The terminology of larval cestodes or metacestodes

Systematic Parasitology 52: 1–33, 2002.© 2002 Kluwer Academic Publishers. Printed in the Netherlands.1The terminology of larval cestodes or metacestodesLenta Chervy ∗Central Laboratory of General Ecology, Bulgarian Academy of Sciences, Sofia, BulgariaAccepted for publication 13th August, 2001AbstractThe terminology associated with the nomenclature of larval or metacestodes is reviewed as well as the variousmorphological and developmental characters used to define different types of larval cestodes. Based on a reviewof the literature, the key characters differentiating the types of larval cestodes are the presence of a primary lacunaand the invagination/retraction of the scolex. The presence of a cercomer and of a bladder-like enlargement of thelarval cestode were considered to be useful secondary characteristics. Using these characters, six basic types oflarval cestodes were identified: the procercoid, an alacunate form which cannot develop further until ingested by asecond intermediate host; the plerocercus, an alacunate form with a retracted scolex; the plerocercoid, an alacunateform with an everted scolex; the merocercoid, an alacunate form with an invaginated scolex; the cysticercoid,a lacunate form with a retracted scolex; and the cysticercus, a lacunate form with an invaginated scolex. Thediversity of larval types within the broad classifications of cysticercoid and cysticercus can be differentiated by theuse of appropriate prefixes. Deficiencies in knowledge of specific types of larval cestodes are identified and furtheravenues of research are indicated.IntroductionThe complexity of the terminology applied to larvalcestodes or metacestodes has been lamented by virtuallyall reviewers of this topic (e.g. Voge, 1967;Freeman, 1973; Jarecka, 1975). However, attemptsto rationalise the names applied to larval cestodeshave often resulted in the introduction of more newterms further complicating the situation (e.g. Freeman,1973) with the unfortunate result that the terminologyis not widely utilised (Scholz, 1999). Additional attemptsto rationalise terminology (e.g. Jarecka, 1975)have challenged the understanding of widely acceptedfeatures of metacestode development, such as thoseof the ‘metacestode’ and ‘cercomer’. Again, thesechanges have been adopted by some authors (e.g.Hoberg et al., 1997) but are not universally accepted(e.g. Freeman, 1973). A further complication is thatit is sometimes difficult to extract a definition of apurportedly novel type of larval cestode or even the∗ Pseudonym for the contributors of a workshop on metacestodeterminology, chaired by I. Beveridge, which took place during theThird International Workshop for Tapeworm Systematics, Sofia,Bulgaria, 20-24 July, 1999 (Organiser: B.B. Georgiev).modification of a classical term from the paper inwhich the new or modified term is presented or the existingterm re-defined (e.g. ‘plerocercoid’ in Freeman,1973). In addition, in competing systems of terminology,the same term can have different meanings(Freeman, 1973; Jarecka, 1975). Nevertheless, somefeatures and terms remain consistent in all competingsystems for the terminology of metacestodes.The aims of this review are: (i) to compare thevarious systems of terminology; (ii) to determine areasof agreement and disagreement among variousproposals for larval cestode terminology; (iii) for areasof disagreement, to analyse the characters whichhave been utilised in developing the terminology andtheir homology, identifying characters which are plesiomorphicor apomorphic both within and betweengroups; and (iv) to attempt to resolve areas of disagreement.Hopefully any new system would be predictivewithin a phylogenetic context and facilitate phylogeneticresolution within the eucestodes generally. Inproposing any revised system of terminology, a subsidiaryaim is to avoid the unnecessary introduction ofnew terms. Apart from this principle, the one underlyingideological view adopted in this review is that

