A review of the Apocreadiidae Skrjabin, 1942 (Trematoda: Digenea) anddescription of Australian species
T. H. Cribb1 & R. A. Bray2
1Department of Microbiology & Parasitology, The University of Queensland, Brisbane, Q4072, Australia2Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK
Accepted for publication 30th June, 1998
Abstract
The Apocreadiidae is reviewed and is considered to include genera recognised previously within the familiesApocreadiidae, Homalometridae, Schistorchiidae, Sphincterostomatidae and Trematobrienidae. Key features ofthe family are extensive vitelline follicles, eye-spot pigment dispersed in forebody, I-shaped excretory vesicle, nocirrus-sac and genital pore opening immediately anterior to the ventral sucker (usually) or immediately posteriorto it (PostporusManter, 1949). Three subfamilies and 18 genera are recognised within the Apocreadiidae. TheApocreadiinae comprisesHomalometronStafford, 1904 (new syn.BarbulostomumRamsey, 1965),Callohelmisn. g.,ChoanoderaManter, 1940,CrassicutisManter, 1936,DactylotremaBravo-Hollis & Manter, 1957,Marsu-pioacetabulumYamaguti, 1952,MicrocreadiumSimer, 1929,MyzotusManter, 1940,NeoapocreadiumSiddiqi &Cable, 1960,NeomegasolenaSiddiqi & Cable, 1960,PancreadiumManter, 1954,ProcaudotestisSzidat, 1954 andTrematobrienDollfus, 1950. The Schistorchiinae comprisesSchistorchisLühe, 1906,SphincterostomaYamaguti,1937,SphincteristomumOshmarin, Mamaev & Parukhin, 1961 andMegacreadiumNagaty, 1956. The Postporinaecomprises onlyPostporus. A key to subfamilies and genera of the Apocreadiidae is provided. It is argued thatthere is no convincing basis for the recognition of the genusApocreadiumManter, 1937 and all its constituentspecies are combined withHomalometron. The following new combinations are proposed for species previouslyrecognised withinApocreadium: Homalometron balistis(Manter, 1947),H. caballeroi (Bravo-Hollis, 1953),H. cryptum(Overstreet, 1969),H. longisinosum(Manter, 1937),H. manteri(Overstreet, 1970),H. mexicanum(Manter, 1937) andH. vinodae(Ahmad, 1985).Apocreadium uroproctoferumSogandares-Bernal, 1959 is foundto lack a uroproct and is made a synonym ofH. mexicanum. Homalometron verrunculinom. nov. is proposed toreplace the secondarily pre-occupiedH. caballeroiLamothe-Argumedo, 1965.Barbulostomumis made a synonymof HomalometronandH. cupuloris(Ramsey, 1965) n. comb. is proposed.Neochoanoderais made a synonymof ChoanoderaandChoanodera ghanensis(Fischthal & Thomas, 1970) n. comb. is proposed. Species withinthe Apocreadiinae and Postporinae are reviewed and the following are recorded or described from Australianfishes:Homalometron wrightaen. sp. fromAchlyopa nigra(Macleay),H. synagris(Yamaguti, 1953) n. comb.from Scolopsis monogramma(Cuvier), H. stradbrokensisn. sp. fromGerres subfasciatusCuvier, Marsupioac-etabulum opallioderman. sp. fromG. subfasciatus, Neoapocreadium karwarensis(Hafeezullah, 1970) n. comb.from G. subfasciatus, N. splendensn. sp. fromS. monogrammaandCallohelmis pichelinaen. g., n. sp. fromHemigymnus melapterus(Bloch),H. fasciatus(Bloch),Stethojulis bandanensis(Bleeker) andChoerodon venustus(De Vis).Callohelmisis recognised by the combination of absence of tegumental spines, caeca terminating midwaybetween the testes and posterior end of body, ventral sucker enclosed in a tegumental pouch, prominent musclesradiating through the body from the ventral sucker, vitelline follicles not extending into the forebody, and a veryshort excretory vesicle that opens ventrally. New combinations for species previously recognised withinCrassicutisare proposed as follows:Neoapocreadium caranxi(Bilqees, 1976) n. comb.,N. gerridis(Nahhas & Cable, 1964)n. comb.,N. imtiazi (Ahmad, 1984) n. comb. andN. marina(Manter, 1947) n. comb. The host-specificity andzoogeography of the Apocreadiinae are considered.
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Introduction
The Apocreadiidae Skrjabin, 1942 is one of thesmaller families of digenean trematodes of fishes.Species occur in the intestines of marine, brackishand freshwater fishes. In the present study we re-port seven species referable to the subfamily Apoc-readiinae within the Apocreadiidae. Of these five arenew. This significant collection created the opportu-nity to review this group of trematodes. To do thiswe have found it necessary to revise the structure ofthe family. A revision of the Schistorchiinae Yam-aguti, 1942, which we recognise as a subfamily of theApocreadiidae is to follow as a later contribution.
Materials and methods
Trematodes were collected by the authors fromfreshly-killed fish hosts and were fixed by pipettingthem into nearly boiling 5% formalin or saline orin cold Berland’s fluid. All specimens were storedin 5% formalin. Whole-mounts were stained withMayer’s haemalum, cleared with methyl salicylate andmounted in Canada balsam. Specimens for sectioningwere embedded in paraffin, cut at 7µm, stained withhaematoxylin and eosin, and mounted in Canada bal-sam or DPX. Drawings were made with the aid of adrawing tube. Measurements are quoted as the rangewith the mean in parentheses and are in micrometres.The following abbreviations are used: BM(NH), TheNatural History Museum, London; QM, QueenslandMuseum, Brisbane.
Taxonomy
The Apocreadiidae, as we conceive it here, is a fam-ily of ‘typical’ digeneans found in the intestines ofmarine, brackish and freshwater fishes. The family istypical in that it has oral and ventral suckers, a phar-ynx, two intestinal caeca and a generally unremarkablereproductive system. The family has been caught upin the ‘allocreadiid problem’, i.e., the progressive tax-onomic disentangling of many such typical digeneansas information about morphology and life-cycles be-comes available and better understood. Many authorshave contributed to this disentangling, which involvesthe Acanthocolpidae, Allocreadiidae, Apocreadiidae,Deropristiidae, Enenteridae, Homalometridae, Lep-ocreadiidae, Opecoelidae, Pleorchiidae, Schistorchi-idae and other families.
The Apocreadiinae was established by Skrjabin(1942) forApocreadiumManter, 1937 as a subfamilyof the Allocreadiinae. Yamaguti (1958) subsequentlyrecognised the group at the family level. Yamagutialso created the Myzotinae within the Apocreadiidaefor MyzotusManter, 1940 andMarsupioacetabulumYamaguti, 1952. At present five genera are gen-erally recognised within this family (Apocreadium,ChoanoderaManter, 1940,NeoapocreadiumSiddiqi& Cable, 1960,NeochoanoderaFischthal & Thomas,1970 andNeomegasolenaSiddiqi & Cable, 1960).The family is essentially similar to other families dis-cussed below but is distinguished by the presence oflymphatic vessels (although these have not been re-ported in all species referred to this family) which areapparently absent in all the related forms discussed be-low. Although the Apocreadiidae has been recognisedwidely, Overstreet (1970) placedApocreadiumin theHomalometrinae which he considered a subfamily ofthe Lepocreadiidae.
The concept of the family Homalometridae isbased on the genusHomalometronStafford, 1904.The Homalometrinae was proposed by Cable & Hun-ninen (1942) as a subfamily of the Lepocreadiidae,and includedHomalometron, MicrocreadiumSimer,1929,CrassicutisManter, 1936 andMyzotus. Withinthe Lepocreadiidae, Cable & Hunninen (1942) char-acterised the subfamily (most importantly) in termsof the median genital pore immediately anterior tothe ventral sucker and the lack of a cirrus-sac. Re-lationship with lepocreadiidssensu lato is estab-lished by general morphological similarity and bysimilarity of the life-cycle stages ofHomalometronpallidum Stafford, 1904,H. armatum(MacCallum,1895),Microcreadium parvumSimer, 1929 andCras-sicutis cichlasomaeManter, 1936 (see Hopkins, 1937;Stunkard, 1964; Scholz, Pech-Ek, & Rodríguez-Canul, 1995) to those of lepocreadiidssensu stricto.Yamaguti (1971) raised the subfamily to family leveland included the genera recognised by Cable & Hun-ninen (1942) and addedDactylotremaBravo-Hollis &Manter, 1957,BarbulostomumRamsey, 1965,Pan-creadiumManter, 1954,MarsupioacetabulumYam-aguti, 1952 andPostporusManter, 1949. The addi-tion of Postporusrequired amendation of the familyto include forms with the genital pore immediatelyposterior to the ventral sucker.
Yamaguti (1942) proposed the Schistorchiidae toinclude the generaSchistorchisLühe, 1906,Apocre-adiumManter, 1937 andChoanoderaManter, 1940.Later (Yamaguti, 1958), he movedApocreadiumand
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Choanoderato the Apocreadiidae.Schistorchissharescharacteristics with apocreadiids and homalometrids,except for multiple testes and an oral sucker thathas a distinctive sphincter at its aperture. A sec-ond genus,MegacreadiumNagaty, 1956, is presentlyrecognised within this family. Hanson (1953) arguedconvincingly thatSchistorchisshould be included inthe Homalometrinae, as defined by Cable & Hunninen(1942).
