1970, S. Iongivesiculatum Orecchia

and Paggi, 1975, S. magnum Skinner, 1975 and S. folitaria Fernandes and Goulart,

1989. To this group we add 3 species from Fiji. A key made to distinguish among

species of Schikhobalotrema led to the conclusion that 3 Fijian specimens represent new

species.

3. Schikhobalotrema southi n. sp.

Fig. 21 Plate IV

TYPE HOST:

SITE:

DATE OF

COLLECTION:

HOLOTYPE:

Scarus rivulatus (Scaridae) 1 / 1 of 1

Intestine

Jan. 22, 1992

USNPC 83984

Description and measurements based on holotype. Body cylindrical, tapering

posteriorly, 1.675 long, 0.700 wide at acetabular level. Cuticle aspinose, eye-spot

pigment present. Oral sucker subspherical, 0. 190 Jong, 0.225 wide; ventral sucker

subspherical with a circular aperture, 0.260 long, 0. 310 wide; sucker ratio 1 : 1 . 37.

Prepharynx shon; pharynx ovoid, 0. 120 long, 0. 1 10 wide; esophagus shon; cecum

extending to posterior level of testis. Testis large, elongate, 0.450 long, 0. 250 wide,

.about mid-hindbody; seminal vesicle long, extending to anterior level of ventral sucker,

then bending posteriorly to fonn U-shaped tube before joining cylindrical prostate

gland. Ovary ovoid, 0. 120 long, 0. 170 wide, occupying space between anterior level

of testis and posterior level of ventral sucker; seminal receptacle saccular, transversely

elongate dorsolateral to ovary, 0.225 long, 0.063 wide; uterus preovarian, extending

from anterior level of ovary occupying most of the space dorsal to ventral sucker; eggs

in moderate numbers, large, 83-88 long, 53-60 wide; vitelline follicles large, extending

from near posterior end of body to level of pharynx dorsally . Genital atrium tubular,

protruding; genital pore midway between oral sucker and ventral sucker. Excretory

bladder sac-like, one arm seen extending to near pharyngeal level; its pore terminal.

This species is most similar to S. obtusum (Linton, 1910) Skrj. and Gusch. ,

1955 sharing with it a saccular seminal receptacle. In S. southi the seminal receptacle

is dorsal to the ovary and transversely elongate with a ventral dorsal orientation. In S.

obtusum, the seminal receptacle runs parallel to the anterior level of the testis and has

an anterior posterior orientation. It is funher distinguished from S. obtusum by the U-

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shaped anterior part of the seminal vesicle in contrast with an almost straight seminal

vesicle in S. obtusum.

Schikhobalotrema sollthi is named for Professor G. Robin South, Professor of

Marine Studies, The University of the South Pacific, Suva, Republic of Fiji, in

appreciation for his assistance in providing the research facilities for the senior author.

A second specimen of Schikhobalotrema was found in the same host. The two

specimens were not suspected as being different species until they were stained and

mounted. The description of the second specimen follows.

4. Schikhobalotrema sp. # 1

Fig. 22 Plate IV

TYPE HOST: Scarus rivulatus (Scaridae) 1 1 1 of 1

SITE:

Intestine

DATE OF

COLLECTION: Jan. 22, 1992

Description and measurements based on a single specimen. Body somewhat

ovoid, flattened ventrally , tapering posteriorly, 1. 450 long, 0. 600 wide at acetabular

level . Cuticle aspinose, eye-spot pigment present. Oral sucker ovoid, 0. 1 80 long ,

0.200 wide; ventral sucker almost spherical with a circular aperture, 0.260 long, 0. 240

wide; sucker ratio 1 : 1 . 3. Prepharynx short; pharynx ovoid, about 0. 120 in diameter;

esophagus short; cecum not evident past testicular level. Testis very large, elongate,

0. 550 long, 0. 375 wide occupying most of the hindbody; seminal vesicle tubular, its

posterior end overlapping testis anteriorly , anterior extent and course not determined.

Ovary ovoid , 0. 150 long, 0. 170 wide, anterodorsal to ventral sucker; seminal

receptacle not sene; uterus not observed; eggs few, sene in the ovario-pharyngeal area,

large, 95 long, 55 wide; vitelline follicles large, extending mostly from near posterior

end of body dorsally to anterior level of pharynx. Genital atrium and excretory bladder

not observed.

The only other species with an ovary dorsal to the ventral sucker are:

S. hawaiiensis, S. crassum, and S. glomerosum.

In S. hawaiiensis, the ovary is elongate, sometimes slightly indented or bent

near middle, a little dextral between testis and ventral sucker or dorsal to ventral

sucker, and the testis is comparatively smaller. In Schikhobalotrema sp. #1, the ovary

is spherical and anterodorsal to ventral sucker and the testis much larger.

In S. crassum, the testis is more anterior and much smaller than that of

Schikhobalotrema sp. #1 .

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S. glomerosum has a subspherical body; the testis is posterodorsal to ventral

sucker in contrast with ovoid body and a postacetabular testis.

Even though a number of important characteristics could not be identified, this

specimen clearly represents a new species because of the anterodorsal location of the

ovary relative to the ventral sucker and the very large testis. A name is not assigned

to this species, however, because the slide, after the specimen was studied, measured

and drawn, was shattered as a result of an Uf!fortunate accident.

The next species is also described but not named, because of the absence of ova

and our inability to observe details relating to the terminal parts of the male and female

reproductive structures.

5. Schikhobalotrema sp. #2

Fig. 23 Plate IV

TYPE HOST: Acanthurus xanthopterus (Acanthuridae) 1 1 1 of 1

SITE: .

Intestine

DATE OF

COLLECTION: Jan. 23, 1992

DEPOSITED

SPECIMEN : USNPC 83985

Description and measurements based on a single specimen. Body elongate,

cylindrical , rounded posteriorly, 1 . 700 long, 0. 525 wide at acetabular level. Cuticle

aspinose, eye-spot pigment present. Oral sucker subterminal, 0. 240 long, 0. 300 wide;

ventral sucker spherical with a circular aperture, 0.260 long, 0. 300 wide; sucker ratio

about 1 : 1 . Prepharynx short; pharynx 0. 1 1 0 in diameter; esophagus short; cecum

extending to midlevel of ovary. Testis ovoid, 0.420 long, 0.250 wide, near posterior

end of body; seminal vesicle long, tubular, extending to level of ventral sucker. Ovary

ovoid, al'lterolateral to testis, 0. 220 long, 0. 1 30 wide; seminal receptacle same level

as ovary, 0. 135 long, 0.073 wide; uterus not observed; no ova present; vitelline

follicles large, extending from posterior end of testis to near posterior level of pharynx.

Male and female reproductive structures could not be differentiated beyond level of

ventral sucker. Excretory bladder I-shaped with 2 arms extending anteriorly; pore

terminal .

Schikhobalotrema sp.#2 bears certain similarities to S. robustum Pritchard and

Manter, 1961 . It differs, however, by its shorter cecum, which extends to midlevel of

ovary rather than to the anterior third of the testis, and a more anterior ovary.

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6. Hymenocotta mulli Manter, 196

Figs. 66, 67 Plate IX

HOSTS:

SITE:

DATE OF

COLLECTION :

DEPOSITED

SPECIMEN :

Liza vaigiensis (Mugilidae) 1 11 of 8

Mugil cephalus (Mugilidae) 111 of 9

Intestine

Jan. 19, 1992,

Jan. 3 1 , 1992

USNPC 83986

Description and measurements based on two specimens, one mature from L.

vaigiensis, the other immature from M. cephalus , (measurements on immature

specimen in parentheses) . Body elongate, rounded posteriorly, 3 .380 (0.90)0 long ,

0. 875 (0. 350) wide at acetabular level; forebody 0.400 long. Cuticle aspinose, eye-spot

pigments very few , near pharynx. Oral sucker replaced by a broad membranous

muscular fold with six short, rounded lobes, as described by Manter (1961); ventral

sucker cup-shaped 0. 600 (0. 240) long , 0. 540 (0. 240) wide. Prepharynx short 0. 125

(0.095) long, 0.075 (0. 020) wide; pharynx ovoid , 0.350 (0. 125) long , 0. 250 (0. 105)

wide; esophagus short; cecum extending to anterior level of ovary . Testis elongate,

0. 675 (0. 105) long , 0. 275 (0.080) wide, near posterior end of body ; sperm duct

tubular, straight, becoming a seminal vesicle just posterior to the ventral sucker;

prostatic duct ovoid, dorsal to ventral sucker, with few prostatic cells in its anterior

half. Cirrus sac, if present, poorly developed. Ovary entire, overlapping anterior end

of testis, 0. 180 long, 0. 170 wide; seminal receptacle globular, thick walled, little

smaller than ovary; uterus not extending posterior to testis; eggs large, opaque ones 80-

100 long, 50-63 wide; vitellaria consisting of fused follicles, extending from posterior

end of testis laterally, but not reaching ventral sucker. Terminal parts of male and

female reproductive structures not discerned clearly anterior to mid acetabular level .

This is the sixth report of this species. Manter (1961) described it from an

unknown mullet (family Mugilidae) from Fiji. Durio and Manter (1968) reported it

from New Caledonia from an unknown mullet (family Mugilidae) and from M.

cephalus from Heron Island, Queensland , Australia. Hafeezullah (1971) found it in

Chirocentrus dorab from India. Overstreet in Lester and Sewell (1989) recorded it

from Crenimugil labiosus, L. vaigiensis, and Myxus elongatus. Cribb et al. (1994)

found it in Crenimugil crenilabis, M. cephalus, and L. vaigiensis from the southern

Great Barrier Reef, Australia. Our mature specimen is in general agreement with

Manter's description but differs in having a larger and more elongate testis. The testis

also occupies a more posterior location. Cribb et al. (1994), studying serial sections,

concluded that H. mulli possesses a vesicular pars prostatica but lacks a cirrus sac. We

have reexamined our specimen but are unable to see clearly any structure anterior to

the ventral sucker. We have also examined a paratype from Manter' s collection

(HWML 0510-F4) and a specimen from the New Caledonia (1847); the paratype shows

a membrane near the anterior level of the ventral sucker which could represent the

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4.1 Page 31

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lining of a cirrus sac or that of a vesicular pars prostatica as described by Cribb et al .

( 1 994) ; In the New Caledonia specimen a thin membrane is also seen which we

interpret as suggestive of a weakly developed cirrus sac thus confinning a conclusion

arrived at by Overstreet ( 1 969) in his examination of the same New Caledonia material ;

a short cirrus extruding from the genital pore was also seen ; the testis, though not as

elongate as the Fijian' s specimen, also occupies a more posterior position. It should be

noted , however, that these observations are based on whole mounts and subject to

personal interpretations; only Cribbs' specimens are based on sectioned material. Our

own conclusion is that a weakly developed cirrus sac is present.

The next group of haplosplanchnids have been reported from other parts of the

world and are presented as a review and an update.

PART II - Haplosplanchnids of Other Parts of the World

7. Haplosplanchnus mugilis Nahhas and Cable, 1 964

Fig . 30 Plate VI

This species was described from 13 specimens taken from Cur�ao, West

Indies.

According to Nahhas and Cable ( 1 964: 1 80)

"this i s the first species of Haplosplanchnus to be

reported from the Gulf-Caribbean region. Of the 3

previously described species H. mugilis is most like H.

pachysomus (Eysenhardt, 1829) , but differs in having a

shorter seminal vesicle, shorter peduncle of the ventral

sucker, a spherical or ovoid pars prostatica and the

uterus extending posterior to the testis. It differs from H.

caudatus Srivastava, 1 939 in the same respects and also

in body shape. In H. purii Srivastava, 1 939, the testis is

in the extreme posterior of the body , the cecum and

seminal vesicle are long, the vitellaria are compact, and

the pars prostatica tubular. "

Bray ( 1 984: 280) suggested that the extent of the uterus posterior to the testis

"may be of little importance and, in geographical terms, an intermediate form may

ocuc r. " We agree, in principle, with Bray ' s comments. We note, however, that none

of the species he placed in synonymy with H. purii, none of the Fijian specimens, or

H. otolithi which we also consider a synonym, have uterine coils that extend posterior

to the testis. Madhavi's (1979) observations on H. caudatum dealt with variations in

body shape and length of cecum but not on extent of the uterus. She did not report any

variations in extent of uterus in her specimens of H. purii either.

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HOSTS :

RECORD S :

GEOGRAPHIC

DISTRIBUTION:

Che/on labrosus, Crenimugil crenilabis, Mugil cephalus, M.

curema (Type host) , M. saliens, M. trichodon (Mugilidae).