2espoused by Joyeux & Baer (1961, p. 450) in theircomprehensive review of cestode life-cycles known atthat time, namely that ‘nous espérons gagner en clartéen les reduisant au minimum’ (literally, we hope togain clarity by reducing them to a minimum). Such ananalysis might result in a system of nomenclature thatis both functional, is based on the criterion of homologyand provides phylogenetic insights. The currentreview results from a workshop held during the 3rd InternationalWorkshop for Tapeworm Systematics, heldin Sofia in 1999 at which agreement was reached thata simpler system of nomenclature for larval cestodeswas needed, even if morphological and developmentaldetails have not yet been resolved.The review utilises the taxonomic arrangement forthe cestodes proposed by Khalil et al. (1994) butaccepts the cyclophyllidean family Gryporhynchidae,following Spasskii & Spasskaya (1973) and Hoberget al. (1999).Historical account of existing systems ofterminologyOriginsThe existing terminology for larval cestodes has developedover a considerable period of time and atits inception utilised generic names. The first wasScolex, applied by Müller (1787) for larval tetraphyllideans.Zeder (1800, 1803) divided the larvalcestodes known at his time into two groups, monocephaliccestodes to which he applied the genericname Cysticercus and polycephalic cestodes for whichthe name Polycephalus was used. Rudolphi (1819,pp. 177, 536) retained the genus Cysticercus but replacedPolycephalus with two new names, Coenurus,for polycephalic larval cestodes in which proliferationwas ‘exogenous’ and Echinococcus for cestodesin which proliferation was considered to be ‘endogenous’.These genera were placed in the order Cystica,which was separate from that of the adult tapeworms,the order Cestoidea. At the time, there was virtuallyno understanding of cestode life-cycles and littlecomprehension that the ‘cystic’ forms were the larvalstages of the Cestoidea. This was particularly thecase in the Tetraphyllidea where species of Scolexexhibited strikingly different morphology to the correspondingadults. The generic names Dithyridium andTetrathyridium were also erected by Rudolphi (1819,p. 559), the first for a cestode of uncertain identityfrom the liver of a lizard and the second from a partridge;neither was allocated to an order. The genusScolex was used by Rudolphi (1819, pp. 124, 198)to include a variety of larval tetraphyllidean cestodes,although the genus was placed in the Cestoidea ratherthan in the Cystica. Subsequently, Diesing (1850) subdividedthe genus Cysticercus into those with armedscoleces, retained in Cysticercus, and those with unarmedscoleces, placed in a new genus Pietocystis,a division subsequently suppressed by Villot (1883,p. 5). Thus the nomenclature used at this stage waspurely descriptive, utilised the most obvious charactersavailable (monocephaly versus polycephaly)and predated any detailed understanding of the basiclife-cycles of cestodes.CysticercoidsLeuckart (1876) introduced the term cysticercoid fora variety of larval cestodes known at the time, mainlyfrom invertebrates, differentiating them primarily ‘intheir minuteness and in the absence of fluid’. The termwas subsequently used as a generic name, Cysticercoides(e.g. Braun, 1894, p. 1559)Villot (1883) considered that Leuckart‘s groupof cysticercoids was highly heterogeneous and reorganisedthem such that only parasites of invertebrateswere involved. This involved moving Gryporhynchus,a larval stage without cercomer, foundin fresh-water fish and now known to be a gryporhynchid,to the ‘cysticerci’ and utilising a numberof new generic names for remaining larval forms. Thefirst group, with two genera, was characterised byendogenous development. Polycercus was proposedfor the polycephalic larva described by Metchnikov(1869) from Lumbricus terrestris, which are larvaeof a dilepidid genus. Monocercus was erected forCysticercus arionis of von Siebold (1850) found inthe mollusc Arion empiricorum, and now consideredto be the dilepidid Molluscotaenia crassiscolex (seeGulyaev & Kornienko, 1998).The second group, characterised by exogenousdevelopment included the genera Cercocystis, Cryptocystis,Urocystis and Staphylocystis. Cercocystis waserected for a cysticercoid found in Tenebrio molitorby Stein (1875), named Cysticercus tenebrionis, andthought to be the larval stage of the hymenolepididRodentolepis microstoma. Cryptocystis contained C.trichodectis, a larva found in the body-cavity of thedog louse Trichodectes canis by Melnikov (1869) andnow known to be the larval stage of Dipylidium can-