The Sphincterostomatidae was proposed by Yam-aguti (1958) as a family resembling the Opecoelidaein some respects. Two genera,SphincterostomaYam-aguti, 1937 andSphincteristomumOshmarin, Mamaev& Parukhin, 1961 (syn.LobatotremaManter, 1963),are now recognised within this family. These generaare characterised by a semicircular patch of musclein the oral sucker ventral and lateral to the openingof the mouth and by the lack of a cirrus-sac. Theyare further characterised by having the caeca open tothe exterior. Nagaty (1956) recognised the similaritybetween his new genusMegacreadiumand Sphinc-terostomaand included it in the Sphincterostomatidae.Howell (1966) pointed out that the lack of a cirrus-sacin the Sphincterostomatinae would allow it to be incor-porated in the Homalometrinae, which he recognisedas one of only two subfamilies of the Lepocreadiidae.Yamaguti (1971) recognised the Sphincterostomatinaeas a subfamily of the Lepocreadiidae. Gibson & Bray(1982) proposed thatSphincterostomaandSphincter-istomummight be associated withCadenatellaandJeancadenatiain the Cadenatellinae Gibson & Bray,1982, a subfamily of the Enenteridae. However, weconclude thatCadenatellaand Jeancadenatiaforma distinct group withEnenterumLinton, 1910. Thethree genera are generally similar, especially in thesharing of muscular processes on the oral sucker andare almost exclusively parasites of kyphosid fishes.Although Cadenatellaand Jeancadenatiaevidentlyhave reduced or absent cirrus-sacs, this seems likelyto be a development separate from that seen for theother forms considered here. In this study we havefound thatSchistorchis, Megacreadium, Sphincteros-toma and Sphincteristomumshare the characteristicof a distinctive patch of circular muscle around theaperture of the oral sucker which appears a complex,derived character that can be used to unite these generaconvincingly.
Dollfus (1950) erected a new family, the Trema-tobrienidae, forTrematobrien haplochromiosDollfus,1950. Manter (1962) re-examined and refigured thespecimens and concluded that the genus could be in-
cluded within the Homalometrinae. Ramsey (1965)disagreed and considered it perhaps closer to theOpecoelidae. Yamaguti (1971) recognised a subfamilywithin the Lepocreadiidae for this species.
Skrjabin & Koval (1960) erected a new subfam-ily within the Lepocreadiidae, the Marsupioacetabu-linae, forMarsupioacetabulum.Mehra (1962) raisedthe Homalometrinae to family level and recognisedthree subfamilies, the Homalometrinae and two fur-ther new subfamilies the Microcreadiinae and theAssamiinae. Mehra includedMicrocreadiumandPro-creadiumMehra, 1962 within the Microcreadiinae.Procreadiumis now considered an allocreadiid. TheAssamiinae included only the genusAssamiaGupta,1955, which is generally considered an opisthorchiid.Neither of these systems has received support withinthe literature.
Lymphatic vessels.Of the characters mentionedabove, the presence and absence of lymphatic vesselsis perhaps the hardest to interpret. This is becausethe vessels are easily overlooked or misinterpretedand because their significance is not well understood.Pearson (1986) reviewed the distribution of lymphaticvessels within the Digenea and found that they maybe present or absent at the level of the family, sub-family or even genus. Overstreet (1970) expressedlittle confidence in lymphatic vessels as a characterto separate families. We have examined the publisheddescriptions and specimens of species, both those saidto possess and those said to lack lymphatic vessels.In our view, it is certainly true that ducts that mightbe termed lymphatic vessels may be present but wefind them difficult to find and interpret. We have littleconfidence in this character and propose to place noemphasis on it until it can be characterised more con-vincingly. The effect of this, essentially, is that we findno basis for distinguishing the Apocreadiidae and theHomalometridae.
Tegumental spines.Tegumental spines are a typi-cal feature of the Lepocreadiidae and are generallyreported in the genera we consider to belong tothe Apocreadiidae here. However, our observationsand those of others suggest that they are not a uni-versal feature of the family. Reports of tegumentalspines must be treated with caution because theymay be overlooked, they may be lost from speci-mens fixed inadequately, and, we suspect, they maybe reported erroneously by authors expecting to seethem. Based upon review of reports in the litera-
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ture and our observations, tegumental spines appearto be unambiguously present in most or all speciesof Apocreadium, Choanodera, Dactylotrema, Homa-lometron, Megacreadium, Microcreadium, Neoapoc-readium, Neomegasolena, Pancreadium, Postporus,Schistorchis, SphincterostomaandSphincteristomum.Spines appear to be absent consistently in the generaCrassicutis, Myzotus, Marsupioacetabulum, Procau-dotestisand Trematobrien. Given that presence orabsence of tegumental spines is often associated withdifferences between families, the significance of thisis problematical and worthy of further study.
SynthesisOur examination of the distribution of charactersamong the taxa discussed above leads us to pro-pose that the genera presently variously included inthe Apocreadiidae, Homalometridae, Schistorchiidae,Sphincterostomatidae and Trematobrienidae are besttreated as belonging to a single family (Apocreadi-idae). To a considerable extent this idea is a syn-thesis of ideas put forward by previous authors whohave recognised the similarity between many of thesegroups. In general, however, perhaps because of thepervasiveness of Yamaguti’s (1971) monograph, theseideas have not prevailed. We emphasise that there isstill a great deal of uncertainty about the morphol-ogy and relationships of many of the forms that weare considering. We therefore fully expect this clas-sification to change. We propose to characterise theApocreadiidae as follows:
DiagnosisTegument spinous or smooth; spines often lost andeasily overlooked. Dispersed eye-spot pigment usu-ally present near pharynx (e.g., Figure 7). Oral suckeropening subterminally, simple or highly glandular,with or without papillae. Ventral sucker in anteriorhalf of body, usually simple, sometimes with lamel-lar lips or flaps (e.g., Figure 10). Prepharynx present,short. Pharynx simple. Oesophagus short. Caeca ex-tend to near posterior end of body, sometimes open toexterior through separate ani or form cyclocoel. Ex-cretory vesicle I-shaped, sometimes very short, often
extending anteriorly as far as posterior testis, some-times to ovary. Excretory pore terminal or distinctlydorsally or ventrally subterminal. Lymphatic vesselspresent or absent. Testes usually two, tandem, obliqueor symmetrical, sometimes multiple (up to 32), usu-ally entire, sometimes deeply lobed. Cirrus-sac absent.Seminal vesicle naked, usually dorsal to ventral sucker(e.g., Figures 13–15). Pars prostatica distinct; prostatecells free in parenchyma. Pars prostatica unites withuterus to form long or short hermaphroditic duct.Hermaphroditic duct opens at common genital poreusually median and immediately anterior to ventralsucker (some distance anterior inPancreadium, imme-diately posterior inPostporus). Ovary usually entireor weakly lobed, rarely distinctly tri-lobed, posteriorto ventral sucker, anterior to testes. Laurer’s canaland canalicular seminal receptacle present. Vitellar-ium follicular; follicles extensive, may be restrictedto hindbody or enter forebody. Uterus winds betweenovary and ventral sucker before uniting with parsprostatica to form hermaphroditic duct. Eggs tanned,operculate, large.
The key feature of the family as we conceive it is that,within the general framework of characters sharedwith the Lepocreadiidae (usually spiny tegument, ex-tensive vitelline follicles, eye-spot pigment dispersedin forebody, I-shaped excretory vesicle and life-cyclecharacteristics), they lack a cirrus-sac and have (withthe exception ofPancreadiumandPostporus) the gen-ital pore opening immediately anterior to the ventralsucker. The life-cycle also serves to unite the group, atleast for the few species that are known. We considerthis combination of characters worthy of recognitionas a single family for which the name Apocreadiidaehas priority.
Priority of namesOf the numerous family-group names that have beenproposed for taxa that we recognise here as belong-ing together, three were first proposed in 1942. Thisnear simultaneous publication has undoubtedly ledto much of the confusion associated with the group.The Apocreadiinae was proposed on April 20th, theHomalometrinae was proposed on an unspecified dayin April which, according to the International Code
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of Zoological Nomenclature, must be construed asApril 30th, and the Schistorchiidae was proposedin December. Thus the Apocreadiidae becomes thesenior synonym. One other contender, the Anallocre-adiinae Hunter & Bangham, 1932, was replaced withthe Homalometrinae by Cable & Hunninen (1942)when they synonymisedAnallocreadiumwith Homa-lometron. Under the terms of Article 40 of the Codethis replacement is valid so that Anallocreadiidae doesnot become the senior synonym.
It is noteworthy that in this study we propose thesynonymy ofApocreadiumwith Homalometron. Un-der the terms of the Code this does not invalidate theuse of Apocreadiidae as the family name.
Subfamily structureWe recognise three subfamilies within the Apocreadi-idae as follows:
Apocreadiinae Skrjabin, 1942Syns Homalometrinae Cable & Hunninen, 1942;Anallocreadiinae Hunter & Bangham, 1932; Myzoti-nae Yamaguti, 1958; Marsupioacetabulinae Skrjabin& Koval, 1960; Eocreadiinae Mehra, 1962This is the main group of apocreadiids and, as we con-ceive it, unites genera previously included mainly inthe Homalometridae and Apocreadiidae. Its memberslack a partial sphincter in the oral sucker and have thegenital pore in the standard position, median and im-mediately anterior to the ventral sucker. The exceptionto this isPancreadiumin which the genital pore is sep-arated from the ventral sucker. This character makesthis genus perhaps the least convincing member of thesubfamily, but, for the present, there seems no morelogical position for it. As discussed above, we chooseto ignore the presence or absence of lymphatic vesselsas a practical or convincing basis for separation at thefamily group level.
This subfamily is not defined relative to the Schis-torchiinae or Postporinae by any derived character so,in cladistic terms, it is undefined. We can expect,therefore, that this subfamily will undergo further sub-division or redefinition as it becomes better known.Perhaps the two most promising lines for investigationare the presence or absence of tegumental spines andthe presence or absence of lymphatic vessels.
Postporinae Yamaguti, 1958This subfamily includes the single genusPostporus,which is defined within the family by the genitalpore being posterior rather than anterior to the ventralsucker. There is only one species in one genus withthis configuration. Inclusion of this genus and speciesin the Apocreadiidae weakens the integrity of the con-cept of the family, but we choose to include it herebecause, at least for the present, there appears no morelogical family in which to place it.
Included genera:PostporusManter, 1949 (Syn.OpisthoporusManter, 1947 pre-occupied).
Schistorchiinae Yamaguti, 1942Syn. Sphincterostomatinae Yamaguti, 1958This subfamily is defined by the nature of the oralsucker. All four genera have a highly characteristicpartial sphincter embedded in the aperture of the oralsucker. This feature appears a strong, shared, derivedcharacter, so that this subfamily appears to be a naturalone.
Included genera:Schistorchis, Megacreadium,SphincterostomaandSphincteristomum.