Skinner ( 1975); Fischthal ( 1977). Juarez-Arroyo and Salgado

Maldonado ( 1989). According to Bray ( 1984) , H. mugilis has

been reported, but not described, from the Mediterranean by

Nikolaeva and Parukhin in 1969, and by Parukhin, Naidenova

and Nikolaeva in 197 1 .

Curacao, Bay of Biscayne , Belize, Mediterranean, Mexican

Pacific

8 . Haplosplanchnus venezuelensis Fischthal and Nasir, 1974

Fig. 35 Plate VI

H. venezuelensis was described from a single specimen.

Fischthal and Nasir ( 1974: 73) stated that this species

" . . . appears closest to H. mugilis Nahhas and Cable,

1964 from a mugiliform (Mugilidae) fish from Curacao.

The latter species differs from H. v�lensis in having

the testis about midway between the ventral sucker and

posterior extremity and the genital pore midway between

the ventral sucker and pharynx, and the vitellaria

consisting of 10-12 inconspicuous, scattered follicles. "

HOST:

RECORD :

GEOGRAPHIC

DISTRIBUTION :

An tennarius multiocella tus (Antennariidae).

Fischthal and Nasir ( 1 974)

Los Roques Islands (Venezuela)

9. Haplosplanchnus bengalensis Gupta and Puri , 1 985

Fig. 37 Plate VI

H. bengalensis was desc ribed from a single specimen .

In comparing this species to others Gupta and Puri ( 1985 : 56) indicated that

" . . . the new form has close resemblance with H. purl and

H. indica in having genital papillae lying on prominent

conical papillae but differs from them in having

intestinal caeca extending up to a little posterior to

ventral sucker instead of up to a little anterior to ovary

in H. purii and up to anterior third of body in H. indica.

The new form further differs from H. purii in the extent

of the uterus between anterior margin of testis and

oesophagus instead of from vitellaria to pars prostatica.

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Accordingly it is regarded as a new species with the

specific name Haplosplanchnus bengalensis sp. nov. "

This species, has a strong resemblance, except for more extensive vitellaria, to

H. elongatus and H. indicus both of which were considered synonyms of H. purii by

Bray ( 1 984) . The vitellaria were described by Gupta and Puri ( 1 985 : 54) as

"follicular, poorly developed, extending from anterior

end of pharynx up to a little anterior to hind end of body

but interrupted in oesophageal region. "

This distribution of vitellaria is unusual for the genus Haplosplanchnus and

needs confirmation.

HOST:

RECOR D:

GEOGR APHIC

DISTRIBUTION :

Acanthurus sandvicensis ( Acanthuridae)

Gupta and Puri ( 1 985) .

Puri, Orissa, Bay of Bengal.

10. Haplosplanchnus vinodae Ahmad, 1 985

Fig. 38 Plate VI

H. vinodae was described from seven specimens.

Ahmad (1985: 191) distinguished it

"from all the known species of the genus

Haplosplanchnus in having prostate vesicle bipartite

instead of unipartite. "

In many respects this species is very similar to H. otolithi except for its

'bipartite' prostate vesicle and the extent of the uterus to the posterior end of the body.

Ahmad's figure shows what looks to us like a ' split' rather than a ' bipartite' prostatic

vesicle.

HOST:

RECOR D:

GEOGRAPHIC

DISTRIBUTION:

Mugil cephalus

Ahmad ( 1 985)

Panjim coast, Goa, India.

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1 1 . Schikhobalotrema acutum (Linton, 1910) Skrj . and Gusch. , 1 955

Figs. 39-42 Plate VII

SYNONYMS : Distomum spp. Linton, 1 907

Deradena acuta Linton, 1910

Haplosplanchnus acuta (Linton, 1910) Manter, 1937

Linton's (1910) original description is based on specimens recovered from the

intestine of Tylosurus acus from Bermuda and T. marinus from Tortugas, Florida.

Manter (1937: 386) redescribed the species from several specimens from T. raphidoma

from Tortugas, stating

"This species differs from all preceding species of

Haplosp'lanchnus in the longitudinal slit-like aperture of

the ventral sucker and the pair of flap-like lateral

processes at its posterior end . These characters may

prove to be of generic value. The genital bulb is much

better developed in H. acutus and the eggs are slightly

smaller than in preceding species from Tortugas.

What seme s to be the same species had bene collected by

the author from Tylosurusfodiator and Kyphosus elegans

from the Pacific Ocean at Port Utria, Colombia. It may

prove to be a characteristic and widely distributed

parasite of Tylosurus. The lobe-like processes of the

ventral sucker are unique. They were apparently

overlooked by Linton and no observations on their living

state are available. They seem to be flexible, perhaps

contractile. Since they do not seem to be strong enough

to aid in attachment they may serve as sense organs" .

Overstreet (1969) described the tubular genital bulb. Madhavi ( 1 979:240) stated

that her 24 specimens are:

" . . . morphologically indistinguishable from those

described from American Atlantic and Pacific

Coasts. . However, a notable feature in the present

specimens is that they lacked spermatozoa inside the

reproductive ducts. In inunature as well as gravid

specimens the receptaculum seminis and seminal vesicle

has a collapsed appearance and they are filled with a

granular material rather than spermatozoa. Earlier

authors illustrated receptaculum seminis and seminal

vesicle of S. acutum as being distended with

spermatozoa. To confirm the absence of spermatozoa in

the present specimens section and smears of testis stained

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4.5 Page 35

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with Feulgen were examined. They revealed but few

spennatozoa which appear abortive. The eggs produced

by these flukes, however, developed nonnally. It appears

that this is a parthenogenic race and detailed cytological

study of this fonn may prove that it is a sibling species. 11

HOSTS :

RECORDS:

GEOGRAPHIC

DISTRIBUTION:

Thyrinops pachylepis (Atherinidae); Strongylura ardeola, S.

timucu, Strongylura sp., Tylosurus acus, T. caribbaeus, T.

crocodilus, T. marinus, T. raphidoma (Belonidae);

Hemiramphus margintatus H. georgi, Hyporamphus unifasciatus

(Hemiramphidae); Mugil cephalus (Mugilidae); Abudefduf

sartilis (Pomacentridae) ; Kyphosus elegans(Kyphosidae) ;

Lachnolaimus maximus (Labridae).

Linton (1910); Manter (1937 , 1940 , 1 947); Caballero et al.

(1 95 3); Perez Vigueras (1956) ; Siddiqi and Cable (1 960);

Sogandares-Bemal and Sogandares (1 961) ; Nahhas and Cable

(1 964); Overstreet (1 969) ; Fischthal (1977); Madhavi (1 979);

Yeo and Spieler (1 980) , Kohn and Fernandes (1 982 ; Fayek et

'

al. (1 990) ; Shen (1 990)

Bermuda, Florida, Brazil, Galapagos Islands, Pacific coast of

Colombia, Cuba, Puerto Rico, Curacao, Jamaica, Belize, Bay

of Bengal, Mediterranean, South China Sea.

12. Schikhobalotrema obtusum (Linton, 1 910) Skrj . and Gusch. , 1 955

Figs. 43 , 44 Plate VII

SYNONYMS: Deradena obtusa Linton, 1 910

Haplosplanchnus obtusus (Linton, 1 910) Manter, 1 937

Manter (1 937 : 38 2) distinguished this species

from 11 • • • all others at Tortugas by the almost equal size

of the suckers and the elongated seminal receptacle. The

hindbody is long, the ovary unlobed in contrast to certain

other species. It differs from H. pachysomus in length of

cecum, in extent of v!tellaria and in larger size of eggs. "

Pritchard and Manter's record from Hawaii was questioned by Yamaguti (1 971)

who indicated that the Hawaiian form is probably S. acanthuri Yamaguti , 1 971 .

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HOSTS:

RECORDS :

GEOGRAPHIC

DISTRIBUTION:

Acanthurus achilles, A. bahianus, A. caerulus, A. sandvicensis,

Paracanthurus hepatus ,( = Acanthurus hepatus)(Acanthuridae) ,

Sparisoma viride (Sparidae) .

Linton (1910); Manter ( 1937 , 1947); Siddiqi and Cable ( 1 960);

Nahhas and Cable ( 1 964); Pritchard and Manter ( 1 96 1 ); Nahhas

and Carlson ( 1994).

Florida, Puerto Rico , Curacao , Jamaica, Hawaii .

1 3 . Schikhobalotrema adacutum (Manter, 1 937) Skrj . and Gusch. , 1 955

Fig. 45 Plate VII

SYNONYM : Haplosplanchnus adacutus Manter, 1937

According to Manter ( 1937: 387)

" it is very difficult to separate this species from

Haplosplanchnus acutus . It is distinctly smaller, only

one specimen of over 20 reaching a length of 1 mm,

whereas the smallest of 6 specimens of H. acutus was

1 . 267 mm. In all except one specimen of H. adacutus,

the posttesticular distance was greater than the testis

ventral sucker distance, whereas the opposite was true in

all specimens of H. acutus. The ventral sucker lobes

were almost always very inconspicuous in H. adacutus

(except two specimens from Halichoeres maculipinnus)

and very evident in H. acutus. A constant difference

occurs in the relative size of the genital atrium or bulb

which is small and inconspicuous in H. adacutus and as

large or larger than the pharynx in H. acutus. These

differences may be those of one species in different hosts

but the general impression given is that the two forms

(each of which was collected several times) are distinct . "

HOSTS :

RECORDS :

GEOGRAPHIC

DISTRIBUTION:

Abudefduf marginatus, A. saxatilis (Pomacentridae);

Halichoerus maculipinnus , H. bivittatus, H. pictus (Labridae);

Hemiramphus brasiliensis (Hemiramphidae); Hepsetia stipes

(Atherinidae) .

Manter ( 1 937, 1947); Nahhas and Cable ( 1 964) , Yeo and

Spieler ( 1 980) .

Florida, Jamaica, Curacao .

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14. Schikhobalotrema brachyurum (Manter, 1937) Skrj . and Gusch. , 1955

Fig. 46 Plate VII

SYNONYM: Haplosplanchnus brachyurus Manter, 1937

According to Manter ( 1961 : 384)

"this species differs from the others at Tortugas by the

short hindbody , large ventral sucker and anterior extent

of vitellaria. In these respects it is especially distinct

from H. obtusus. The sucker ratio is approximately that

of H. sparisomae but the hindbody is much shorter and

the ovary is unlobed. "

HOSTS:

RECORDS:

GEOGRAPHIC

DISTRIBUTION:

Cryptotomus auropunctatus, PseTJ(foscarus guacamaia,

P. coelestinus (Scaridae); Sparisoma aurofrenatum, S.

spinidens, S. viride (Sparidae).

Manter ( 1937, 1947).

Florida.

15. Schikhobalotrema pomacentri (Manter, 1937) Skrj. and Gusch. , 1955

Figs. 47-49 Plate VII

SYNONYM : Haplosplanchnus pomacentri Manter, 1937

According to Manter ( 1 937:385)

"this species was not reported by Linton. It differs from

all others at Tortugas in the presence of a distinct

prostatic vesicle with tall transparent cells and in a more

muscular genital atrium. The species most similar to it is

H. brachyurus from parrot fish. But in addition to the

point noted, H. pomacentri differs in that the hindbody

is never shorter that the forebody . "

Manter ( 1 937: 385) also indicated that

" . . . a Haplosplanchnus species from Pomacentrus

rectifraenum Gill collected in the Galapagos Islands

agrees with H. pomacentri from Tortugas in all

important respects including the prostatic vesicle and is

probably the same species. "

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Nahhas and Carlson ( 1 994) listed its most important characteristics: a relatively

smal l seminal receptacle, almost equal length of fore- and hindbody , smal l ovary

(about same size as egg length) , transverse acetabular aperture, tendency of vitellaria

to coalesce longitudinally, muscular genital atrium, and a distinct prostatic vesicle.

Cribb et. al ( 1 994) reported this species from several pomacentrids; their figure shows

a ventral sucker slightly anterior to midbody but more importantly eggs much smaller

than the ovary ; the measurements they give in their Table II do not include egg size for

comparison with ovary size; In other respects, it has many similarities to S.

pomacentri. Based on their figure, their specimens do not key out to S. pomacentri or

any known Schikhobalotrema species (no key is really adequate or good enough to

make a definitive identification especially if based on a drawing) . The Australian

species may represent a new form but a comparison between ovary size and egg length

should be made before definitive diagnosis is made; for the time being we accept the

authors' identification. S. pomacentri was not found in 1 3 fishes belonging to six

species of pomacentrids from Fij i (unpublished data) .

Fischthal' s (1977) report of S. pomacentri from Sparisoma chrysopterus is the

only report of this species from a non-pomacentrid host.