Genera excludedMalagashitremaCapron, Deblock & Brygoo, 1961was established forM. aphallosumCapron, Deblock& Brygoo, 1961 and placed in the family Allocre-adiidae by Capron, Deblock & Brygoo (1961). Fis-chthal (1976) subsequently erected a second species,M. cameroonenseFischthal, 1976, and placed thegenus in the Homalometridae. Both species have beenrecorded from chameleons. Despite a general similar-ity to apocreadiids, we consider that their occurrencein chameleons indicates that an association with thisgroup of fish parasites is unlikely. In addition, the ter-minal genitalia, at least ofM. aphallosum, are distinctfrom that of apocreadiidssensu strictoin that the maleand female ducts open into the genital atrium sepa-rately. It is not clear to which other family this genusbelongs.
GloboporumMacCallum, 1921 includes a singlespecies,G. moronisMacCallum, 1921, and was in-cluded by Yamaguti (1971) as an uncertain synonymof Homalometron, although he did not list the speciesnor propose a new combination withHomalometron.The species is generally consistent with the Apocre-adiidae, as we conceive it, but the genital pore opens
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nearly midway between the suckers and the male andfemale ducts do not appear to unite. This combinationof features puts it outside our concept of the family,although the relationships of this genus clearly requirefurther consideration.
pore terminal or ventro-terminal, body length usually> 3× body width . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1414a. Genital pore immediately anterior to ventralsucker; ovary entire . . . . . . . . . . . . . .Neoapocreadium14b. Genital pore well anterior to ventral sucker; ovarydeeply lobed . . . . . . . . . . . . . . . . . . . . . . . .Pancreadium15a. Testes symmetrical; vitelline follicles restrictedto post-testicular zone . . . . . . . . . . . . .Microcreadium15b. Testes tandem to oblique; vitelline follicles ex-tending anterior to testes . . . . . . . . . . . . . . . . . . . . . . . 1616a. Vitelline follicles restricted to posterior half ofhindbody; uterus very extensive, filling most of hind-body; testes near posterior extremity .Procaudotestis16b. Vitelline follicles extending to near ventralsucker; uterus short, between ovary and ventral sucker;testes in mid-hindbody . . . . . . . . . . . . . . . . . . . . . . . . 1717a. Excretory vesicle short, opens postero-ventrally;tegumental spines absent; caeca terminate midway be-tween testes and posterior end of body; ventral suckerenclosed in tegumental pouch . . . . .Callohelmisn. g.17b. Excretory vesicle usually long, opens terminally;tegument usually spiny; caeca terminate near posteriorend of body; ventral sucker not in pouch . . . . . . . . . . .Homalometron
Review of genera and species
Apocreadiinae Skrjabin, 1942
HomalometronStafford, 1904Syns Anallocreadium Simer, 1929; ApocreadiumManter, 1937 (new synonym);BarbulostomumRam-sey, 1965 (new synonym)
Diagnosis. Tegument usually spinous, occasionallysmooth. Dispersed eye-spot pigment usually presentnear pharynx. Oral sucker simple, rarely with papillae.Ventral sucker simple. Caeca blind. Excretory vesicleI-shaped, sometimes very short, often extending ante-riorly as far as posterior testis. Excretory pore terminalor distinctly dorsally subterminal. Lymphatic vesselspresent or absent. Testes usually two. Genital poremedian, immediately anterior to ventral sucker. Ovaryentire or occasionally weakly lobed. Vitelline folliclesextensive, not extending into forebody. Type-species:H. pallidumStafford, 1904.
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CommentsAs we conceive it, this is the largest genus in theApocreadiinae.Anallocreadiumis a long-recognisedand uncontroversial synonym.ApocreadiumandBar-bulostomumare here proposed as synonyms for thefirst time. The concept ofBarbulostomum, as distinctfrom Homalometron, is based only on the presence ofpapillae on the ventral sucker. This level of differencehardly warrants a separate genus and we note that twoother species ofHomalometron(H. carapevaeAmato,1983 andH. elongatumManter, 1947) have prominentpapillae as well. Throughout the literatureApocread-ium is distinguished fromHomalometronon the basisthat it has lymphatic vessels, whereasHomalometronlacks them. As discussed earlier, we note that theselymphatic vessels are difficult to observe and have, infact, not been reported from some species ofApocrea-dium. The two genera are otherwise indistinguishable.Given the uncertainty surrounding the significanceof lymph vessels we propose to unite these speciesin Homalometronuntil they can be separated moreconvincingly.
Tegumental spines have been reported for allspecies in the new enlarged concept of the genus ex-cept forH. cryptum(Overstreet, 1969) n. comb. andH. longisinosum(Manter, 1937) n. comb. We havealso found tegumental spines to be absent in one of thenew species described below. There seems no reasonto doubt the absence of spines in these species norin the form we describe. Given the overall similarityof these three species to other species in the genus,we are unwilling to move them to a separate genus.This does then, however, highlight sharply some of theproblems of apocreadiid taxonomy: normally valuablecharacters such as presence or absence of tegumentalspines may vary between what otherwise appear to beclosely related species. Indeed the absence of tegu-mental spines seems a useful genus level character forthe genusCrassicutis(see below).
Australian species
Homalometron wrightaen. sp.(Figures 1, 4)Type-host:Soleidae:Achlyopa nigra(Macleay).Type-locality: Moreton Bay, SE Queensland, Aus-tralia, 27◦25′ S, 153◦20′ E.Material examined:exA. nigra, Moreton Bay, 5 spec-imens, Nov. 1990; 3, Feb. 1991.Site in host:Intestine.Prevalence:2 of 4 A. nigraexamined.
Type-deposition:Holotype and 4 paratypes QM G214975-9; 3 paratypes, BM(NH) Nos 1998.7.13.5–7.
Description
Measurements are of 5 gravid specimens (see Table I).Body flattened, elongate, often with distinct constric-tion at level of ventral sucker. Tegumental spines com-pletely absent. Cercarial eye-spot pigment distributedindistinctly in forebody. Oral sucker opening subter-minally. Prepharynx distinct, short. Caeca terminateblindly just short of posterior end of body. Excre-tory vesicle I-shaped, extends from posterior extremityto near level of ends of intestinal caeca. Excretorypore terminal. Excretory collecting ducts sometimesvery broad but no unequivocal lymphatic vessels ob-served. Testes entire, tandem, in anterior hindbody.Sperm ducts unite at base of naked seminal vesicle.Seminal vesicle saccular, extends well beyond ven-tral sucker posteriorly. Pars prostatica distinct, directlydorsal to ventral sucker. Ejaculatory duct joined byuterus to form hermaphroditic duct immediately distalto pars prostatica. Hermaphroditic duct runs directlyto common genital pore. Common genital pore me-dian, immediately anterior to ventral sucker. Ovaryentire, close to ventral sucker. Egg-forming compleximmediately posterior to ovary. Oviduct arises frompostero-dorsal surface of ovary, joined by ducts lead-ing to vitelline reservoir, Laurer’s canal and canalicu-lar seminal receptacle. Vitelline follicles extend fromnear posterior margin of ovary or midway betweenovary and anterior testis to posterior end of body, in-terrupted by testes; fields separate anterior to testes,confluent dorsally posterior to testes. Vitelline reser-voir posterior to ovary. Laurer’s canal opens dorsallybetween ovary and ventral sucker. Seminal receptacleprominent, extends antero-dorsally from ovary. Uteruswinds between ovary and ventral sucker before unitingwith ejaculatory duct dorsal to ventral sucker. Eggssparse, up to c. 9, operculate, tanned.
Etymology: This species is named in honour of MsTrudy Wright.
Comparison The very elongate body in which thepost-testicular zone occupies>50% of the body lengthimmediately distinguishes this from all species ofHomalometronexcept H. galaicus (Sanmartín, Al-varez, Quinteiro & Paniagua, 1995) n. comb. andH. senegalenseFischthal & Thomas, 1972. The newspecies differs from these, however, in its evident
complete lack of tegumental spines and its very shortexcretory vesicle. It is noteworthy thatH. wrightae,H. galaicusandH. senegalenseare the only apocre-adiids known from soleid fishes. Given their strikingoverall similarity, it seems likely that they form aclosely related group of species.
Tegumental spines have been reported as absentin only two other species in this genus:H. cryp-tum (Overstreet, 1969) n. comb. andH. longisinosum(Manter, 1937). We have examined good specimens ofboth these species (USNPC 74172-3; 9060) and thereis no reason to doubt the absence of spines in either ofthese species nor in the form described here. A veryshort excretory vesicle comparable to that found hereis seen inH. pallidum.
Homalometron synagris(Yamaguti, 1953) n. comb.(Figures 2, 5)Syn.Apocreadium synagrisYamaguti, 1953Host: Nemipteridae: Scolopsis monogramma(Cu-vier).Material examined: S. monogramma, Heron Is., south-ern Great Barrier Reef, 23◦27′ S, 151◦55′ E. 3 speci-mens, Mar. 1990; 2, Sept. 1993; 1 (sectioned), Jan.1994; 2, Jul. 1994; 5, Jul. 1994; 3, Jul. 1995.Site:Intestine.Prevalence:7 of 10S. monogrammaexamined.Specimen deposition:11 (including 3 sets of sections)QM G 214980-90; 4, BM(NH) Nos 1998.7.21.1–4.
Description
Measurements are of 9 mature specimens (see Ta-ble I). Body flattened, lanceolate, often with distinctconstriction at level of ventral sucker. Tegumentalspines dense and prominent in forebody, far less densein hindbody. Cercarial eye-spot pigment distributedindistinctly in vicinity of pharynx. Oral sucker open-ing subterminally. Prepharynx distinct, sometimesentirely within concavity of oral sucker. Caeca ter-minate blindly just short of posterior end of body.Excretory vesicle I-shaped; anterior extent variableposterior to posterior testis. Excretory pore terminal.No unequivocal lymphatic vessels observed. Testesentire, distinctly elongate, tandem, in anterior half ofhindbody. Sperm ducts unite at base of naked sem-inal vesicle. Seminal vesicle saccular, may extendwell posterior to ventral sucker. Pars prostatica dis-tinct, directly dorsal to ventral sucker. Ejaculatory ductjoined by uterus to form short hermaphroditic ductimmediately distal to pars prostatica. Hermaphroditic
duct runs directly to common genital pore. Commongenital pore median, immediately anterior to ventralsucker. Ovary entire, midway between ventral suckerand anterior testis. Oviduct arises from dorsal surfaceof ovary, joined by ducts leading to vitelline reser-voir. Canalicular seminal receptacle antero-dextral toovary. Vitelline follicles extend from close to poste-rior margin of ventral sucker to posterior end of body;fields separate anterior to testes, confluent ventrallyand dorsally posterior to testes. Vitelline reservoir be-tween ovary and anterior testis. Laurer’s canal opensdorsal to ovary. Seminal receptacle antero-dorsal toovary. Uterus winds between anterior testis and ventralsucker before uniting with ejaculatory duct dorsal toventral sucker. Eggs numerous, up to c. 40, operculate,tanned.Records: 1 Yamaguti (1953), 2 Fischthal & Kuntz(1965), 3 Present study.Descriptions:1, 2, 3.Hosts: Nemipteridae: Synagris taeniopterus(1),Scolopsis margaritifer(2), Scolopsis monogramma(3).Localities: Indonesia (1), Malaysia (2), Queensland,Australia (3).