HOSTS :

RECORDS :

GEOGRAPHIC

DISTRIBUTION:

Abudefduf whitleyi, Acanthochromis polyacanthus, Amphiprion

akinodynos, A. perideraion; Microspathodon chrysurus;

Panna polylepis; Chromis chrysura ( = Pomacentrus chrysurus),

C. Xanthura ( = Pomacentrus xanthurus), C. analis

(Pomacentrus analis), Pomacentrus fuscus, P. leucostictus, P.

philippinus, P. planifrons, P. rectifraenum, P. tripunctatus,

Pomacentrus sp., Stegastes apicalis (Pomacentridae) ; Sparisoma

chrysopterum (Sparidae).

Manter ( 1937, 1 947); Siddiqi and Cable ( 1960); Sogandares

Bernal and Sogandares (1961); Nahah s and Cable (1964) ;

Fischthal ( 1 977) ; Yeo and Spieler (1980); Dyer et a/. (1991);

Nahah s and Carlson (1994) ; Cribb et al. (1 994).

Florida, Puerto Rico , Panamanian Atlantic , Jamaica, Belize,

southern Great Barrier Reef.

16. Schikhobalotrema sparisomae (Manter, 1937) Skrj . and Gusch. , 1955

Fig. 50 Plate VII

SYNONYM: Haplosplanchnus sparisomae Manter, 1937

Manter ( 1 937: 382) distinguished this species

" . . . from others at Tortugas by the large ventral

sucker with circular aperture and the deeply

lobed or tripartite ovary. It differs from H.

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4.9 Page 39

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pachysomus in sucker ratio, shape of ovary,

extent of vitellaria and in its much larger eggs. "

Nahhas and Carlson (1994 :11) stated

"Posterior extent of the seminal vesicle was not

described by Manter (1937) nor mentioned by

other autho rs. One of the five specimens clearly

shows a long seminal vesicle which is almost

straight extending posteriorl y to level of ventral

sucker. A reexamination of th ree worms

identified as this species from Pseudoscarus

guacamaia from me earlier Jamaican collection

shows, in one worm, a seminal vesicle

extending only to mid- acetabular level. "

HOSTS:

Mugil cephalus (Mugilidae) ; Nicholsina usta, Pseudoscarus

guacamaia, P. perrico, Scarus croicensis, Scarus sp . (Scaridae) ;

. Sparisoma abildgaardi, S. brachiale, S. jlavescens, S. radians, S.

viride (Sparidae) .

R EC ORDS:

Manter (1937) ; Nahhas an d C able (1964) ;

Overstree t (1969) ; Nahhas and Carlson (1994).

GEOGRAPH IC

DISTRIBUTION: Florida, Jamaica, C ur�ao.

1 7 . Schikhobalotrema kyphosi (Manter, 1947) Skrj. an d Gusch. , 1955

Fig. 51 Plate VIII

SYNONYM: Haplosplanchnus kyphosi Manter, 1947

According to Manter (1947 :3 26)

" . . .H. sparisomae is the only other species with

lobed ovary and seem to be the most closely

related species. It differs in body shape , sucker

ratio (the ventral sucker is 1 .5 times the oral

sucker) , in extent of uterus, and in its very sh ort

posttesticular sp ace. "

HOSTS:

Kyphosus incisor, K. sectatrix (Kyphosidae).

REC ORDS:

Manter (1947) ; Overstree t (1969) .

GEOGRAPH IC

DISTRIBUTION : Florida (Tortugas , Bay of B iscayne)

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18. Schikhobalotrema girellae (Manter and van Cleave, 195 1 ) Skrj. and Gusch. ,

1 955

Fig. 52 Plate VIII

SYNONYM: Haplosplanchnus girellae Manter and Van Cleave, 1951

According to Manter and Van Cleave ( 1 95 1 : 335)

"H. girellae is probably most similar to H.

kyphosi Manter, 1947, and H. obtusus (Linton,

1 9 10) from Tortugas, Fla. It differs from H.

obtusus in its long posttesticular space, in the

spherical shape of the seminal receptacle, in

J acking distinct vitelline follicles, in the

interruption of the vitellaria opposite the testis,

and in shape of the eggs. It differs from H.

kyphosi in its unlobed ovary, relatively larger

ventral sucker, elongated testis, interrupted

vitellaria and smaller body sire. "

HOST:

Girella nigricans Kyphosidae

RECORDS:

Manter and Van Cleave ( 1951).

GEOGRAPHIC

DISTRIBUTION: La Jolla (California) .

19. Schikhobalotrema adbrachyurum Siddiqi and Cable, 1960

Fig. 53 Plate VIII

According to Siddiqi and Cable ( 1 960: 275)

"S. adbrachyura resembles most S. brachyura

but differs from it in having a strongly lobed

ovary and shorter seminal vesicle. "

HOSTS :

Pseudoscarus guacamaia, P. plumbaeus (Scaridae) ; Sparisoma

jlavescens, S. viride, Sparisoma sp. (Sparidae).

RECORDS:

Siddiqi and Cable ( 1 960); Nahhas and Cable (1 964)

GEOGRAPHIC

DISTRIBUTION: Puerto Rico, Jamaica, Curacao.

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20. Schikhobalotrema manteri Siddiqi and Cable, 1960

Fig . 54 Plate VIII

According to Siddiqi and Cable ( 1 960: 274)

"Schikhobalotrema manteri differs from all other

species of the genus in the distribution of

vitellaria, the relative position of the gonads,

and the posterior extent of the uterus. "

HOSTS :

a "reeffish with a collar "; Acanthurus bahianus (Acanthuridae)

RECORDS:

Siddiqi and Cable ( 1 960); Dyer et al. ( 1 992) .

GEOGRAPHIC

DISTRIBUTION: Puerto Rico.

21 . Schikhobalotrema crasswn Pritchard and Manter, 1 96 1

Fig . 5 5 Plate VIII

According to Pritchard and Manter ( 1 96 1 : 195)

"S. brachyurum and S. hawaiensis may also

have the testis near or even overlapping the

ventral sucker. S. brachyurum has conspicuously

larger suckers relative to body siz.e, although the

sucker ratio is probably similar, the hindbody is

much shorter, and the vitellaria are more

extensive and more follicular. S. hawaiensis has

a shorter hindbody , a smaller sucker ratio, lacks

large prostatic cells, lacks a well-differentiated

metraterm, and lacks the conspicuously thick

cuticula. "

Pritchard and Manter ( 1 96 1 : 196) noted that

" . . . S. crassum also resembles S. robustum with

which it may be sympatric but S. crassum has a

thicker body with a conspicuously thick cuticula,

the testis overlaps the ventral sucker 113 or more

with the ovary correspondingly more anterior,

and the excretory vesicle is shorter. "

HOST:

Stegastes fasciolotus ( =Pomacentrus jenkinsi) (Pomacentridae)

RECORD :

Pritchard and Manter ( 1 96 1).

GEOGRAPHIC

DISTRIBUTION : Hawaii

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22. Schikhobalotrema glomerosum Pritchard and Manter, 1961

Fig. 56 Plate VIII

According to Pritchard and Manter ( 196 1 : 196)

" . . . S. brachyurum (Manter, 1 937) and S.

adbrachyurum Siddiqi and Cable, 1960 are the

only other species in which the ventral sucker

may be found posterior to the midbody . In both

species the cecum extends posterior to the

ventral sucker, the ventral sucker is larger, the

ovary and testis are in the hindbody, the testis is

smaller than the ventral sucker, the vitellaria are

follicular, and the body is more elongate. "

HOSTS:

Acanthurus achilles, A. sandvicensis (Acanthuridae).

RECORD:

Pritchard and Manter ( 1 961).

GEOGRAPHIC

DISTRIBUTION: Hawaii.

23. Schikhobalotrema hawaiiensis Pritchard and Manter, 1961

Fig. 57 Plate VIII

According to Pritchard and Manter ( 1 96 1 : 194)

"three species, S. brachyurum (Manter, 1 937),

S. pomacentri (Manter, 1937), and S.

adbrachyurum Siddiqi and Cable, 1960, have

the ventral sucker located at or slightly behind

the midbody . Tortugas, Florida, is the type

locality for the first two species and Puerto Rico

is the type locality for S. adbrachyurum. Manter

(1940) has also reported S. pomacentri from the

Galapagos Islands. " S. hawaiensis is like S.

pomacentri in that the hindbody may equal the

forebody in length but is never shorter, and the

anterior vitellaria do not extend to the oral

sucker. S. hawaiensis, however, differs from S.

pomacentri by lacking a prostatic vesicle, by

lacking a posterior marginal projection on the

oral sucker, by a less tapered and more rounded

hindbody , in the testis which is larger than the

ventral sucker and immediately posterior to it

(rather than being in the middle of the

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5.3 Page 43

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hindbody). S. hawaiensis is like S. brachyurum

in lacking the prostatic vesicle, in lacking a

posterior marginal projection of the oral sucker,

in the testis that may overlap the ventral sucker,

and the seminal vesicle that is sinuous rather

than almost straight. It differs from S.

brachyurum in that the hindbody is never shorter

than the forebody (though it may be nearly

equal), the vitellaria usually extend only to the

level of the genital pore (and no farther forward

than the posterior edge of the pharynx), the

uterus is entirely preovarian, and the ventral

sucker is slightly smaller affecting the sucker

ratio (1: 1. 2 to 1. 4 as compared with 1: 1. 5 to 2

for S. brachyurum) . S. adbrachyurum has the

ventral sucker slightly posterior to midbody, but

the testis is near the posterior end of the body,

the ovary is lobed, the seminal vesicle is shorter,

the eggs are wider, and the body is smaller"

Yamaguti (1970) indicated that a metraterm is present, contrary to Pritchard and

Manter' s (1961) assertion of its absence. Yamaguti 's specimens were obtained from

the same host species and locality as Pritchard and Manter' s.

HOSTS :

Acanthurus mata, CtetWchaetus strigosus (Acanthuridae) .

RECORDS:

Pritchard and Manter (1961) ; Yamaguti (1970) .

GEOGRAPHIC

DISTRIBUTION : Hawaii .

24. Schikhobalotrema robustum, Pritchard and Manter, 1961

Fig. 58 Plate VIII

According to Pritchard and Manter ( 1 96 1 : 192)

" in size and long posttesticular space S.

robustum is similar to S. kyphosi (Manter,

1947), but it differs markedly in having an

unlobed ovary, much larger testis, larger sucker

ratio, and less follicular vitellaria. S. robustum

i s most similar to S. girellae (Manter and Van

Cleave, 195 1) . It differs in being much larger,

although the egg size is about the same. The

difference in body size makes the eggs appear to

be much larger in S. girellae. The so-called

cirrus of S. girellae is probably a thick-walled

tubular atrium although entrance of the uterus

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could not be sene in 15 paratypes. The atrial

tube in S. robustum is thin-walled and shorter.

Prostatic cells are much smaller in S. girellae.

Although the interruption of the vitelline glands

opposite the testis was emphasiz.ed for S.

girellae, we now find that indistinct strands of

vitelline material connect the pre- and

posttesticular vitelline masses in some of the

paratype specimens. In S. robustum the dorsal

connections are conspicuous" .

HOSTS:

Acanthurus sandvicensis, Zebrasoma flavescens (Acanthuridae);

Chaetodon fremblii (Chaetodontidae); Stegastes fasciolatus

( = Pomacentrus jenkinsi) (Pomacentridae) .

RECORDS :

Pritchard and Manter (1961); Yamaguti (1970) ; Juarez-Arroyo and

Salgado-Maldonado (1989).

GEOGRAPHIC

DISTRIBUTION: Hawaii, Mexican Pacific

25 . Schikhobalotrema bivesiculum Nahhas and Cable, 1964

Fig. 59 Plate VIII

According to Nahhas and Cable ( 1964: 182)

"Schikhobalotrema bivesiculum differs from all

other species of the genus in its conspicuous

bipartite seminal vesicle. It resembles S. acutum

and S. adacutum in general topography and

although it has a longitudinal aperture in the

ventral sucker as in those species, the sucker

lacks posterolateral lobes. The bipartite seminal

vesicle with a thick anterior division in this

species may be of generic value but the species

is placed in Schikhobalotrema because others

showing gradations in that respect may exist. "

S. bivesiculum 's original description was based on six specimens from A.

saxatilis from the south shore of Jamaica. Nine specimens of this species from the same

host species were also reported by Nahhas and Carlson (1994:9) from the north shore

of Jamaica who added the following observations:

"the muscular (anterior thick part) of the seminal

vesicle is one to one and one-half length of the

pharynx and may be globular or cylindrical in

shape; a shon prostate duct is present but no

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5.5 Page 45

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prostate cells are seen; the genital atrium is

conspicuous but not muscular; the ovary is

usually anterior to testis but is dorsal to it in one

specimen and dorsal to the ventral sucker in

another. In the live material the excretory

vesicle seemed to reach the testis, level

depending on degree of contraction. The

aperture of the ventral sucker is a narrow

longitudinal slit in some but broadly so in

others. "

HOST:

Abudefduf saxatilis (Pomacentridae).

RECORDS :

Nahhas and Cable (1964); Nahhas and Carlson ( 1 994) .

GEOGRAPHIC

DISTRIBUTION: Jamaica.

26. Sthikhobalotrema elongatum Nahhas and Cable, 1964

Fig. 60 Plate VIII

According to Nahhas and Cable ( 1 964: 182)

" t he

most

distinctive

features

of

Schikhobalotrema elongatum are its long

hindbody with prominent cuticular rings, and its

well-developed bulb of prostatic ducts. In body

shape, S. elongatum is similar to several species.

S. acutum and S. adacutum have a ventral

sucker with a longitudinal aperture and lateral

lobes. S. obtusum lacks a prostatic vesicle; the

genital atrium is non-muscular and the ovary

close to the ventral sucker. S. pomacentri has an

equat0rial ventral sucker and S. kyphosi

(Manter, 1947) a lobed ovary. S. girellae

(Manter and Van Cleave, 1 95 1) is most like S.

elongatum but differs from that species in the

extent of the seminal vesicle, in having a long

tubular genital atrium and a more anterior

ovary. S. manteri Siddiqi and Cable, 1960,

differs in the distribution of the vitellaria,

position of the testis and posterior extent of the

uterus. S. robustum Pritchard and Manter, 1961 ,

is much larger , has a thin-walled genital atrium

and the genital pore on a finger-like projection. "

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5.6 Page 46

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HOSTS:

Mugil cephalus, M. curema (Mugilidae).

RECORDS:

Nahhas and Cable ( 1 964); Skinner ( 1 975).

GEOGRAPHIC

DISTRIBUTION: Jamaica, Florida.

27. Schikhobalotrema acanthuri Yamaguti, 1970

Fig. 61 Plate VIII

According to Yamaguti ( 1 970: 25)

"this species resembles Schikhobalotrema

obtusum (Linton, 19 10) , but differs from it in

the ovary being far posterior to the ventral

sucker and in the uterus not extending posterior

to the posterior end of the seminal vesicle which

reaches to the ovary. S. obtusum (Linton, 1910),

found by Pritchard and Manter ( 1 961) in

Acanthuros sandvicensis and other Acanthurus

species of Hawaii, probably belongs to the

present species. "

HOSTS:

Acanthurus sandvicensis, A. nigrofascus, Zebrasoma flavescens

(Acanthuridae) , Mugil liza (Mugilidae)

RECORDS :

Yamaguti (1970) , Fernandes and Goulart ( 1989)

GEOGRAPHIC

DISTRIBUTION : Hawaii; Praia de Copacabana, Rio de Janeiro State (Brazil)

28. Schikhobalotrema longivesiculatum Orecchia and Paggi , 1975

Fig. 62 Plate IX

According to Orecchia and Paggi ( 1 975 : 74), whose description is based on 1 1

specimens ,

"Schikhobalotrema longivesiculatum differs

from Schikhobalotrema obtusa (Linton, 1910)

Skrjabin and Guschanskaja, 1955, especially for

sucker ratio, lobed ovary, seminal vesicle coiled

and in larger size of eggs; from

SchikhobalotrelTUl pomacentri (Manter, 1937)

Skrjabin and Guschanskaja, 1955 for lobed

ovary, elongated seminal receptacle, smaller

vitelline follicles and coiled seminal vesicle;

from Schikhobalotrema sparisomae (Manter,

1 937) Skrjabin and Guschanskaja, 1955 for

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5.7 Page 47

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elongated seminal receptacle, coiled seminal

vesicle and extent of excretory vesicle. "

HOST:

Blennius sanguinolentus (Blenniidae)

RECORDS :

Orecchia and Paggi ( 1 975) .

GEOGRAPHIC

DISTRIBUTION: Gulf of Gaeta (Italy) .

29. Schkhobalotrema magnum Sknner, 1 975

Fig. 63 Plate IX

According to Skinner (1975: 328)

"the most distinctive features of S. magnum are

its large siz.e, comparatively small oral sucker,

ventral sucker, and eggs, extensive vitellaria,

large testis and lobed ovary, and the structure of

its terminal genitalia. S. magnum is similar to S.

.

kyphosi (Manter,

Tortugas, and S.

1 947) from Kyphosus sp. ,

sparisomae (Manter, 1937)

from Sparisoma sp. , also from Tortugas, in its

lobed ovary and large siz.e. S. magnum differs

from S. kyphosi in its larger testis, larger sucker

ratio, and less follicular vitellaria. It differs

from S. sparisomae in its smaller sucker ratio,

a shon cecum, sinuous seminal vesicle. and the

size of the eggs. In overall siz.e and proportions

S. magnum is most like S. robustum Pritchard

and Manter, 1 96 1 , from Hawaiian fishes. The

extension of the vitellaria, large siz.e, sinuous

seminal vesicle with a distal constriction, and

the presence of large prostatic cells are similar

in both species. S. robustum differs mainly in

having its genital pore on a finger-like

projection, the lack of a prostatic vesicle, and an

unlobed ovary. "

HOST:

Mugil cephalus (Mugilidae)

RECORD:

Skinner (1 975) .

GEOGRAPHIC

DISTRIBUTION: Biscayne Bay (Florida) .

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30. Schikhobalotrema solitaria Fernandes and Goulart, 1989

Fig 71 Plate X

According to Fernandes and Goulart (1989) who compared the single specimen

of their new species to the 19 species of Schikhobalotrema the most distinctive feature

of S. solitaria is the ratio of the oral sucker to the pharynx which is 1 : 1 . 1 whereas in

all the others it is 1 : 0. 3-0. 6.

HOST:

RECORDS :

GEOGRAPHIC

DISTRIBUTION:

Stephanolepis hispidus (Balistidae)

Fernandes and Goulart ( 1 989)

Praia de Copacabana, Rio de Janeiro State (Brazil)

3 1 . Pseudoschikhobalotrema heterocotylum (Nahsah ans Cable, 1964),

Yamaguti, 197 1

Fig. 69 Plate IX

SYNONYM: Sckikhobalotrema heterocotylum Nahhas and Cable, 1964

According to Nahhas and Cable ( 1 964 : 13)

"no haplosplanchnid has bene described as

having a ventral sucker with the tuberculated

lobes characteristic of this species. Most like it

in other respects is S. brachyurum (Manter,

1937) a paratype of which we have examined

and found to lack such lobes. It further differs

from S. heterocotylwn in having a different body

shape; S. glomerosum Pritchard and Manter,

1 961 , has a smaller ventral sucker, a

preacetabular ovary, more anterior testis and a

well-developed metraterm. "

P. heterocotylum was originally described from P. guacamaia from Cur�ao.

Four specimens were reported from S. croicensis from the nonh shore of Jamaica by

Nahhas and Carlson ( 1 994: 1 1) who stated

"The four large worms have an almost spherical

shape when studied alive. One was immature

and whitish in color, the other three were

mature with a brown-red coloration. All four

clearly showed the characteristic tuberculated

papillae or lobes of the ventral sucker

characteristic of this species.

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5.9 Page 49

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HOSTS:

Pseudoscarus guacamaia, Scarus croicensis (Scaridae).

RECORDS :

Nahhas and Cable ( 1964) ; Nahhas and Carlson ( 1994) .

GEOGRAPHIC

DISTRIBUTION: Cur�ao, Jamaica.

32. Haplosplanchnoides hemiramphi Nahhas and Cable, 1964

Fig. 65 Plate IX

According to Nahhas and Cable ( 1 964: 183)

"although certain other haplosplanchnids have

short hindbodies, their gonads are never anterior

to the ventral sucker except perhaps in

Schikhobalotrema glomerosum which Pritchard

and Manter ( 1961) described from two

specimens in poor condition. "

HOST:

Hemiramphus brasiliensis (Hemiramphidae)

RECORDS : . Nahhas and Cable ( 1 964) .

GEOGRAPHIC

DISTRIBUTION: Jamaica

33. Hymenocotta manteri Overstreet, 1969

Fig . 68 Plate IX

SYNONYM: Hymenocottoides manten· (Overstreet, 1969) Yamaguti , 197 1

According to Overstreet ( 1969: 133)

"Manter ( 1 96 1 : 67-69) erected the genus

Hymenocotta to accommodate a single species,

H. mulli Manter, 196 1 , which differs from all

other haplosplanchnids in having a cirrus sac

and a six-lobed disc, which replaces the oral

sucker. The present species is the second with a

disc , but it is not six-lobed, and a cirrus sac is

absent. What appears to be the cirrus sac is

weakly developed and not evident in all of Dr.

Manter's specimens of H. mulli from New

Caledonia. Pending further infonnation� the

present species is placed in Hymenocotta

because of the oral disc which, with the absence

of a well-developed bulb of prostatic duct,

distinguishes H. monteri from Schikhobalotrema

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5.10 Page 50

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elongatum Nahhas and Cable, 1964 and

otherwise similar species from the same host. "

Yamaguti ( 1 971) removed H. monteri from the genus Hymenocotta and erected

a new genus Hymenocottoides, based on two distinguishing characteristics of H.

manteri: absence of a cirrus sac and presence of a bulbous prostatic vesicle free in the

parenchyma.

The original description of this species was based on 16 whole mounts and three

sectioned specimens from M. cephalus, Biscayne Bay, Florida; H. manteri was

collected again by Overstreet ( 1 97 1) from the same host species from artificial ponds,

Price Lake in Rockefeller Wildlife Refuge, Grand Chenier, Louisiana, and waters

adjacent to Mississippi Sound, Mississippi, redescribed it and found it to have a cirrus

sac .

According to Skinner ( 1 975) , H. manteri was also found in the same host

species by Rawson in 1973 along the coast of Georgia. Tantalean et al. ( 1982) and

Tantalean et al. ( 1992) also reported this species from the Peruvian coast.

Fernandez and Bendezu ( 1986) did not observe a cirrus sac in their specimens

of H. manteri from San Marcos, but Bariega ( 1 987) reported the presence of a weak

cirrus sac in specimens from M. cephalus in Chile.

HOST:

Mugil cephalus Mugilidae

RECORDS :

Overstreet ( 1969, 1 97 1 ) ; Rawson in Skinner

( 1 975) ; Fernandez and Bendezu ( 1 986) ; Bariega ( 1 987).

GEOGRAPHIC

DISTRIBUTION: Biscayne Bay (Florida), Louisiana, Mississippi, Georgia, San

Marcos, Chile, Peru.

34. Prohaplosplanchnus diorchis Tang and Lin, 1978

Fig. 20 Plate IV

Prohaplosplanchnus diorchis, described from several specimens, is the only

member of the family Haplosplanchnidae with two testes.

HOSTS :

Mugil cephalus, Liza haematochilus.

RECORD :

Tang and Lin ( 1 978)

GEOGRAPHIC

DISTRIBUTION: Min River, Fujian, China.

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35 . Provitellotrema crenimugilis Pan, 1984

Fig. 64 Plate IX

Pan ( 1984) erected the genus Provitellotrema, for P. crenimugilis based on a

single spec imen, placed it in the subfamily Sch ikhobalotremat inae , compared it with

Schikhobalotrema not ing se veral spec ific differences be tween the two genera:

" the vitellar ia of Schikhobalotrema is well

developed, located at po ster ior end and sides of

body, whereas the v itellar ia of Provitellotrema

is div ided into two groups form ing an arch

between the phary nx and ventral sucker. The

ovary and testis of Schikhobalotrema are situated

at m idbody level; i n Provitellotrema the ovary

and testis are near po ster ior end of body. "

HOST:

Crenimugil crenilabis (M ugi l idae)

RECORD :

Pan (1984)

GEOGRAPHIC

DISTRIBUTION : C h ina.

36 . Neohaplosplanchnus ablennis Abdu l-Sal am and Khal il, 1987

Fig.70 Plate IX

According to Abd ul- Sal am and Khal il (1987:153) whose descr iption and

measurements were base d "on7 whole- mounts, 3 sets of sec t ioned speci mens and3

spec imens examined under the scanning elec tron m icrosc ope. "

"as the present spec imens cannot be a ssigned to

any of the ex isting genera of the fam ily

(Haplosplanchni dae) , a new genus is establi shed

for them. From Hymenocotta Manter 196 1 and

Hymenocottoides Yamagut i, 197 1 it differs i n

the presence of an oral sucker of the normal type

as opposed to a l obed disc. Fro m

Haplosplanchnoides N ahhas and C able, 1964 it

differs in the pre-equ ator ial po sit ion of the

ventral sucker instead of bei ng near the po sterior

extremity and in havi ng a shorter cec um not

reach ing the po steri or extremity. From

Haplosplanchnus Loo ss, 1902 and Laruea

Srivastava, 1939 , it differ s in hav ing an

extensive follicular vitel larium instead of an

ac ino us vi tel larium of l imited extent. From

Prohaplosplanchnus Tang and Li n, 1978 , it

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6.2 Page 52

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differs in having one testis and in the

arrangement and extent of the vitellarium. From

Schikhobalotrema Skrjabin and Guschanskaja,

1955, it differs in the general shape of the body,

in having a large ventral sucker with auricular

appendages and in having 'salivary ' glands.