ComparisonWe have no hesitation in identifying these specimensasH. synagris. They resemble Yamaguti’s (1953) fig-ured specimen closely and also agree generally inmeasurements. Two voucher specimens of Fischthal& Kuntz (1965) that we examined (USNPC 60072)are in very poor condition and do not allow criticalstudy. Fischthal & Kuntz (1965) reported lymphaticvessels but we saw nothing that we could identify un-equivocally as such. Their specimens seem broadlyconsistent with this species, however.
We have found this species in seven of 10Scolopsismonogrammaexamined from the southern Great Bar-rier Reef but from none of fiveS. margaritiferfrom thesame locality, despite the fact that Fischthal & Kuntz(1965) reported it as a host.
Type-deposition:Holotype and 3 paratypes QM G214991-4; 3 paratypes, BM(NH) Nos 1998.7.13.8–10.
Description
Measurements are of 3 mature specimens (see Table I).Body elongate, often with distinct constriction at levelof ventral sucker. Tegumental spines prominent anddense in forebody, far less dense in hindbody. Cercar-ial eye-spot pigment distributed indistinctly in vicinityof pharynx. Oral sucker opening subterminally. Ven-tral sucker usually with longitudinal aperture. Prephar-ynx distinct. Oesophagus very short. Caeca terminateblindly just short of posterior end of body. Excretoryvesicle I-shaped, terminates just posterior to poste-rior testis. Excretory pore terminal. Lymphatic vesselsnot observed. Testes entire, tandem, in mid-hindbody.Seminal vesicle saccular, may extend distinctly pos-terior to ventral sucker. Pars prostatica bulbous, dis-tinct, at level of posterior margin of ventral sucker.Ejaculatory duct joined by uterus to form long her-maphroditic duct immediately distal to pars prostatica.Hermaphroditic duct runs directly to common geni-tal pore. Common genital pore median, immediatelyanterior to ventral sucker. Ovary entire, midway be-tween ventral sucker and anterior testis. Oviduct arisesfrom dorsal surface of ovary, joined by ducts leadingto vitelline reservoir. Canalicular seminal receptacledorsal to ovary. Vitelline follicles extend from anteriormargin of ovary to posterior margin of body; fieldslargely separate anterior to testes, confluent dorsally
and ventrally posterior to testes. Vitelline reservoir be-tween ovary and anterior testis. Laurer’s canal opensdorsal to ovary. Mehlis’ gland between ovary and an-terior testis. Uterus winds between Mehlis’ gland andventral sucker before uniting with ejaculatory ductdorsal to ventral sucker. Eggs few, up to about 7, notobviously operculate, tanned.
ComparisonHomalometron stradbrokensisn. sp. has generalisedmorphological features and can be grouped with 12other species with ‘typical’ morphology (see below).Among these it is distinctive in the combination of itselongate form, the extensive post-testicular zone, therestriction of the vitelline follicles to well posteriorto the ventral sucker, and the excretory vesicle whichextends close to the posterior testis.
Sciaenidae:Aplodinotus grunniens(1, 2, 4, 5, 6, 9, 10,14, 15, 18, 19, 20); Sparidae:Archosargus probato-cephalus(3).Localities: Lake Erie, North America (5, 6, 14, 19),Louisiana, United States (9, 10), Michigan, UnitedStates (16), Mississippi, United States (4), Ontario,Canada (1, 18), Quebec, Canada (7), Tennessee,United States (8), Texas, United States (11, 12, 13, 15,17), Wisconsin, United States (2, 3), Alabama, UnitedStates (20).Comments:Life-cycle information given by Hopkins(1937) and Gentner & Hopkins (1966). Miller (1940)and Miller (1959) argued convincingly thatH. pearseiis a synonym ofH. armatum.
Homalometron cryptum(Overstreet, 1969) n. comb.Syn.Apocreadium cryptumOverstreet, 1969Records:1 Overstreet (1969), 2 Fischthal (1977).Descriptions:1.Hosts: Haemulidae:Anisotremus virginicus(1, 2),Haemulon flavolineatum(2), H. parrai (1).Localities:Florida, United States (1), Belize (2).
Homalometon cupuloris(Ramsey, 1965) n. comb.Syn.Barbulostomum cupulorisRamsey, 1965Records:1 Ramsey (1965), 2 Fiorillo & Font (1996).
13
Descriptions:1.Hosts: Centrarchidae:Lepomis macrochirus(2), L.microlophus(1, 2), L. punctatus(1, 2), L. megalotis(2).Localities:Louisiana, United States (1, 2).
Homalometron dowgialloiDyer, Williams & Bunkley-Williams, 1992Records: 1 Dyer, Williams & Bunkley-Williams(1992).Descriptions:1.Hosts:Haemulidae:Haemulon flavolineatum(1).Localities:Puerto Rico (1).
Homalometron elongatumManter, 1947Records: 1 Manter (1947), 2 Sogandares-Bernal(1959), 3 Siddiqi & Cable (1960), 4 Nahhas & Ca-ble (1964), 5 Fischthal (1977), 6 Nahhas & Carlson(1994).Descriptions:1.Hosts:Ephippidae:Chaetodipterus faber(3); Gerrei-dae:Eucinostomus californiensis(2), Gerres cinereus(1, 2, 3, 4, 5, 6); Sparidae:Calamus bajanado(5).Localities: Florida, United States (1), Bahamas (2),Puerto Rico (3), Jamaica (4, 6), Belize (5), Panama,Pacific coast (2).Comments:Bravo-Hollis & Manter (1957) providedextra information about the structure of the oral suckerof this species, showing that it has papillae that theysuggested may be homologous with those ofDacty-lotrema squamatumBravo-Hollis & Manter, 1957.
Homalometron foliatumSiddiqi & Cable, 1960Syn. Apocreadium foliatum(Siddiqi & Cable, 1960)Overstreet, 1969Records:1 Siddiqi & Cable (1960), 2 Nahhas & Ca-ble (1964), 3 Overstreet (1969), 4 Dyer, Williams &Bunkley-Williams (1992).Descriptions:1.Hosts:Ephippidae:Chaetodipterus faber(4); Haemul-idae: Brachygenys chrysargyreus(2), Haemulon au-rolineatum(3), H. carbonarium(3), H. flavolineatum(1, 2, 4),H. parrai (3), H. album(2), H. sciurus(2,4); Kyphosidae:Kyphosus sectatrix(4); Lutjanidae:Lutjanus apodus(4), L. mahogoni(2).Localities: Puerto Rico (1, 4), Curaçao (2), Jamaica(2) Florida, United States (3).
Localities: Florida, United States (7), Tangola Tan-gola, Mexico (1, 2), Gulf of Mexico (6), Belize (8,9), Puerto Rico (4), Jamaica (5), Bahamas (3).Comments:We have examined the holotype ofApoc-readium uroproctoferumSogandares-Bernal, 1959(USNPC 38867) and found that, quite clearly, it doesnot possess a uroproct. In the absence of a uroproctthere appears to be no basis for separation of thisspecies fromH. mexicanumwith which it shares aCaribbean distribution and one of the same hosts.We therefore have no hesitation in proposingH. uro-proctoferumas a junior synonym ofH. mexicanum.
Homalometron pseudopallidumMartorelli, 1986Records:1 Martorelli (1986)Descriptions:1.Hosts:Cichlidae:Gymnogeophagus australis(1).Localities:Argentina (1).Comment:Martorelli (1986) described the life-cycle.
Homalometron senegalenseFischthal & Thomas,1972Records:1 Fischthal & Thomas (1972).Descriptions:1.Hosts:Soleidae:Solea hexophthalma(1).Localities:Senegal (1).
Homalometron verrunculinom. nov.Syn. Homalometron caballeroiLamothe-Argumedo,1965Records:1 Lamothe-Argumedo (1965).Descriptions:1.Hosts: Balistidae: Balistes [Verrunculus] polylepis(1).Localities:Gulf of California, Mexico (1).Comments: The synonymy ofApocreadiumwithHomalometron forces the creation of a seniorhomonym Homalometron caballeroi(Bravo-Hollis,1953), which necessitates the proposal of a replace-ment name forH. caballeroi Lamothe-Argumedo,1965.
Homalometron vinodae(Ahmad, 1985) n. comb.Syn.Apocreadium vinodaeAhmad, 1985Records:1 Ahmad (1985).Descriptions:1.Hosts: Balistidae: Sufflamen (as Hemibalistes)chrysopterus(1).Localities:India (1).
Homalometronsp.Syn.Apocreadiumsp.Records:1 Quintero-Alonso, Martínez-Ubeiro, Fer-nández & Sanmartín-Durán (1988).Descriptions:Nil.Hosts: Soleidae:Microchirus variegatus(1), Solealascaris(1).Localities:Spain (1).Comment: This species is probably a synonym ofHomalometron galaicus, according to Sanmartín, Al-varez, Quinteiro & Paniagua (1995).
Homalometronsp.Records:1 Mamaev (1970).Descriptions:Nil.Hosts:Gerreidae:Gerres filamentosa(1).Localities:Gulf of Tonkin (1).
‘Apocreadium misakiense’Williams & Bunkley-Williams (1996) listApocrea-dium misakiense(p. 299) as a parasite ofScomberjaponicus. This species is apparently based onLep-ocreadium misakienseShimazu, 1986, which wasdescribed by Shimazu (1986), fromS. japonicusinJapanese waters. The transfer toApocreadiumappearsto have been an unintended mistake, as this specieshas a clear cirrus-sac and no particular affinity withthe Apocreadiidae.