From Provitellotrema Pan, 1984, it differs in the

pretesticular position of the ovary and the

extensive vitellarium. In fact the nearest genus

to these specimens is Pseudoschikhobalotrema

Yamaguti, 197 1 , a genus established for the

species originally reported as Schikhobalotrema

heterocotylum Nahhas and Cable, 1964, from

the intestine of Pseudoscarus guacamaia from

Cur�ao. Both species have appendages on the

ventral sucker and ' salivary ' glands in the

forebody which open on the ventral lip of the

oral sucker. However, the present specimens

differ from that genus in: ( 1 ) the elongate

instead of subspherical body; (2) the pre

equatorial position of the ventral sucker; (3)

having a ventral sucker with an elongate opening

bearing two auricular appendages on the

posterior end only instead of a transverse

opening provided with two appendages on the

anterior and posterior lips; (4) the position of

the testis, ovary and seminal receptacle; and (5)

the extent of the cecum and vitellarium. For

these reasons a new genus has to be erected to

accommodate these specimens for which the

name Neohaplosplanchnus is proposed because

the general shape of the body resembles species

of the genus Haplosplanchnus. "

The authors gave the following generic diagnosis:

"body elongate, fusiform with prominent

annulations posteriorly. Oral sucker subterminal,

its ventral lip with papilla bearing openings of

' salivary ' glands; pharynx well developed;

oesophagus short; caecum extending to mid

level of testis. Single testis at about middle of

hind-body; seminal vesicle long, slender; genital

pore median, pre-acetabular. Ovary submedian;

vitellarium with large follicles, extending on

each side of body from posterior level of

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oesophagus to posterior extremity . Eggs few,

operculate, large. Intestinal parasites of marine

teleosts. "

The authors distinguished the new genus from Schikhobalotrema by body shape ,

a large ventral sucker with auricular appendages, and the presence of salivary glands.

Additional characteristics cited by the authors include longitudinal acetabular opening

and cuticular annulations. Collectively such characteristics may justify this genus but

several species of Schikhobalotrema share individually these features. Many have

similar body shape (Plates VII and VIII) . Auricular appendages (acetabular papillae,

acetabular lobes) are characteristic of S. acutum (Manter, 1937) Skrj. and Gusch. ,

1955 , and S. adacutum (Manter, 1 937) Skrj . and Gusch. , 1955. These acetabular

appendages are often quite conspicuous in S. acutum, but poorly developed in S.

adacutum. These two species also have a longitudinal opening of the ventral sucker as

does S. bivesiculum Nahhas and Cable, 1964. S. bivesiculum, however, lacks auricular

appendages. The presence of salivary gland openings on the ventral lip of the oral

sucker is not unique to N. oblennis either. Abdul-Salam and Khalil ( 1 987) noted that

Overstet: et (1971) has drawn atnte tion to the fact that a number of species of the family

Haplosplanchnidae have sets of glands which release their products into the oral sucker.

Cuticular annulat•ons have been described for S. elongatum Nahhas and Cable, 1964

and therefore this characteristic is not unique to N. ablennis.

N. oblennis has a strong superficial resemblance to S. acutum, a species

common to many belonids and found in many parts of the world outside the Carribean

and Gulf of Mexico. This resemblance is evident in many of the characteristics cited

above, in addition to general body shape and topography of the reproductive organs.

It may be distinguished from S. acutum by the presence of cuticular annulations, more

conspicuous acetabular flaps, and more extensive vitellaria.

HOST:

Ablennes hians (Belonidae)

RECORDS:

Abdul-Salam and Khalil ( 1987).

· GEOGRAPHIC

DISTRIBUTION : Kuwaiti coast (Arabian Gulf).

37. Discocephalotrema kyphosi Machida, 1 993

Fig. 72 Plate X

According to Machida ( 1993:28) whose description is based on 5 specimens

recovered from the pyloric ceca

" This species resembles the members of the

genus Hymenocotta, H. mulli Manter, 1961 and

H. manteri Overstreet, 1 969, in the oral sucker

replaced by a lobed or flared oral disk, a long

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tubular seminal vesicle, and tubular vitellaria

extending far beyond the caecal termination. "

HOST:

Kyphosus cinerascens (Kyphosidae)

RECORDS :

Machida ( 1 993)

GEOGRAPHIC

DISTRIBUTION: Japan

The next species, described from 5 specimens, was placed in a new genus,

Neohaplosplanchnus, by Lu ( 1 995) who was unaware that such a generic name had

already been assigned to N. ablennis Abdul-Salam and Khalil, 1987, from Ablennes

hians. Lu's species N. cirrusaci neither belongs in Neohaplosplanchnus nor in any

other haplosplanchnid genus. Thus a new generic name, Parahaplosplanchnus, is

proposed.

38. Parahaplosplanchnus cirrusaci (Lu, 1995) n. comb.

Fig. 73 Plate X

SYNONYM : Neohaplosplanchnus cirrusaci Lu, 1 995

Lu ( 1995) distinguished his genus from Haplosplanchnus by

"having a cirrus sac containing a large internal

seminal vesicle, ejaculatory duct and a cirrus,

prepharynx absent, cecum only reaching to

ovary or not, the different position of genital

pore and vitellaria. "

HOST:

Engraulis japonica (Engraulidae)

SITE:

Intestine

RECORDS :

Lu ( 1 995)

GEOGRAPHIC

DISTRIBUTION: Guandong Province, China

Since the generic description appeared in Chinese a translation follows:

Parahaplosplanchnus n. gen!

Generic diagnosis: Haplosplanchnidae; Haplosplanchninae. Body small, rather obtuse

triangular, smoto h; anterior extremity in transverse almost equal to posterior extremity.

Oral sucker well-developed; Pharynx well developed; prepharynx absent; esophagus

long; Cecum may or may not reach ovary . Ventral sucker more or less elongated,

equatorial or preequatorial ; testis single, near posterior end, cirrus sac present

containing internal seminal vesicle, prostatic glands, ejaculatory duct and short cirrus.

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Genital pore about midway between pharynx and ventral sucker. Ovary median,

pretesticular, or anterodorsal to testis; seminal receptacle oval-shaped , situated between

ovary and testis. Vitell�a rather poorly developed, dorsal to uterus. Uterine coils

chiefly between ovarian complex and ventral sucker. Eggs large compared with the

small body , very few in number; miracidum without eyespots. Excretory vesicle Y-

shaped, arms reaching to posterior level of oral sucker. Parasitic in intestine of marine

fishes. Synonym: Neohaplosplanchnus nee Abdul-Salam and Khalil. Type species P.

cirrusaci n.comb.

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VIII. DISCUSSION

Yamaguti (1971) recognized or introduced the following subfamilies and their

genera: Haplosplanchninae (Haplosplanchnus, Laruea) , Schikhobalotrematinae

(Schikhobalotrema) , Haplosplanchnoidinae (Haplosplanchnoides) , Hymenocottinae

(Hym eno cotta ,

Hymenocottoides) and

Pseudoschikhobalotrematinae

(Pseudoschikhobalotrema). Several authors working with haplosplanchnids consider

Laruea a synonym of Haplosplanchnus, and Hymenocottoides congeneric with

Hymenocotta, which, if accepted ( and we do) , results in 5 monotypic subfamilies.

Yamaguti actecp ed or used the following features to create the subfamilies: the

oral sucker (a disk or the normal type); position of the ventral sucker (near posterior

extremity or far apart from the posterior end, its size and presence of acetabular

projections) ; location of the gonads (pre- or postacetabular) ; J1resence or absence of a

cirrus sac, and vitellaria (few, many and their distribution).

Since 1 97 1 , 5 other genera have bene described: Prohaplosplanchnus, Tang and

Lin, 1978 , Provitellotrema Pan 1984, Neohaplosplanchnus Abdul-Salam and Khalil

1 987, Discocephalotrema Machida 1993, and Neohaplosplanchnus Lu, 1 995

renamed, in this paper, Parahaplosplanchus.

Prohaplosplanchnus has many similarities to Haplosplanchnus, except for the

presence of 2 testes, including eggs with fully developed eye-spotted miracidia. It was

properly placed in subfamily Haplosplanchninae.

Provitellotrema, placed in subfamily Schikhobalotrematinae, is clearly related

to Haplosplanchninae except for the location of its vitelline follicles which are found

in l ateral fields between the ventral sucker and pharynx rather than in the ovarian

acetabular region.

Neohaplosplanchnus was placed in Pseudoschikhobalotrematinae; it was shown,

in remarks under its listing in this paper, that it has many characteristics individually

found in several species of SchikJwbalotrema.

Discocephalotrema was placed by Machida (1993) in a new subfamily,

Discocephalotrematinae. Machida recognized the similarity to Hymenocottinae based

on the presence of an oral disk rather than an oral sucker of the usual type; he

distinguished the new subfamily by the shape of that disk (flat compared with lobed or

flared oral disk, a bipartite rather than tubular seminal vesicle, and follicular instead

of tubular vitellaria that do not extend beyond the cecal termination) . Even though

Discocephalotrema is characterized by a hermaphroditic sac whereas Hymenocqtta has

a weakly developed cirrus sac, we prefer to place Discocephalotrema in

Hymenocottinae based on the nature of the oral sucker.

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Parahaplosplanchnus (Lu, 1995) resembles Haplosplanchnus in its vitelline

distribution and other characteristics except for the presence of a well developed cirrus

sac . A cirrus sac is,, usually considered a family characteristic . There are several

families, however, that are characteriz.ed by the presence or absence of a cirrus sac

(Sanguinicolidae, Angiodictyidae, Paramphistomidae, Gorgoridae, Cryptogonimidae) .

A cirrus sac is absent in many opecoelids but a few have a rudimentary one. The

haplosplanchnids may also be characterized by presence or absence of a cirrus sac .

We question the need for a subfamily to accommodate Pseudoschikhobalotrema

heterocotylum, a species which was originally placed in Schikhobalotrema but renamed

Pseudoschikhobalotrema by Yamaguti because of its subspherical body and a ventral

sucker with tuberculated lobes or papillae. Such a silbfamily may be justified if and

when other genera are found to have those two important characteristics. Until then we

prefer to place Pseudoschikhobalotrema in Schikhobalotrematinae.

In contrast with Pseudoschikhobalotrematinae, we recognize the validity of

Haplosplanchnoidinae as a monotypic subfamily characterized by the presence of a

ventral .sucker at the posterior end of the body and preacetabular gonads, features not

found in other haplosplanchnid genera.

Several investigators including Siddiqi and Cable ( 1960) and Pritchard and

Manter( l 961) have questioned the validity of Schikhobalotrema as distinct from

Haplosplanchnus, and by extension the validity of Schikhobalotrematinae. Sogandares

Bernal and Sogandares ( 1959), reduced Schikhobalotrema to a subgenus of

Haplosplanchnus. Their suggestion has not been accepted by others. When all species

in the 2 genera are taken into consideration, the only morphologic difference between

the two is the number, extent and distribution of the vitelline follicles. In

Haplosplanchnus, the vitellaria are few, poorly developed and confined to the ovario

acetabular zone; in Schikhobalotrema they are extensive, stretching from the posterior

or near posterior end of the body to the pharyngeal region in some, to the anterior or

posterior level of the ventral sucker in others; in some, the vitelline follicles are close

together, in others well separated from each other (Plates IV, VII-X) . H. bengalensis

Gupta and Puri 1 985 was described from a single specimen as having extensive

vitellaria; if such an argnar ement is confirmed , this species would be the link between

Haplosplanchnus and Schikhobalotrema. . The eggs of Haplosplanchnus contain

developed miracidia whereas those of Schikhobalotrema are not fully embryonated. The

miracidia of H. pachysomus swim and penetrate the snail host and its cercariae develop

in rediae which had bene produced in sporocysts. The eggs of Schikhobalotrema

require a period of embryonation in the envi ronment after discharge from the worm;

whether they hatch or are eaten by, or penetrate, the snail host, is not known. The

cercariae, presumably of H. acuta, develop in sporocysts (no redial stage) . We are not

certain that these life cycle patrte ns apply to all the species in the 2 genera or to the

other 5 related genera. Pritchard and Manter ( 1 961 : 191) questioned the validity of

Schikhobalotrematinae and suggested that

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" If two subfamilies are to be recognized here,

the distinguishing characters should be

embryonated or nonembryonated uterine eggs,

the extent of the vitellaria, and, perhaps, the

host (mullet or non-mullet). "

The addition of 5 genera, since then, rules out stage of development of the egg

and host as criteria. The most logical approach is to recogniz.e 2 subfamilies based on

the nature of the oral sucker: Hymenocottinae for Hymenocotta and Discocephalotrema

and Haplosplanchninae for the other 8 genera (T. H. Cribb - personal communication:

FMN . There is some justification, from a practical aspect, for having more than 2

subfamilies including retention of the subfamily Schikhobalotrematinae as distinct from

Haplosplanchninae at least for the time being.