Speciesincertae sedisApocreadium priacanthiWang & Wang, 1993 wasdescribed from the priacanthidPriacanthus macra-canthusand fromGastrophysus lunarisfrom Chinesewaters (Wang & Wang, 1993). The description and fig-ure are not sufficient to allow clear recognition of thisspecies and we do not include it in the Apocreadiidaefor the present. We draw attention to the superficialresemblance between this species and certain speciesof the opecoelid genusPseudopecoeloidesYamaguti,1940, which is common in the priacanthid fishes of thegenusPriacanthus. In particular, the spindle-shaped
15
testes are reminiscent of this genus.
Groups within HomalometronIn view of the enlarged concept ofHomalometronrecognised here, and the description of two newspecies, we have considered the composition of thegenus in a search for groups of species. We observeeight groups of one or more species and a group of14 ‘typical’ species which includes the type-species.We suspect that some of these groups may ultimatelyrequire separate genera of their own.
1. Oral sucker far larger than ventral sucker (uniquecharacter):H. cryptum.2. Three pairs of large papillae on oral sucker:H. cara-pevaeandH. elongatum.3. One pair of papillae on oral sucker:H. cupuloris.4. Testes deeply lobed (unique character):H. ca-balleroi.5. Extremely long hindbody; post-testicular zonegreater than 50% of body length:H. galaicus, H. sene-galenseand H. wrightae. These are the only threeapocreadiids to infect soleid fishes.6. Vitelline follicles extend only to anterior margin oftestes:H. balistisandH. foliatum.7. Ovary separated from testes by nearly one-third ofbody length:H. longulum.8. Typical species: H. armatum, H. dowgial-loi, H. longisinosum, H. manteri, H. mexicanum,H. pallidum, H. stradbrokensis, H. pseudopallidum,H. sophiae, H. synagris, H. verrunculiandH. vinodae.
Callohelmisn. g.
Diagnosis.Tegument smooth. Dispersed eye-spot pig-ment present near pharynx. Oral sucker opening sub-terminally, simple. Ventral sucker in anterior half ofbody, simple, usually retracted in distinct pouch (Fig-ures 7–9). Prepharynx present, short. Pharynx simple.Oesophagus short. Caeca extend to midway betweentestes and posterior end of body. Excretory vesicleI-shaped, short, not reaching posterior testis. Excre-tory pore distinctly ventrally subterminal. Lymphaticvessels absent. Testes two, tandem. Seminal vesiclenaked, usually dorsal to ventral sucker. Pars prostaticadistinct; prostate cells free in parenchyma. Pars pro-statica unites with uterus to form hermaphroditic duct.Hermaphroditic duct opens at common genital pore,median and immediately anterior to ventral sucker.
Ovary entire, posterior to ventral sucker, anterior totestes. Laurer’s canal and canalicular seminal recepta-cle present. Vitelline follicles restricted to hindbody.Uterus winds between ovary and ventral sucker beforeuniting with pars prostatica to form hermaphroditicduct. Eggs tanned, operculate. Type-species:Callo-helmis pichelinaen. sp.
CommentsThe combination of absence of tegumental spines,caeca terminating midway between the testes and theposterior end of the body, ventral sucker enclosedin a tegumental pouch, prominent muscles radiatingthrough the body from the ventral sucker (Figure 8),vitelline follicles not extending into the forebody andvery short excretory vesicle that opens ventrally makethis species distinctive among apocreadiids. We con-clude that these differences are best recognised by theerection of a distinct genus.
Callohelmis pichelinaen. sp.(Figures 7, 8, 9)Type-host:Labridae:Hemigymnus melapterus(Bloch).Type-locality:Heron Is., southern Great Barrier Reef,23◦27′ S, 151◦55′ E.Other hosts:Labridae:Hemigymnus fasciatus(Bloch),Stethojulis bandanensis(Bleeker),Choerodon venus-tus(De Vis).Material examined:All Heron Is. H. melapterus:1specimen, Jan. 1991; 3, Jan. 1992; 19, Jan. 1993;3, Sept. 1993; 17 (including 7 sets of sections), Jan.1994; 20, Jan. 1996.H. fasciatus:5, Jan. 1996.S. ban-danensis:3, Jan. 1996.C. venustus:3, Jan. 1996.Site:Intestine.Prevalence:11 of 14H. melapterus; 3 of 6 H. fascia-tus; 1 of 2S. bandanensis; 1 of 20C. venustus.Type-deposition: Holotype and 18 paratypes (in-cluding 4 sets of sections) QM G 214995-5013;13 paratypes (including 2 sets of sections), BM(NH)Nos 1998.7.9.1–15.
Description
Measurements are of 10 specimens (see Table I). Bodyflattened, often with slight constriction at level ofventral sucker. Tegumental spines completely absent.Cercarial eye-spot pigment distributed indistinctly inforebody. Oral sucker opening subterminally. Ventralsucker usually retracted in distinct pouch. Prepharynxdistinct, sometimes entirely within concavity of oralsucker. Oesophagus short. Caeca terminate blindlymidway between posterior testis and posterior end of
body. Excretory vesicle I-shaped, notably variable inlength, may extend to well short of ends of intestinalcaeca or well anterior to them. Excretory pore opensventrally, distinctly short of posterior extremity. Lym-phatic vessels not observed. Testes entire, tandem, inmid-hindbody. Sperm ducts unite at base of nakedseminal vesicle. Seminal vesicle saccular, extendsslightly beyond ventral sucker posteriorly. Pars prosta-tica distinct, directly dorsal to ventral sucker. Ejacula-tory duct joined by uterus to form hermaphroditic ductimmediately distal to pars prostatica. Hermaphroditicduct runs directly to common genital pore. Commongenital pore median, immediately anterior to ventralsucker. Ovary entire, antero-dextral to anterior testis.Oviduct arises from dorsal surface of ovary, joinedby ducts leading to vitelline reservoir, Laurer’s canaland canalicular seminal receptacle. Vitelline folliclesextend from about posterior margin of ventral suckerto posterior end of body, limited to extra-caecal areasexcept posterior to posterior testis where they fill inter-caecal zone; fields confluent dorsally in hindbody pos-terior to testes. Vitelline reservoir immediately ventralto ovary. Laurer’s canal opens dorsally between ovaryand ventral sucker. Seminal receptacle antero-dorsal toovary. Uterus winds between ovary and ventral suckerbefore uniting with ejaculatory duct dorsal to ventralsucker. Eggs few, tanned, operculate.
Etymology:Named in honour of Dr Sylvie Piche-lin.
ComparisonThe features that distinguish the new genus serve todistinguish this species from all previously describedapocreadiids.
ChoanoderaManter, 1940Syn.NeochoanoderaFischthal & Thomas, 1970Diagnosis.Tegument spinous. Forebody with edgesfolded ventrally and converging to meet at posterioredge of ventral sucker. Oral sucker simple. Ventralsucker simple. Caeca blind, extend to near poste-rior end of body. Excretory vesicle I-shaped, extendsanteriorly as far as posterior testis. Excretory pore ter-minal. Lymphatic vessels present. Testes two. Genitalpore median, immediately anterior to ventral sucker.Ovary entire or weakly lobed. Vitelline follicles re-stricted to hindbody. Type-species:C. caulolatiliMan-ter, 1940.
CommentsThis genus is recognisable for the distinctive lateralflaps in the forebody. We proposeNeochoanoderaasa new synonym ofChoanodera. There is only a singlespecies in each genus. These are strikingly similar ingeneral features, especially in the defining conforma-tion of the forebody. We prefer to consider the char-acteristics ofNeochoanoderaoutlined by Fischthal &Thomas (1970) (slit-like oral aperture, relatively mas-sive pharynx and distribution of vitelline follicles) tobe of specific significance.
Choanodera caulolatiliManter, 1940Syn. Choanodera moseriFrost & Dailey, 1994 (newsynonymy)Records:1 Manter (1940), 2 Frost & Dailey (1994).Descriptions:1, 2.Hosts: Malacanthidae:Caulolatilus anomalus(1),C. princeps(2), C. sp. (1); Serranidae:Paralabraxnebulifer(2).Localities: Mexico (1), Galapagos Islands (1), Cali-fornia, United States (2).Comments: Frost & Dailey (1994) distinguishedC. moseri,from C. caulolatili on grounds that seemweak. We have examined their type specimens fromthe USNPC as well as the holotype ofC. caulo-latili . Frost & Dailey (1994) reported the absenceof tegumental spines, whereas we have found themunequivocally in one of their specimens; they com-mented on the smaller body size of their specimens,although their sample was small and Manter (1940)in fact refers to a gravid specimen well within therange they reported; and they refer to the round ratherthan lobed ovary, although Manter (1940) actually de-scribed the ovary ofC. caulolatili as ‘without distinctlobes’. Frost & Dailey’s specimens appear somewhatmacerated to us (presumably accounting for the loss ofmost of the tegumental spines). In figure, descriptionand specimens the two species seem very similar andwe see no justification for recognisingC. moseri.
CrassicutisManter, 1936Syn.EocreadiumSzidat, 1954Diagnosis.Body length< 3× body width. Tegumentsmooth. Dispersed eye-spot pigment usually presentnear pharynx. Oral sucker simple. Ventral sucker sim-ple. Caeca blind, extend to near posterior end ofbody. Excretory vesicle I-shaped, usually extendinganteriorly as far as posterior testis. Excretory pore usu-ally distinctly dorsally subterminal. Lymphatic vesselsabsent. Testes two, tandem to diagonal or almostsymmetrical, distinctly lobed to entire. Genital poremedian, immediately anterior to ventral sucker. Ovaryentire or weakly lobed. Vitelline follicles extend wellinto forebody. Parasites of freshwater and brackishwater fishes. Type-species:C. cichlasomaeManter,1936.
CommentWe have revised the concept of this genus. It isclose toNeoapocreadiumSiddiqi & Cable, 1960, butdiffers in lacking tegumental spines consistently, inbeing less elongate and in generally having the ex-cretory pore opening distinctly dorso-subterminallyrather than terminally. This concept restricts the genusto seven species of which six (C. cichlasomae(type-species),C. bravoae, C. chuscoi, C. intermedius,C. opisthoseminisand C. wallini) are parasites offreshwater fish and one,C. archosargi, parasitises abrackish water fish. This revised concept requires themovement of five species,C. caranxi, C. marinum,C. gerridis, C. karwarensisandC. imtiazito Neoapoc-readium.These and all other species ofNeoapocre-adium are parasites of marine fish. Three of thesespecies,C. marinum, C. karwarensisand C. imtiaziare reported to lack tegumental spines. This meansthat, like Homalometron, Neoapocreadiumcontainsspecies both with and without tegumental spines. As aresult we suspect thatNeoapocreadiummay not repre-sent a natural group. The new concept ofCrassicutis,however, appears a strong one, supported by mor-phological characters that are reinforced by biologicalfeatures.
(1997), 10 Salgado-Maldonaldo, Pineda-López,Vidal-Martínez & Kennedy (1997), 11 Scholz &Vargas-Vázquez (1998).Descriptions:1, 2, 3, 5, 7, 8.Hosts: Cichlidae: Cichlasoma aureum(11), C. cit-rinellum (4), C. fenestratum(6,), C. friedrichstahlii(10),C. geddesi(10),C. helleri (10),C. labiatum(4),C. managuense(4, 10),C. mayorum(1), C. meeki,(7,8, 11)C. nicaraguense(4),C. octofasciatum(8),C. pa-sionis(10), C. pearsei(8, 10),C. robertsoni(10), C.rostratum(4), C. spilurum(4), C. synspilum(8, 10,11),C. tetracanthum(3, 5),C. urophthalmus(5, 7, 8,9, 10, 11),Cichlasomasp. (2),Petenia splendida(10).Localities: Costa Rica (1, 2), Cuba (3, 5), Nicaragua(4), Mexico (1, 5, 6, 7, 8, 9, 10, 11).Comments: Scholz, Pech-Ek & Rodriguez-Canul(1995) described the life-cycle of this species. Scholz,et al. (1995), Lamothe-Argumedo, García, Osorio-Sarabia & Pérez-Ponce de Léon (1996) and Pérez-Ponce de Léon, García-Prieto, Osorio-Sarabia &León-Règagnon (1996) summarise more records ofthis species from the same and further species of Cen-tral American cichlids.
Crassicutis archosargiiSparks & Thatcher, 1960Records:1 Sparks & Thatcher (1960), 2 Joy (1971), 3Overstreet (1976a).Descriptions:1, 3.Hosts:Sparidae:Archosargus probatocephalus(1, 2,3).Localities: Louisiana, United States (1, 3), Texas,United States (2).Comments:Overstreet (1976b) and Weidner & Over-street (1979) recorded a myxozoan hyperparasite inthis species.
Crassicutis intermedius(Szidat, 1954) Bray, deChambrier & Vaucher, 1996Syn.Eocreadium intermediumSzidat, 1954Records:1 Szidat (1954); 2 Kohn & Fróes (1986);3 Fortes, Gutierres & Hoffmann (1985); 4 Fortes &Hoffmann (1995); 5 Bray, de Chambrier & Vaucher(1996).Descriptions:1, 2, 5.Hosts:Anostomidae:Leporinus copelandi(3), L. ob-tusidens(4); Callichthyidae:Hoplosternum littorale(5); Loricariidae: Cochliodon cochliodon(4), Hy-postomus commersoni(1, 2, 5), H. piratatu (5), H.boulengeri(5), H. paranensis(5).Localities: Buenos Aires, Argentina (1), Brazil (2, 3,4), Paraguay (5).Comment:This species is usually in the alimentarysystem, but Kohn & Fróes (1986) report an immaturespecimen from the swim-bladder.
DactylotremaBravo-Hollis & Manter, 1957Diagnosis.Tegument spinous. Oral sucker with sev-eral pairs of elongate pointed processes embedded inwall of outer margin dorsally and ventrally. Ventralsucker simple. Excretory vesicle unknown. Excre-tory pore terminal. Lymphatic vessels not reported.Testes two. Genital pore median, immediately ante-rior to ventral sucker. Ovary entire. Vitelline folliclesrestricted to hindbody. Type-species:D. squamatumBravo-Hollis & Manter, 1957;
CommentsThis genus is characterised by the highly distinctiveoral sucker. The only other specialisations of the oralsucker seen in this subfamily are the single pair ofpapillae on the oral sucker ofHomalometron cupu-loris and the three pairs of papillae on the oral suckerof H. carapevaeandH. elongatum. In none of thesespecies are the papillae as complex or distinctive acharacter as they are in the only species ofDacty-lotrema.
Diagnosis.Tegument smooth. Dispersed eye-spot pig-ment present near pharynx. Oral sucker simple. Ven-tral sucker with lamellar lips embedded in aperture(Figure 10). Caeca blind, extend to near posteriorend of body. Excretory vesicle I-shaped, extends totestes or ovary. Excretory pore dorso-subterminal.Lymphatic vessels absent. Testes two, symmetrical.Genital pore median, immediately anterior to ventralsucker. Ovary entire. Vitelline follicles extend wellinto forebody. Type-species:M. marinumYamaguti,1952.
CommentsThis genus is characterised by the smooth tegumentand characteristic form of the ventral sucker. Theabsence of tegumental spines and parasitism of ger-reid fishes suggests an affinity with the two spine-less species ofNeoapocreadiumthat also parasitisegerreids.
The type-species,M. marinum, was described froma single flattened specimen and is figured with a ter-minal excretory pore. The pore in the new speciesdescribed below is clearly slightly dorso-subterminaland we suspect that this is typical for the genus.
Australian species
Marsupioacetabulum opallioderman. sp. (Figures10, 13)Type-host:Gerreidae:Gerres subfasciatusCuvier.Type-locality: Moreton Bay, SE Queensland, Aus-tralia, 27◦25′ S, 153◦20′ E.Material examined: G. subfasciatus, Moreton Bay, 9specimens, (including 2 sets of serial sections), Jan.1994; 7, Feb. 1994; 3, Nov. 1994; 9, Aug. 1995.Site:Intestine.Prevalence:13 of 95G. subfasciatusexamined.Type-deposition:Holotype and 7 paratypes (including2 sets of sections) QM G 215014-21; 6 paratypes,BM(NH) Nos 1998.7.20.1–6.
Description
Measurements are of 12 specimens (see Table I). Bodyplump. Tegument very thick (up to 26µm), dis-tinctively opalescent in life. Tegumental spines com-pletely lacking. Cercarial eye-spot pigment distributedindistinctly in forebody. Pre-oral lobe prominent. Oralsucker opening subterminally. Ventral sucker withprominent lamellar lips at aperture. Prepharynx dis-tinct, short, usually entirely within concavity of oralsucker. Oesophagus short. Caeca terminate blindlyclose to posterior end of body. Excretory vesicle I-shaped, opens slightly dorso-subterminally, extendsto posterior margin of testes. Excretory pore slightlydorso-subterminal; groove in tegument sometimesleads from excretory pore to posterior extremity giv-ing impression of terminal pore. Lymphatic vesselsnot observed. Testes entire, symmetrical, in mid-hindbody. Sperm ducts unite at base of naked seminalvesicle. Seminal vesicle saccular, entirely dorsal toventral sucker. Pars prostatica distinct, immediatelyanterior to ventral sucker. Ejaculatory duct joinedby uterus to form hermaphroditic duct immediatelydistal to pars prostatica. Hermaphroditic duct veryshort, runs directly to common genital pore. Commongenital pore median, just anterior to ventral sucker.Ovary median, contiguous with the anterior marginsof testes. Egg-forming complex immediately anteriorto ovary. Oviduct arises from anterior surface of ovary,joined by ducts leading to vitelline reservoir, Laurer’scanal and canalicular seminal receptacle. Vitelline fol-licles extend from level of pharynx to posterior endof body; left and right fields confluent dorsally andventrally posterior to testes, separate anterior to testes.Vitelline reservoir immediately dorsal to ovary. Lau-rer’s canal opens dorsally between ovary and ventralsucker. Seminal receptacle prominent, antero-dorsal toovary. Uterus winds between testes and ventral suckerbefore uniting with ejaculatory duct dorsal to ventralsucker. Eggs few, tanned, operculate.
Etymology:From the Greekopallios(opal) andderma(skin), referring to the opalescent tegument of theliving worm.
ComparisonYamaguti’s (1952) description ofMarsupioacetabu-lum marinumfrom Gerres punctatusfrom Sulawesi(as Celebes) is the only previous record of this genus.Yamaguti based his description on a single ‘somewhatflattened’ specimen which was about 3 mm long. The
22
present specimens are generally similar toM. mar-inum, so that there is no doubt that they belong inMarsupioacetabulum. We see two clear points of dis-tinction which suggest to us that the present specimensrepresent a new species. Firstly, in Yamaguti’s spec-imen the excretory vesicle passes between the testesand extends unambiguously to the ovary, whereas inours it clearly extends only to the posterior marginof the testes. Secondly, the oral sucker of Yamaguti’sspecimen is clearly relatively smaller than in ours. Ithas a maximum width of only 255µm in a specimenabout 3 mm long whereas in our sample oral suckersthat small are seen only in specimens about half thatlong. If anything, we would have expected the flatten-ing of Yamaguti’s specimen to bring about an artificialincrease in the width of the oral sucker. Yamaguti re-ported no eye-spot pigment and that the "cuticle" wasonly 3 µm thick. In addition the pars prostatica ap-pears somewhat more extensive inM. marinum(dueto flattening ?), reaching well into the hindbody.
MicrocreadiumSimer, 1929Diagnosis. Tegument spinous. Oral sucker simple,larger than ventral sucker. Ventral sucker simple.Caeca blind, extend to near posterior end of body.Excretory vesicle I-shaped, extends almost to testes.Excretory pore terminal. Lymphatic vessels absent.Testes two, symmetrical. Genital pore median, im-mediately anterior to ventral sucker. Ovary entire.Vitelline follicles restricted to post-testicular zone.Type-species:M. parvumSimer, 1929.
CommentThis genus is distinguished by the combination ofsymmetrical testes and the vitelline follicles restrictedto the post-testicular zone.