Four of the 5 newer taxa show many similarities to Haplosplanchnus or

Schikhobalotrema and can be placed in the 2 respective subfamilies: : Prohap

lospalnchnus, Provitellotrema and Parahaplosplanchnus (Haplosplanchninae) ; and

Neohaplosplanchnus (Schikhobalotrematinae) . This leads us to the conclusion that the

10 genera can be accommodated in 4 subfamilies:

Haplosplanchninae:

Schikhobalotrematinae:

Haplosplanchnoidinae:

(Haplosplanchnus, Prohaplosplanchnus, Provitellotrema,

Parahaplosplanchnus)

( Schikhobalotrema,

Pseudoschikhobalotrema,

Neohaplosplanchnus)

(Haplosplanchnoides)

Hymenocottinae

(Hymenocotta, Discocephalotrema)

The family Haplosplanchnidae and its 4 subfamilies may be redefined as

follows:

HAPWSPLANCHNIDAE Poche, 1 926

Family diagnosis: Digenea. Body with smooth cuticle, often with well developed

cervical gland cells. Eye-spot pigment usually present. Oral sucker of the usual type

or disk-like; ventral sucker pedunculate or not, well developed, with or without

acetabular lobes. Prepharynx absent or short; pharynx conspicuous; ceca single.

Gonads pre- or postacetablu ar. Testes one or two. Cirrus sac present or absent; seminal

vesicle long, usually not differentiated from vas deferens; pars prostatica and prostate

cells well or poorly developed. Ovary pre- or paratesticular; seminal receptacle present:

Laurer' s canal present or absent; uterine coils between gonads and genital pore,

occasionally extending to near posterior end; vitellaria usually follicular, sometimes

acinous, exceptionally tubular. Genital pore preacetabular. Eggs large, fully

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embryonated or not. Excretory vesicle Y- or I-shaped. Intestinal parasites of marine

teleosts.

Subfamily Haplosplanchninae Skrj . and Gusch. 1955

Subfamily diagnosis: Haplosplanchnidae. Body usually elongate. Oral sucker of the

usual type. Ventral sucker in anterior half of body, rarely in midbody region, with or

without peduncle or acetabular lips. Cecum short, usually not extending posterior to

ovary. Gonads preacetabular. Testes usually one, sometimes 2 (Prohaplosplanchnus),

in posterior half of body; cirrus and cirrus sac usually absent, occasionally present

(Parahaplosplanchnus) . Ovary globular, median or. submedian globular, usually in

posterior half of body; vitellaria few, poorly developed, restricted to ovario-acetabular

zone or acetabulo-pharyngeal region (Provitellotrema) ; uterine coils chiefly between

ventral sucker and ovary, sometimes extending posterior to testis. Eggs embryonated

with fully developed miracidia in some, non-embryonated in others. Haplosplanchnus

Looss , 1902 (Type genus) ; other genera: Prohaplosplanchnus Tang and Lin, 1978;

Provitellotrema Pan 1984; Parahaplosplanchnus n.g. (Synonym: Neohaplosphlanchnus

Lu, 1995 , Nee Abdul-Salam and Khalil).

Subfamily Schikhobalotrematinae Skrj. and Gusch. , 1 955

Subfamily diagnosis: Haplosplanchnidae. Body usually elongate, rarely spherical

(Pseudoschikhobalotrema) , posterior end with annular rings in some. Oral sucker of

the usual type. Ventral sucker non-pedunculate, in anterior half or midbody region,

with or without acetabular lobes. Cecum not extending posterior to testis. Gonads post

pre- or paracetabular. Testis single usually in mid or posterior half of body, rarely in

acetabular region; cirrus and cirus sac absent. Ovary globular or lobed, pretesticular,

post-, pre- or par-acetabular; vitelline follicles numerous extending from near posterior

end of body to pharynx, anterior or posterior level of ventral sucker; uterine coils

preov�an. Eggs not embryonated . Schikhobalotrema Skrj. and Gusch. , 1955(Type

genus) ; other genera: Pseudoschikhobalotrema (Nahhas and Cable, 1964) ;

Neohaplosplanchnus Abdul-Salam and Khalil, 1987 .

Subfamily Haplosplanchnoidinae Yamaguti, 197 1

Subfamily diagnosis: Haplosplanchnidae. Body plump. Cuticle thick. Oral sucker of

usual type. Ventral sucker near posterior extremity without peduncle or acetabular

lobes. Cecum long extending to posterior extremity. Gonads preacetabular. cirrus sac

absent. Ovary pretesticular. Vitellaria follicular, extensive from posterior end of body

to prepharyngeal level. Haplosplanchnoides Nahhas and Cable, 1964 (Type genus).

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Subfamily Hymenocottinae Yamaguti, 197 1

Subfamily diagnosis: Haplosplanchnidae. Body elongate. Oral sucker replaced by a

disk or lobes. Cecum relatively long . Ventral sucker large in anterior hal f of body .

Testis single; cirrus sac present or absent. Ovary globular, pretesticula, close to testis.

Vitellaria tubular or follicular extending from post acetabular or ovarian level to

testicular region or farther posteriorly. Uterus well developed , short, restricted to area

between metraterm and testis or extending to near posterior end of cecum. Eggs with

undeveloped miracidia. Hymenocotta (Type genus) Manter, 196 1 ; Discocephalotrema

Machida, 1993 .

The following keys are proposed to distinguish among the subfamilies, genera, and

species of Haplosplanchnus and Schikhobalotrema.

KEY TO THE SUBFAMILIES OF HAPLOSPLANCHNIDA.E

l a.

Oral sucker modified to form lobes or disk. . . . . . . . Hymenocottinae

b.

Oral sucker of usual type . . . . . . . . . . . . . . . . . . . . . . . 2

2a.

Ventral sucker near posterior extremity; gonads . . . . . . . . . .

preacetabular. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Haplosplanchnoidinae.

b.

Ventral sucker far apart from posterior extremity ;

. . . . .

..

gonads par- Pre- or po stacetabular . . . . . . . . . . . . . . . . . . 3

3a.

Testes 1 or 2; cirrus sac present or absent; vitellaria follicular with

restricted distribution . . . . . . . . . . . . . . . Haplosplanchninae

b.

Testis single; cirrus sac absent; Vitellaria follicular, extensive,

extending from near posterior end of the body to the ventral sucker

or forebody . . . . . . . . . . . . . . . . . . . Schikhobalotrematinae

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KEY TO THE GENER A OF H APLOSPL ANCHNI DAE

l a.

Oral sucker disk-like . . . . . . . . . . . . . . . . . . . . . . . . . . . 2

b.

Oral sucker of normal shape . . . . . . . . . . . . . . . . . . . . . . 3

2a.

Oral sucker a lobed disk . . . . . . . . . . . . . . . . . Hymenocotta

b.

Oral sucker a flat disk . . . . . . . . . . . . . . Discocephalotrema

3a.

Vitelline follicles few with limited distribution in body; one or two

testes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4

b.

Vitelline follicles many with extensive distribution; one testis . 7

4a.

Two testes . . . . . . . . . . . . . . . . . . . . . Prohaplosplanchnus

b.

One testis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5

5a.

Cirrus sac present . . . . . . . . . . . . . Parahaplosplanchnus n. g.

b.

Cirrus sac absent . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6

6a.

Vitelline follicles in two lateral groups between ventral sucker and

pharynx . . . . . . . . . . . . . . . . . . . . . . . . . . Provitellotrema

b.

· Vitelline follicles between gonads and ventral sucker. . .. .. .. . . . . . ...

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .Haplosplanchnus

7a.

Ventral sucker near posterior end of body ; gonads preacetabular

. . . . . . . . . . . . . . . . . . . . . . . . . . . . Haplosplanchnoides

b.

Ventral sucker near midbody region or in forebody . . . . . . . 8

8a.

Body spherical; ventral sucker with two pairs of papillae, one

anterior, the other posterior . . . . . . . Pseudoschikhobalotrema

b.

Body elongate or somewhat ovoid; acetabular papillae present or

absent . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9

9a.

Vitellaria extending from posterior end of body to near anterior

level of ventral sucker; one pair of conspicuous acetabular papillae

present; hind body with prominent annulations posteriorly

. . . . . . . . . . . . . . . . . . . . . . . . . . . . Neohaplosplanchnus

b.

Vitellaria extensive from posterior end of body to variable levels

relevant to ventral sucker ; acetabular papillae usually absent,

rarely present; hind body rarely with posterior annulations. . . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Schikhobalotrema

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KEY TO THE SPECIES OF HAPLOSPLANCHNUS

l a.

Ventral sucker length greater than twice its width; muscular

acetabular lips present . . . . . . . . . . . . . . . . H. pachysomus

b.

Ventral sucker length less than twice its width; muscular acetabular

lips absent . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2

2a.

Uterus not extending posterior to testis . . . . . . . . . . . . . . . 3

b.

Uterus extending posterior to testis . . . . . . . . . . . . . . . . . . 4

3a.

Vitelline follicles few restricted to ovarioacetabular level

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . H. purii

b.

Vitelline follicles relatively extensive, distributed from ovario-

testicular level to near pharyngeal level . . . . . . . . . . . . . .H. bengalensis

4a.

Gonads immediately posterior to ventral sucker; prostate vesicle

bipartite . . . . . . . . . . . . . . . . . . . . . . . . . . . . H. vinodae

b.

Gonads some distance posterior to ventral sucker; prostate vesicle

un1part1te . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5

5a.

Testis nearer to posterior end than to ventral sucker; ventral sucker

at junction of anterior and midbody third . . . . . . . . H. mugilis

b.

Testis midway between ventral sucker and posterior end of body;

ventral sucker in anterior third of body . . . . . . . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . H. venezuelensis

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KEY TO THE SPECIES OF SCHIKHOBALOTREMA

la.

Ovary lobed . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2

b.

Ovary entire

6

2a.

Oral sucker larger than ventral sucker ( 1 : 0. 57- 0.67) ; testis in

middle third of body . . . . . . . . . . . . . . . . . . . . S. kyphosi

b.

Oral sucker smaller than or equal to ventral sucker; testis in

posterior half of body . . . . . . . . . . . . . . . . . . . . . . . . . . 3

3a.

Ventral sucker in midbody or posterior to midbody

level . . . . . . . . . . . . . . . . . . . . . . . . . . S. adbrachyurum

b.

Ventral sucker anterior to midbody . . . . . . . . . . . . . . . . . . 4

4a.

Ovary near posterior margin of ventral sucker; vitellaria relatively

large follicles . . . . . . . . . . . . . . . . . . . . . . . S. sparisomae

b.

Ovary some distance posterior to ventral sucker . . . . . . . . . 5

5a.

Seminal vesicle long and coiled, posterior to ventral sucker;

vitellaria relatively small and diffuse; cecum extending to

midtesticular level . . . . . . . . . . . . . . . . S . longivesiculatum

b.

Seminal vesicle long and straight posterior to ventral sucker;

vitellaria dense uninterrupted mass dorsally; cecum extending

posteriorly to level of ovary . . . . . . . . . . . . . . . S . magnum

6a.

Ventral sucker with longitudinal aperture . . . . . . . . . . . . . 7

b.

Ventral sucker with circular or transverse aperture . . . . . . . 9

7a.

Ventral sucker lacking acetabular lobes; seminal vesicle bipartite

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . S. bivesiculum

b.

Ventral sucker with acetabular lobes on its posterior border; seminal

vesicle unipartite . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8

8a.

Body sire usually less than one mm; ventral sucker lobes

inconspicuous; genital atrium (bulb) inconspicuous . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . S. adacutum

b.

Body sire larger than one mm ; ventral sucker with conspicuous

lobes; genital atrium (bulb) well-developed

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . S. acutum

9a.

Ventral sucker in anterior half of body . . . . . . . . . . . . . . 10

b.

Ventral sucker in midbody or posterior half of body . . . . . . 21

lOa.

Pharynx as large as oral sucker . . . . . . . . . . . . . . S. solitaria

b.

Pharynx smaller than oral sucker . . . . . . . . . . . . . . . . . 1 1

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1 1 a.

Testis nearer to ventral sucker than to posterior end of body; ovary

dorsal to or lateral to ventral sucker . . . . . . . . . . . . . . . . 12

b.

Testis in midbody or farther posteriorly ; ovary posterior to ventral

sucker . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14

1 2a.

Cirrus muscular; prostatic cells well developed; testis overlapping

ventral sucker dorsally . . . . . . . . . . . . . . . . . S. crassum

b.

Cirrus not muscular; prostrate cells poorly developed ; testis usually

posterior to ventral sucker . . . . . . . . . . . . . . . . . . . . . . 1 3

1 3a.

Testis less than twice the sire of ventral sucker . . . . . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . S. hawaiiensis

b.

Testis at least twice the sire of the ventral sucker

. . . . . . . . . . . . . . . . . . . . . . . . Schikhobalotrema sp. #1

l 4a.

Vitelline follicles extending from midtesticular region to posterior

level of ventral sucker; uterus extending posterior to testis. . . . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . S. mtltl eri

b.

Vitelline follicles extending from posterior end of body to at least

anterior level of ventral sucker; uterus not extending posterior to

testis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 5

1 5a.

Seminal receptacle globular . . . . . . . . . . . . . . . . . . . . . 1 6

b.

Seminal receptacle saccular . . . . . . . . . . . . . . . . . . . . . . 18

1 6a.

Vitelline follicles interrupted opposite testis . . . . . . . . . . . 1 7

b.

Vitelline follicles not interrupted opposite testis . . . . . . . . 1 9

17a.

Cecum extending half way between ventral sucker and testis; testis

in posterior third of hindbody; ovary near ventral sucker in anterior

half of body . . . . . . . . . . . . . . . . . . . . . . . . . S. acanthuri

b.

Cecum extending to level of anterior third of testis; testis half way

between ventral sucker and posterior end of body; ovary in

posterior third of body . . . . . . . . . . . . . . . . . . . . S. girellae

1 8a.

Seminal receptacle parallel to testis, with anterior-posterior

orientation; anterior part of seminal vesicle straight tube

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . S. obtusum

b.

Seminal receptacle dorsal to ovary and transversely elongate;

anterior part of seminal vesicle U-shaped . . . . S. southi n. sp .

1 9a.

Prostatic duct with well-developed bulb; prominent circular

cuticular rings posterior to ovary . . . . . . . . . . . S. elongatum

b.

Prostatic duct well-developed or not; cuticular rings absent . 20

58

7.5 Page 65

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20a.

b.

2la.

b.

22a.

b.

Cecum extending to midlevel of ovary; ovary midway between

testis and ventral sucker . . . . . . . . . Schikhobalotrema sp. #2

Cecum extending to level of anterior third of testis; ovary almost

contiguous with anterior level of testis. . . . . . . . . . S. robustum

Body subspherical ; testis postero-dorsal to and much larger than

ventral sucker . . . . . . . . . . . . . . . . . . . . . . S. glomerosum

Body elongate o r plump-like; testi s smaller than ventral sucker .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22

Vitellaria extending from posterior end of body laterally to anterior

level of pharynx; ventral sucker large relative to body size; prostatic

vesicle lacking; genital atrium not muscular; hindbody shorter than

forebody . . . . . . . . . . . . . . . . . . . . . . . . . S. brachyurum

Vitellaria not reaching pharyngeal level ; ventral sucker relatively

small compared to body size; prostatic vesicle well developed with

tall transparent cells; genital atrium muscular; hindbody almost

same length as forebody . . . . . . . . . . . . . . . . S. pomacentri

59

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x.

TABLE I

Egg size of Haplosplanchnus pachysomus-H. caudatus complex (µm)

H. pachysomus

Looss ( 1902)

Yamaguti ( 1 934)

Fischthal and Kuntz (1963)

Fares and Maillard ( 1 975)

Brglez and Paradiznik ( 1 988)

Garippa, Sanna and Guzzupoli

( 1 988)

Radujkovic, Orrechia and Paggi

( 1 989)

Gaevskaya and Dmitrieva ( 1 992)

Fijian specimens

57 X 26

5 1 X 27 (empty shells)

60-67 X 27-30 (miracidia )

45-54 x 25-29

49-70 x 20-50

45-75 x 25-50

40-55 x 20-35

40-50 x 30-35

39-57 x 18-30

45-67 x 27-35

H. caudatus

Srivastava ( 1 939)

Madhavi ( 1 979)

Bray (Pers. comm. : FMN)

38-40 x 19-23

39-43 x 18-22

42-48 x 26-28

H. straightum

lehan (J_9'1�)

H. orientalis

Gupta and Ahmad (1979)

"!><\\ x. \\_l

35-42 x 1 8-20

H. stunkardi

Gupta and Ahmad ( 1 979)

40-42 x 18-20

H. guptai

Ahmad ( 1985)

50-65 x 26-37

60

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Figure 1 .

Figure 2.

Figure 3.

Figure 4.

Figure 5.

PLATE I

Haplosplanchnus pachysomus from Mugil cephalus, Suva, Fiji.

H. pachysomus from Mugil cephalus, Suva, Fiji.

*Scale indicated near individual figures represents length in millimeters.

61

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PLATE I

\\

\\\\l\\

6

2

1

3

\\

6 \\ll

\\

5

62

j

�

I

4

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PLATE II

Figure 6.

Haplosplanchnus caudatus (Srivastava, 1939)from Liza vaigiensis, Puri,

Bay of Bengal.

Figure 7 .

H. caudatus of Madhavi ( 1979) from Mugil cephalus, Waltair coast, Bay

of Bengal .

·

Figure 8.

H. caudatus of Madhavi ( 1 979) from Mugil cephalus, Waltair coast, Bay

of Bengal .

Figure 9.

H. caudatus of Bray ( 1 984) from Mugil cephalus, Sodwana, Natal ,

South Africa.

Figure 10. · n. caudatus of Bray ( 1 984) from Mugil cephalus, Sodwana, Natal ,

South Africa.

63

7.10 Page 70

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PLATE II

9

7

6

10

8

64

8.1 Page 71

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PLATE III

Figure 1 1 .

Haplosplanchnus pachysomus Looss, 1 902 from Mugil cephalus,

Trieste.

Figure 12.

H. pachysomus of Fischthal and Kuntz (1963) from Mugil cephalus,

Egypt.

Figure 1 3 .

H. pachysomus o f Fischthal and Km:1tz (1963) from Mugil ramada,

Egypt.

Figure 14.

H. pachysomus of Fares and Maillard (1975) from Mugil cephalus,

Languedoc-Roussillon, French Mediterranean Coast.

Figure 15.

H. pachysomus of Garippa et al. (1988) from Mugil cephalus , " Is

Benas" , Oristano Providence, Italy .

65

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PLATE III

11

12

14

!:JI

\\•

I

15

66

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PLATE IV

Figure 16.

Haplosplanchnus straightum (Jehan, 1973) from Pseudosciaena

diacanthus Karachi , Arabian Sea.

Figure 17. H. orientalis Gupta and Ahmad , 1979 from Ilisha elongata ( =Pellona

. elongata) Puri , Orissa, Bay of Bengal.

Figure 1 8 .

H . stimko.rdi Gupta and Ahmad , 1 979 from Acanthurus sandvicensis,

Puri , Orissa, Bay of Bengal .

Figure 19.

H. guptai Ahmad, 1985 from Mugil cephalus, Panjim Coast, Goa,

Ind i a.

Figure 20.

Prohaplosplanchnus diorchis Tang and Lin, 1 978 from Liza

hematochilus Min River, Fujian, China.

Figure 2 1 . Schiklwbalotrema soUJhi n. sp. from Scarus rivulatus, Suva, Fiji.

Figure 22. Schikhobalotrema sp . # 1 from Scarus rivulatus, Suva, Fiji.

Figure 23 . Schiklwbalotrema sp . #2 from Acanthurus xanthopterus, Suva, Fiji.

67

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PLATE IV

18

23

17

68

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PLATE V

Figure 24. Haplosplanchnus purii from Liza vaigiensis, Suva, Fij i .

Figure 25. H. purii from Liza vaigiensis, Suva, Fiji.

Figure 26. H. purii from Liza vaigiensis, Suva, Fiji.

Figure 27. H. purii Srivastava, 1 939 from Liza vaigiensis, Puri , Orissa, Bay of

Bengal .

Figure 28 . H. purii of Madhavi , 1979 from Mugil cephalus, Waltair Coast, Bay of

Bengal .

Figure 29.

H. purii of Bray ( 1 984) from Liza tricuspidens, Swarthtops River

estuary, Algoa Bay , Cape Province, South Africa

69

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PLATE V

I

\\()

�

jj

0

I

26

24

29

28

27

70

8.7 Page 77

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PLATE VI

Figure 30.

Haplosplanchnus mugilis Nahhas and Cable, 1964 from Mugil curema,

Cura�ao .

Figure 3 1 .

H. bivi tellosus Zhukov, 197 1 from Mugil soiuy, Poyset Bay , Sea of

Japan and Liao Ho River, Yellow Sea.

Figure 32.

H. cuneatus Tang and Lin, 1978 from Mugil cephalus, Min River,

Fujian, China.

Figure 33.

H. elongatus Tang and Lin, 1978 from Mugil cephalus, Min River,

Fujian, China.

Figure 34.

H. indicus Gupta and Ahmad , 1979 from Liza vaigiensis, Puri , Orissa,

Bay of Bengal.

Figure 35 .

H. venezuelensis Fischthal and Nasir, 1974 from Antennarius

multiocellatus, Los Roques Islands, Venezuela.

Figure 3�.

H. otolithi Gupta and Ahmad, 1979 from Otolithus ruber, Puri, Orissa,

Bay of Bengal .

Figure 37.

H. bengalensis Gupta and Puri , 1985 from Acanthurus sandvicensis,

Puri , Orissa, Bay of Bengal .

Figure 38.

H. vinodae Ahmad , 1985 from Mugil cephalus, Panjim Coast, Goa,

India.

71

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PLATE VI

1

J

I

32

37

38

30

35

\\

'6

\\

36

31

72

8.9 Page 79

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PLATE VII

Figure 39.

Schikhobalotrema acutum of Manter (1937) from Tylosurus raphidoma,

Tortugas, Florida.

Figure 40.

S. acutum of Siddiqi and Cable ( 1 960) from Strongylura sp. , Punta

Arenas, Puerto Rico.

Figure 4 1 . S. acutum of Madhavi ( 1979) from Tylosurus crocodilus, Waltair Coast,

Bay of Bengal .

Figure. 42. S. acutum of Kohn and Fernandes ( 1982) from Strongylura marina,

, Angra dos Reis, Rio de Janeiro, Brazil.

Figure 43 . S. obtusum of Manter ( 1937) from Acanthurus coeruleus, Tortugas,

Florida.

Figure 44. S. obtusum of Siddiqi and Cable (1960) from Acanthurus bahianus,

Mona Island, Puerto Rico.

Figure 45.

S. adacutum (Manter, 1937) from Halichoeres bivittatus, Tortugas,

Florida.

Figure 46. S. brachyurum (Manter, 1 937) from Sparisoma spinidens, Tortugas,

Florida.

Figure 47. S. pomacentri. (Manter, 1937) from Pomacentrus leucostictus, Tortugas,

Florida.

Figure 48. S. pomacentri. (Manter, 1937) from Pomacentrus leucostictus, Tortugas,

Florida.

Figure 49. S. pomacentri of Siddiqi and Cable ( 1 960) from Pomacentrus juscus,

Punta Arenas, Puerto Rico.

Figure 50. S. sparisomae (Manter, 1937) from Sparisoma jlavescens, Tortugas,

Florida.

73

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PLATE VII

\\

39

"'

6

\\

42

1

';t

l

45

49

\\

.c..

\\

74

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PLATE VIII

Figure 5 1 .

Schikhobalotrema f.y. phosi (Manter, 1947) from Kyphosus incisor,

Tortugas, Florida.

Figure 52.

S. girellae (Manter and Van Cleave, 1 95 1 ) from Gire/la nigricans, La

Jolla, California.

Figure 53 .

S. adbrachyura Siddiqi and Cable, 1 960 from Sparisoma sp. , Mona

Island, Puerto Rico.

Figure 54. · S. rrzanteri Siddiqi and Cable, 1 960 from a "reef fish with a collar" ,

Punta Arenas, Puerto Rico.