Microcreadium parvumSimer, 1929Records:1 Simer (1929).Descriptions:1.Hosts:Sciaenidae:Aplodinotus grunniens(1).Localities:Mississippi, United States (1).
Comment:Life-cycle information given by Hopkins(1937) and Gentner & Hopkins (1966).
MyzotusManter, 1940
Diagnosis. Tegument smooth. Oral sucker simple.Ventral sucker with conspicuous bilobed flap on eachlateral margin. Caeca blind, extend to near poste-rior end of body. Excretory vesicle I-shaped, extendsto posterior testis. Excretory pore terminal. Lym-phatic vessels absent. Testes two, tandem. Genitalpore median, immediately anterior to ventral sucker.Ovary entire. Vitelline follicles extend to oral sucker.Type-species:M. vitellosusManter, 1940.
CommentThis genus is distinguished by the lateral flaps on theventral sucker and the very extensive vitelline follicles.
Myzotussp.Records:1 Escalante, Jara & Silva (1984).Descriptions:(1).Hosts:Malacanthidae:Caulolatilus cabezon.Localities:Peru (1).
NeoapocreadiumSiddiqi & Cable, 1960
Diagnosis.Tegument spinous or smooth. Body length2.5–7× body width. Dispersed eye-spot pigment usu-ally present near pharynx. Oral sucker simple. Ventralsucker simple. Caeca blind, extend to near posteriorend of body. Excretory vesicle I-shaped. Excretorypore terminal. Lymphatic vessels frequently said tobe present. Testes two, usually tandem. Genital poremedian, immediately anterior to ventral sucker. Ovaryentire. Vitellarium follicles extend well into forebody.Parasites of marine fish. Type-species:N. angustum(Sogandares-Bernal, 1959).
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CommentThis genus is most similar toHomalometronfromwhich it differs in the distribution of the vitelline folli-cles (which extend well into the forebody inNeoapoc-readium) and Crassicutiswith which it is discussedabove. It is characterised by the combination of the(usually) spiny tegument, the vitelline follicles ex-tending into the forebody, the simple oral and ventralsuckers, and a terminal excretory pore. Lymphaticvessels have been reported frequently but we are notbasing the concept of the genus on this character.
Australian species
Neoapocreadium karwarensis(Hafeezullah, 1970)n. comb.(Figures 11, 14)Syn.Crassicutis karwarensisHafeezullah, 1970Host:Gerreidae:Gerres subfasciatusCuvier.Material examined: G. subfasciatus,Moreton Bay SEQueensland, 27◦25′ S, 153◦20′ E: 41 specimens (in-cluding one set of serial sections), Feb. 1993; 2, Mar.1995; 1, Apr. 1995.Site:Intestine.Prevalence:15 of 92G. subfasciatusexamined.Specimen deposition:10 QM G 215022-31; 6BM(NH) Nos 1998.7.13.1–4; 1998.7.21.5–7.
Description
Measurements are of 15 specimens (see Table I). Bodyelongate, with nearly parallel sides. Tegumental spinescompletely absent. Cercarial eye-spot pigment distrib-uted indistinctly in forebody. Oral sucker opening sub-terminally. Prepharynx distinct, short, usually entirelywithin concavity of oral sucker. Oesophagus short,distinct. Caeca terminate blindly close to posterior endof body. Excretory vesicle I-shaped, extends from pos-terior extremity to just posterior to posterior testis.Excretory pore terminal. Lymphatic vessels not ob-served. Testes entire, tandem, in mid-hindbody. Spermducts unite at base of naked seminal vesicle. Semi-nal vesicle saccular, extends distinctly beyond ventralsucker posteriorly. Pars prostatica distinct, directlydorsal to ventral sucker. Ejaculatory duct joined byuterus to form hermaphroditic duct immediately distalto pars prostatica. Hermaphroditic duct runs directly tocommon genital pore. Common genital pore median,immediately anterior to ventral sucker. Ovary entire,antero-dextral to anterior testis. Laurer’s canal opensdorsally between ovary and ventral sucker. Seminalreceptacle canalicular, antero-dorsal to ovary. Vitelline
follicles extend from pharynx to posterior end of body;fields dorsally confluent in forebody, dorsally and ven-trally confluent posterior to testes. Vitelline reservoirimmediately posterior to ovary. Uterus winds betweenanterior testis and ventral sucker before uniting withejaculatory duct dorsal to ventral sucker. Eggs tanned,operculate.Records: 1 Hafeezullah (1970), 2 Wang (1982), 3Rekharani & Madhavi (1985), 4 Present study.Descriptions:1, 4.Hosts: Gerreidae:Gerres filamentosus(1); G. sub-fasciatus(4); Moronidae:Lateolabrax japonicus(2);Mugilidae:Valamugil cunnesius(3).Localities: India (1, 3), Fujian Province, China (2),Queensland, Australia (4).
ComparisonThe specimens reported here agree well with thedescription given by Hafeezullah (1970) forN. kar-warensisfrom Gerres filamentosusfrom India. Thereis no significant point of disagreement. Hafeezullah(1970) observed that the tegumental spines had prob-ably been lost in processing but, given their absencehere and in the closely relatedN. marina (Manter,1947), it seems that they are genuinely absent. Thisspecies is close toN. marina, but the present speci-mens had the same distinction in the distribution ofthe vitelline follicles as observed by Hafeezullah.
Neoapocreadium splendensn. sp.(Figures 12, 15)Type-host: Nemipteridae: Scolopsis monogramma(Cuvier).Type-locality:Heron Is., southern Great Barrier Reef,23◦27′ S, 151◦55′ E.Material examined: S. monogramma, Heron Is., 4specimens, Mar. 1990; 3, Mar 1994; 7, Jan 1993; 4,Sept. 1993; 1, Jan. 1994; 2, Jul. 1994; 3, Jul. 1995.Site:Intestine.Prevalence:7 of 10S. monogrammaexamined.Type-deposition:Holotype and 8 paratypes QM G215032-40; 6 paratypes, BM(NH) Nos 1998.7.10.1–6.
Description
Measurements are of 11 mature specimens (see Ta-ble I). Body flattened, lanceolate, often with dis-tinct constriction at level of ventral sucker. Tegu-mental spines prominent in forebody, less prominentin hindbody. Cercarial eye-spot pigment distributedindistinctly in forebody. Pre-oral lobe distinct. Oralsucker opening subterminally. Prepharynx distinct,
24
short, sometimes entirely within concavity of oralsucker. Caeca terminate blindly close to posterior endof body. Excretory vesicle I-shaped, extends from pos-terior extremity to just posterior to posterior testis.Excretory pore terminal. Lymphatic vessels not ob-served. Testes entire, tandem, in anterior half ofhindbody. Anterior testis more or less quadrangular;posterior testis nearly triangular with distinctively ta-pering posterior end. Sperm ducts unite at base ofnaked seminal vesicle. Seminal vesicle saccular, ex-tends posterior to ventral sucker, sometimes reaches toanterior testis. Pars prostatica distinct, directly dorsalto ventral sucker. Ejaculatory duct joined by uterusto form hermaphroditic duct immediately distal topars prostatica. Hermaphroditic duct runs directly tocommon genital pore. Common genital pore median,immediately anterior to ventral sucker. Ovary entire,antero-dextral to anterior testis; anterior margin usu-ally abuts ventral sucker. Oviduct arises from dorsalsurface of ovary, joined by ducts leading to vitellinereservoir, Laurer’s canal and canalicular seminal re-ceptacle. Vitelline reservoir immediately sinistral toovary. Laurer’s canal opens dorsally between ovaryand ventral sucker. Seminal receptacle antero-dorsalto ovary. Vitelline follicles extend from caecal bifurca-tion to posterior end of body, interrupted prominentlyat level of ventral sucker, confluent dorsally in fore-body, confluent dorsally and ventrally in hindbody.Uterus winds between ovary and ventral sucker beforeuniting with ejaculatory duct dorsal to ventral sucker.Eggs relatively few, tanned, operculate.
ComparisonIn its generally typical apocreadiid features, vitellinefollicles extending into the forebody and presenceof tegumental spines, this species agrees well withNeoapocreadium. The present form is distinct from allNeoapocreadiumspp. exceptN. imtiazi in having thevitelline follicles interrupted distinctly at the level ofthe ventral sucker. It differs fromN. imtiazi in hav-ing an entire rather than tri-lobed ovary, the vitellinefollicles only extending as far anteriorly as the caecalbifurcation (rather than to the oral sucker) and in hav-ing a relatively much longer post-testicular zone. Noneof the species ofNeoapocreadiumwith uninterruptedvitelline follicles exhibit any other particular similar-ity to the present species, so we have no hesitation inproposing a new species for it.
Neoapocreadium bravoae(Sogandares-Bernal, 1959)Siddiqi & Cable, 1960 emend.SynsApocreadium bravoiSogandares-Bernal, 1959;Neoapocreadium bravoi(Sogandares-Bernal, 1959)Siddiqi & Cable, 1960Records:1 Sogandares-Bernal (1959).Descriptions:1.Hosts:Balistidae:Balistes naufragium(1).Localities:Panama, Pacific coast (1).Comment: Sogandares-Bernal (1959) stated unam-biguously that this species was named after Dr Mar-garita Bravo-Hollis, so the specific name is clearly alapsusand needs emendation.
Neoapocreadium caballeroiAhmad, 1987Records:1 Ahmad (1987).Descriptions:1.Hosts:Sillaginidae:Sillago sihama(1).Localities:Arabian Sea (1).
Neoapocreadium caranxi(Bilqees, 1976) n. comb.Syn.Crassicutis caranxiBilqees, 1976Records:1 Bilqees (1976).Descriptions:1.Hosts:Carangidae:Caranx affinis(1).Localities:Karachi Coast, Pakistan (1).Comments: The holotype (BM(NH) 1982.5.13.7)from C. affinis was examined. The specimen is invery poor condition, although it agrees generally withthe published figure and description. It has quite defi-nite eye-spot pigment in the forebody and contrary tothe description, unequivocal spines in the hindbody.These spines necessitate the transfer of this species toNeoapocreadium.
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Table II. Host-parasite checklist of Apocreadiinae and Postporinae.
Localities: Bimini, Bahamas (1), Puerto Rico (2),Panama, Caribbean coast (3), Florida, United States(5, 6), Jamaica (4).Comments:Sogandares-Bernal & Sogandares (1961)recorded this species from the labridHalichoeresbivittatus, but reported that the specimens were metac-ercariae that had come from the muscle of a shrimp inthe fish. This both throws doubt on the authenticity ofthe host record and, perhaps, introduces a new dimen-sion to the diversity of apocreadiid life-cycles.
Our concept of the genus has led to its enlargementto contain 13 species; we observe three groups ofspecies: Group A:N. gerridis, N. imtiazi, N. karwaren-sis andN. marinahave very extensive vitelline folli-cles which reach at least to the pharynx and, exceptfor N. gerridis, are reported to lack tegumental spines;all have oral suckers smaller than the ventral sucker.Group B:N. angustum, N. bravoae, N. chabaudiandN. coili have vitelline follicles not reaching anterior tothe caecal bifurcation and oral suckers distinctly largerthan the ventral sucker and with distinctive longitu-
dinal slits; all possess tegumental spines. Group C:N. caballeroi, N. caranxi, N. malaysiae, N. splendensand N. viguerasihave vitelline follicles not reach-ing anterior to the caecal bifurcation and oral suckerswith standard round apertures; all possess tegumentalspines; all have oral suckers smaller than the ventralsucker.
NeomegasolenaSiddiqi & Cable, 1960
Diagnosis.Tegument spinous. Dispersed eye-spot pig-ment present near pharynx. Oral sucker simple. Phar-ynx massive, larger than ventral sucker. Caecal bifur-cation posterior to ventral sucker. Ventral sucker sim-ple. Caeca blind, extend to near posterior end of body.Excretory vesicle I-shaped, extending to ovary. Ex-cretory pore slightly dorsally subterminal. Lymphaticvessels said to be present. Testes two, tandem. Sem-inal vesicle an elongate tube. Genital pore median,immediately anterior to ventral sucker. Ovary entire.Vitelline follicles restricted to hindbody. Type-species:N. chaetodipteriSiddiqi & Cable, 1960.
CommentsThis genus can be recognised for the combination ofenormous pharynx, caecal bifurcation posterior to theventral sucker and elongate, tubular seminal vesicle.This combination of characters causes this genus andsole species to be quite distinctive within the Apocre-adiidae. The possibility of closer relationship to othergroups should be considered further in the future.
Diagnosis.Tegument spiny. Oral sucker simple. Ven-tral sucker simple. Caeca blind, extend to near poste-rior end of body. Excretory vesicle I-shaped, extendsanteriorly between testes. Excretory pore terminal.Lymphatic vessels absent. Testes two, oblique. Genitalpore median, well anterior to ventral sucker. Ovarydistinctly lobed. Vitelline follicles extend to level of
30
oesophagus. Uterus coils between ovary and genitalpore. Type-species:P. otagoensisManter, 1954.
CommentsThis genus has generally typical apocreadiine featuresbut is distinguished by the deeply lobed ovary and bythe fact that the genital pore opens well anterior tothe ventral sucker. This genital pore position is uniquewithin the subfamily and may suggest that the genusbelongs best elsewhere. The oblique testes with theexcretory vesicle passing between is also distinctive.
Pancreadium otagoensisManter, 1954Records:1 Manter (1954), 2 Wallet & Kohn (1987).Descriptions:1, 2.Hosts: Pinguipedidae:Parapercis colias(1); Sci-aenidae:Cynoscion acoupa(2).Localities:New Zealand (1), Brazil (2).Comment:The very wide geographical distributionand completely unrelated hosts suggests that Wallet& Kohn’s (1987) specimens should be reviewed toensure that they are indeedP. otagoensis.
ProcaudotestisSzidat, 1954
Diagnosis. Tegument smooth. Oral sucker simple.Ventral sucker simple. Caeca blind, extend to near pos-terior end of body. Excretory vesicle I-shaped, extendsto posterior testis. Excretory pore terminal. Lymphaticvessels absent. Testes two, oblique, close to posteriorend of body. Genital pore median, immediately ante-rior to ventral sucker. Ovary entire. Vitelline folliclesrestricted to posterior half of hindbody. Uterus veryextensive, occupies bulk of hindbody. Type-species:P. uruguayensisSzidat, 1954.
CommentThis genus is unique within the Apocreadiinae in hav-ing the testes distant from the ventral sucker and a veryextensive uterus filling the intervening space.
Diagnosis. Tegument smooth. Oral sucker simple.Ventral sucker simple. Caeca unite to form cyclocoel.Excretory vesicle I-shaped, extending anteriorly as faras testes. Excretory pore ventral, anterior to posteriorjunction of cyclocoel. Lymphatic vessels not reported.Testes two, symmetrical. Genital pore median, im-mediately anterior to ventral sucker. Ovary entire.Vitelline follicles extend to pharynx. Type-species:T.haplochromiosDollfus, 1950.
CommentsThis genus is close toCrassicutis, but is distin-guished by the presence of a cyclocoel and symmet-rical testes. Manter (1962) re-examined paratypes ofT. haplochromiosand refigured the whole worm andthe terminal genitalia. He commented on its similarityto Crassicutis, and suggested that the cyclocoel wasthe major distinctive feature.
Diagnosis. This genus and subfamily is defined withinthe family by the genital pore being posterior ratherthan anterior to the ventral sucker. Type-species:P. epinepheli(Manter, 1947).
Simá-Alvarez, & Güemez-Ricalde (1997), 9 Aguirre-Macedo & Bray (in press).Descriptions:1, 2, 7, 8, 9.Hosts: Serranidae:Diplectrum radiale (7), Epine-phelus adscensionis(4), E. guttatus(4), E. morio (1,4, 6, 8, 9),E. striatus(3, 4),Epinephelussp. (2),Myc-teroperca bonaci(5), M. venenosa(1).Localities:Florida, United States (1, 5), Curaçao (4),Jamaica (4), Puerto Rico (3), Bermuda (2), Belize (6),Mexico (8, 9), Venezuela (7).Comments:Siddiqi & Cable (1960) argued convinc-ingly for the synonymy ofP. mycteropercaewith P.epinepheli.Manter (1947) drew attention to the possi-bility that Lepocreadium levenseniof Linton (1910)in part from Mycteroperca venenosamight be syn-onymous with this species. Hanson (1950) reported asimilar worm fromTrachinotussp. from Bermuda.
We have examined the holotype ofOpisthogono-porantesophagus intrususNasir & Gomez, 1977from Diplectrum radialefrom Venezuela (BM(NH)1976.3.19.7) and it is clear that it is a synonym ofP. epinepheli. We have looked closely at the termi-nal genitalia and cannot detect the cirrus-sac Nasir &Gomez (1977) figured.
Discussion
Host-specificity of the Apocreadiinae and Postporinae
Host-parasite records of the Apocreadiinae and Post-porinae are summarised in Table II. These recordsinclude 170 host-parasite combinations. Commentshere refer mainly to the Apocreadiinae as there is onlya single species of the Postporinae. About half thespecies (30 of 58) have been recorded from only asingle host species; most of these have been recordedonly once. Several species (e.g.,Callohelmis piche-linae, Crassicutis cichlasomaeand Homalometronsynagris) are known from a range of closely re-lated hosts. Two species (Homalometron armatumandH. pallidum) show a very broad specificity, hav-ing each been found in more than 10 species andat least five families of fishes. Incomplete collectingnot withstanding, it thus appears that apocreadiids arehighly variable in their host-specificity. No particularexplanation presents itself for this level of variation.
Although 36 families of fishes are recorded ashosts, seven of them (Balistidae, Centrarchidae, Ci-chlidae, Gerreidae, Haemulidae, Sciaenidae and Ser-ranidae) account for more than half of the reported
host-parasite combinations. It is striking that there islittle ecological similarity between these families.
Over 100 different species of fish have been re-ported as hosts of apocreadiines. Remarkably, ofthese, 17 are reported to harbour at least two differ-ent species of apocreadiids. Concentration of infectionin particular host species is most marked in the Bal-istidae in the cases of two Atlantic species,Balistescapriscus(three species) andB. vetula(five species),and the Gerreidae in the cases ofGerres cinereusandG. subfasciatus(three species each). In addition, notonly are infections strikingly diverse in some hosts,they are notably absent in other closely related species.For example, there is an enormous literature concern-ing the trematodes of the approximately 40 species ofbalistid fishes. Yet the 13 host-parasite combinationsof apocreadiines reported from them are from just fiveidentified host species. Further evidence for this con-centration effect comes from our records; we haveexamined 88 specimens of seven species of balistidsfrom the Australian Great Barrier Reef without findingany apocreadiine trematodes.
Taxonomy
We consider the classification that we propose herethe best solution in the light of available information.However, we are far from convinced that this clas-sification will remain stable. The principle problemlies with the characterisation of the family itself. Themain uniting feature is the nature of the terminal gen-italia. Unfortunately, this is in no way unique to thefamily. Several other families (e.g., Cryptogonimidaeand Haplosplanchnidae) have similar terminal geni-talia (naked seminal vesicle and pars prostatica unitingwith uterus to open close to ventral sucker). It seemslikely to us that the typical close proximity of the gen-ital pore to the ventral sucker reflects a role for theventral sucker during copulation.
If the presence of a cirrus-sac is considered prim-itive (plesiomorphy) for the lepocreadioid group withwhich the apocreadiids appear to be associated, thenthe condition of the terminal genitalia has presumablybeen arrived at as a loss. Given that this conditionof the terminal genitalia is not rare within the Dige-nea, it seems plausible that the condition might havearisen more than once. It would be desirable, then,if other characters could be used to help define thefamily. Unfortunately we can find none at present. In-deed some of the variability contained in the family(position of genital pore, position of excretory pore,
32
presence or absence of tegumental spines, the enig-matic lymphatic vessels and the use of very differenthost groups) suggests heterogeneity within the group.
Acknowledgements
We thank the staff of the Heron Island Research Sta-tion and the University of Queensland Trawler forfacilitating much of the collection that led to this study.We also thank Glenn Anderson, Steve Barker, Clin-ton Chambers, Alistair Dove, Sylvie Pichelin, VickiSands and Trudy Wright for assistance with the col-lecting. Trudy Wright did most of the staining andmounting for this study and Desley Scott made thehistological sections. We thank the Australian Biologi-cal Resources Study for the grant which supported thiswork.
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