Figure 55 .

S. crassum Pritchard and Manter. 1 961 from Stegastes fasciolatus ( =

Pomacentrus jenkinsi), Hawaii.

Figure 56. S. glomerosum Pritchard and Manter, 1 961 from Acanthurus

sandvicensis , Hawaii.

Figure 57 . S. hawaiiensis Pritchard and Manter, 1961 from Ctenochaetus strigosus,

Hawai i .

Figure 58.

S. robustum Pritchard and Manter, 1 961 from Stegastes fasciolatus ( =

Pomacentrus jenkinsi), Hawaii.

Figure 59. S. bivesiculum Nahhas and Cable, 1 964 from Abudefduf saxatilis,

Jamaica.

Figure 60.

S. elongatus Nahhas and Cable, 1964 from Mugil cephalus, Cur�ao and

Jamaica.

Figure 61 . S. acanthuri Yamaguti, 1 970 from Acanthurus sandvicensis, Hawaii.

75

9.2 Page 82

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PLATE VIII

J

"'

()

1

51

""T

C)

l

53

I

o\\ll '

\\

57

59

52

I

":l-

0

\\

54

T

lo

�

1

55

56

58

76

9.3 Page 83

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PLATE IX

Figure 62. Schikhobalotrema longivesiculatum Orecchia and Paggi, 1 975 from

Blennius sanguinolentus, the Gulf of Gaeta, Italy.

Figure 63 . S. magnum Skinner, 1975 from Mugil cephalus, Biscayne Bay , Florida.

Figure 64. Provitellotrema crenimugilis Pan, 1984 from Crenimugil crenilabis,

China.

Figure 65. Haplosplanchnoides hemiramphi Nahhas and Cable, 1 964 from

Hemiramphus brasiliensis, Jamaica.

Figure 66. Hymenocotta mulli Manter, 1961 from Liza vaigiensis, Suva, Fiji.

Figure 67. H. mulli Manter, 1 961 from an unknown mullet, Fiji.

Figure 68 . H. manteri Overstreet, 1969 from Mugil cephalus, Biscayne Bay,

Florida.

Figure 69.

Pseudoschikhobalotrema heterocotylum (Nahhas and Cable, 1 964) from

Pseudoscarus guacamaya, Curacao.

Figure 70. Neohaplosplanchnus ablennis Abdul-Salam and Khalil , 1 987 from

Ablennes hians, Kuwaiti coast, Arabian Gulf.

77

9.4 Page 84

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PLATE IX

I

o'Y

./

64

I/)

ti

1

tNi

l

68

78

9.5 Page 85

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PLATE X

Figure 7 1 . Schikhobalotrema solitaria Fernandes and Goulart, 1 989 from

Stephanolepis hispidus, Brazil.

Figure 72. Discocephalotrema kyphosi Machida, 1 993 from Kyphosus cinerascens

from Japan.

Figure 73. Parahaplosplanchnus cirrusaci (Lu, 1 995) from Engraulis japonica

from China.

79

9.6 Page 86

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PLATE X

71

73

72

80

9.7 Page 87

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XII . LITERATURE CITED

Abdul-Salam, J. and Khalil, L. F. 1 987. Two digeneans from the needlefish Ablennes

hians in Kuwait and the description of a new genus and species

Neohaplosplanchnus ablennis (Haplosplanchnidae) . Syst. Parasit. 10: 149- 1 58 .

___ and Sreelatha, B . N . S . 1 995. Studies o n cercariae from the Kuwait Bay. VI.

Description and surface topography of Cercaria kuwaitae VI sp. n.

(Trematoda: Haplosplanchnidae) . Korean Jo'!-'· Parasit. 33 : 147- 153.

Ahmad, J. 1 985. Studies on digenetic trematodes of marine fishes from the Arabian

Sea, off the Panjim Coast, Goa, India. Part 48. Revista Iberica Parasitologia.

45: 185- 194.

Amin, 0. M . and Nahhas, F. M. 1994. Acanthocephala of Marine Fishes off Fiji

. Islands, with descriptions of Filisoma longcementglandatus n. sp. ,

Neorhadinorhynchus macrospinosus n. sp. (Cavisomidae), and gravid females

of Rhadinorhynchus johnstoni (Rhadinorhynchidae) ; and keys to species of the

genera Filisoma and Neorhadinorhynchus. Jour. Parasit. 80: 768-774.

Bariega, J. B. 1987. The parasites of the " Lisa" Mugil cephalus L. in Chile:

Systematic and populations features (Perciformes: Mugilidae) . Gayana,

Zoologica. 5 1 : 3-58.

Bray , R. A. 1984. Some helminth parasites of marine fishes and cephalopods of South

Africa: Aspidogastrea and the digenean families Bucephalidae,

Haplosplanchnidae, Mesometridae and Fellodistomidae. Jour. Natur. History .

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Brglez; J. and Paradiznik, V. 1988. Trematodes: Saccocoelium tensum Looss, 1 902

and Haplosplanchnus pachysomus (Eysenhardt, 1829) Looss, 1 902 in Mugil

from the Northern Adriatic. Zb. biotechn. fak. Univ. E. Kardelja, Vet. 25: 45-

51.

Caballero y C . E. , Bravo-Hollis, M. , Grocott, R. G . 1953. Helmintos de la

Republica de Panama. VII . Descripcion de algunos trematodos de peces

marinas. Anales Inst. Biol. Mexico. 24: 97- 1 36.

Cable, R. M. 1954. Studies on marine digenetic trematodes of Puerto Rico. The life

cycle in the family Haplosplanchnidae. Jour. Parasit. 40: 7 1 -76.

Cribb, T. H. , Bray, R. A. , and Barker, S. C. 1994. Bivesiculidae and Haplos

planchnidae (Digenea) from fishes of the southern Great Barrier Reef,

Australia. Syst. Parasit. 28: 8 1 -97.

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Durio , W. 0. and Manter, H. W. 1968. Some digenetic trematodes of marine fishes

of New Caledonia. I. Bucephalidae, Monorchiidae, and some smaller families.

Proc. Helm. Soc. Washington. 35: 143- 153.

Dyer, W. G. , Williams, E. H . and Bunkley-Williams, L. 1 991 . Schikhobalotrema

pomacentri (Digenea) in Microspathodon chrysurus (Osteichthyes) from Puerto

Rico. Trans. Illinois State Acad. Sci. 84: 1 5 1 - 153 .

, and

1992. Homalometron

---

dowgialloi sp. n. (Homalometridae) from Haemulon flavoliniatum and

additional records of digenetic trematodes of marine fishes in the West Indies.

lour. Helm. Soc. Washington. 59: 182-189.

Ezz El-Dien, N. M . , Abdel-Rahman, M . S . , Fahmy, M. M. , El-Gawady , H. M . A . ,

and Imam, E. A. E. 1990. Seven marine fish species as new hosts for helminth

parasites in Egypt. lour. Egyptian Vet. Med. Assoc. 50: 5 1 9-525.

Fares, A. and MaiHard, C. 1975. Cycle evolulif a Haplosplanchnus pachysomas

(Eysenhardt, 1829) Loso s, 1902, (Trematoda, Haplosplanchnidae) Parasite de

mugilides (Teleostei) . Bull. Mus. Natioool Hist. Nat. Series 3 , 3 12: 837-844,

Zool. 2 1 9.

Fayek, S . A . , Amer, 0. H . and Ahmed, N . E. 1 990. Some fish trematodes from the

Mediterranean Sea. Vet. Med. lour. , Giz.a. 38: 429-439.

Fernandez, J. G. and Bendem, L. S. 1 986. Hymenocotta manteri Overstreet, 1 969

(Trematoda: Digenea) endoparasito de Mugil cephalus Linnaeus, 1 758. Revista

de Ciencias Universidad Nacioool Mayor de San Marcos. 74: 58-62.

Fernandes, B. M . M . and Goulart M . B. 1 989. Schikobalotrema solitaria and S.

acanthuriYamaguti, 1 970 (Haplosplanchnidae: Digenea) in Brazilian marine

fishes. Mem.lnst. Oswaldo Cruz, Rio de Janeiro. 84, Supl. IV: 1 89- 192.

Fischthal, J. H. 1977. Some Digenetic Trematodes of Marine Fishes from the Barrier

Reef and Reef Lagoon of Beliz.e. Zoo/. Ser. 6:8 1 -88.

, and Kuntz, R. E. , 1 963 . Trematode parasites of fishes from Egypt.

---

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1 9 : 9 1 -98.

, and Nasir, P. , 1974. Some digenetic trematodes from freshwater and

---

marine fishes of Venezuela. Norwegian lour. Zoo/. 22: 7 1 -80.

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Gaevskaya, A. V. , and Dmitrieva, E. V. 1992. Haplosplanchnus pachysomus

(Trematoda: HapJosplanchnidae) - parasite of Black Sea mullets. Parazitologiya.

26: 385-388. Instit. Bio. Southern Seas, Ukrainian Academy of Sciences,

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Garippa, G. , Sanna, E. and Cuzpzu oli , G. F. 1 988. Segnalazione di Haplosplanchnus

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Gupta, V. and Ahmad, J. 1979. Digenetic trematodes of marine fishes. VIII. On four

new species of the genus Haplosplanchnus LOoss, 1 902 from marine fishes of

Puri , Orissa. Helminthologia 1 6: 1 85- 1 93.

___ and Puri, M . 1 985. On some trematode parasites from marine fishes of

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Hafeezullah, M. 1 97 1 . On some new and known digenetic trematodes from marine

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Juarez-Arroyo, J. and Salgado-Maldonado, G. 1989. Helmintos de la "Lisa" Mugil

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(HaplospJanchnidae) trematodes of marine fishes in Brazil. Anna/es Parasit.

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Lester, R. J . G. and Sewell, K. B. 1 989. Checklist of parasites from Heron Island,

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Linton, E. 1910. Helminth fauna of the Dry Tortugas. II. Trematodes. Carnegie Inst.

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Lu , J. Y. 1 995. Notes on digenetic trematodes parasitic in fishes near shallow sea in

Guandong Province, China. III. Three new species, two new genera and one

new subfamily of Digenea. Acta Zoto axonomica Sinica 20: 1 4 1 - 1 52.

Machida, M. 1993. Trematodes from kyphosid fishes in Japanese and adjacent waters.

Bull. Nat. Sci. Mus. , Ser. A, 19:27-36.

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Madhavi, R. 1 979. Digenetic trematodes from marine fishes of Waltair Coast, Bay of

Bengal. Families Haplosplanchnidae and Haploporidae. Rivista Parassit.

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Manter, H. W. , 193 1 . Further studies on trematodes of Tortugas fishes. Carnegie Inst.

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1 937 . The status of the tremadode genus Deradena Linton with a

description of six species of Haplosplonchnus Looss (Trematoda) . Rabot.

Gel 'mint. , Skrjabin (Skrjabin Jubilee Vol .) 381 -387.

1 940. Digenetic trematodes of fishes from the Galapagos Islands

and the neighboring Pacific. Rep. Allan Hancock Pac. Exp. 2: 329-497.

1947. The digenetic trematodes of marine fishes of Tortugas, Florida.

The American Midland Naturalist. 3 8 : 324-326.

1953 . Two new species of Prosorhynchinae (Trematoda:

---

Gasterostomata) from the Fiji Islands. Thapar Commemorative Volume. Studies

from the Dept. of'Zool. , University ofNebraska. No. 263.

1 961 . Studies on digenetic trematodes of fishes of Fiji. I. Families

Haplosplanchnidae, Bivesiculidae, and Hemiuridae. Proc. Helm. Soc.

Washington . 28 : 67-74.

1963a. Studies on digenetic trematodes of fishes of Fiji . II. Families

Lepocreadiidae, Opistholebetidae, and Opecoelidae. Jour. Parasit. 49: 99-1 1 3 .

1963b. Studies on digenetic trematodes of fishes of Fiji. III. Families

---

Acanthocolpidae, Fellodistomatidae, and Cryptogonimidae. Jour. Parasit.

49: 443-450.

1963c. Studies on digenetic trematodes of fishes of Fiji. IV. Families

---

Haploporidae, Angiodictyidae, Monorchiidae and Bucephalidae. Proc. Helm.

Soc. Washington . 30: 224-232.

___ and Prince, D. F. 1953. Some monogenetic trematodes of marine

fishes from Fiji. Proc. Helm. Soc. Washington. 20: 105- 1 12.

and ___ Van Cleave, H. J. 1 95 1 . Some digenetic trematodes including

eight new species from marine fishes of La Jolla, California. Proc. U. S. Nat.

Mus. 10 1 : 3 15-340.

Mehra, H. R. 1 980. The fauna of India and adjacent countries. Platyhelminths Vol.

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