3inum (= Taenia cucumerina). Both Leuckart (1876)and Moniez (1880) noted that the scolex was invaginated,as occurs in Echinococcus, rather than retractedas in the related cysticercoids. Urocystis and Staphylocystiswere both erected for polycephalic larvae foundin a variety of invertebrates, which are now knownto be larval stages of hymenolepidids from shrews(Joyeux & Baer, 1961).The terms employed by Zeder (1800), Rudolphi(1819), Villot (1877, 1882, 1883), Braun (1883)and other authors were incorporated by Braun (1894,p. 1,567) into his synopsis of types of larval cestodes(Table 1). Subsequently, most of the names ceased tobe used as generic names but were retained in slightlymodified forms to describe types of larval cestodes.A full list of such names was provided by Freeman(1973).Terms for pseudophyllideans and trypanorhynchsOriginating from studies on the life cycles of pseudophyllideancestodes came the term procercoid todescribe the first larval stage in the crustacean intermediatehost (Janicki & Rosen, 1917) characterisedby the lack of a primary lacuna and the presence of atail-like appendage termed the cercomer. The pseudophyllideanstage in the second, vertebrate intermediatehost was termed a plerocercoid by Braun (1883) andwas also used subsequently as a generic name, Plerocercoides(e.g. Braun, 1894, p. 1,559). Plerocercoidswere characterised as having a solid body and havingthe future scolex develop externally (Figure 1).The term plerocercus was also proposed by Braun(1883) for the larval stage of trypanorhynch cestodes,in which the scolex forms retracted within a blastocyst.Dollfus (1946, p. 66) provided a detailed comparisonof the structure of plerocerci and plerocercoids; hisoriginal drawings having been utilised subsequentlyby Wardle & McLeod (1952, p. 296) and Campbell& Beveridge (1994, p. 54). Dollfus (1946) utilised forhis illustration of a plerocercoid, a species of Phyllobothrium,showing invagination of the scolex withinthe pars proliferans of the scolex. Wardle & McLeod(1952, p. 66) subsequently defined a plerocercoid ashaving an invaginated scolex. However, most plerocercoidshave an evaginated scolex, such as thoseof Diphyllobothrium, Triaenophorus and Abothrium(See Rosen 1919, p. 261, plate I, figure 3, p. 273, plateIII, figure 5) as well as the tetraphyllideans Scolexpolymorphus and S. pleuronectis. Hence, the term plerocercoidhas been used for larval stages with bothinvaginated and non- invaginated scoleces. In addition,S. bothriosimplex, with a single apical sucker, isprobably the larval stage of a tetrabothriidean (Hoberg,1987), further complicating the the analysis of theearly application of this term.An additional term, merocercoid, for the larvalstage of Triaenophorus nodulosus was attributed toJanicki by Rosen (1919, p. 298), although the publicationof the name was not cited. Rosen (1919)dismissed Janicki‘s use of a novel term, insisting thatthe larva in question was a plerocercoid. The termappears not to have been employed subsequently forpseudophyllidean larvae.In a review of types of cestode larvae, Fuhrmann(1933) used the terms procercoid and plerocercoidfor stages of pseudophyllidean life-cycles, as wellas the older terms cysticercus and cysticercoid (incorporatingcryptocystis and cercocystis), plerocercusand dithyridium (for Mesocestoides), in additionto the new term merocercus for the metacestodeof the lecanicephalidean genus Lecanicephalum (seeFuhrmann, 1933, p. 240).Particular terms for metacestodes were not necessarilyrestricted to a single taxonomic group ascysticercus was applied not only to the metacestodesof taeniids but also to tetraphyllidean metacestodes(Monorygma grimaldii). Rudolphi (1819) had previouslyapplied the term cysticercus to the metacestodeof another tetraphyllidean, Phyllobothrium delphini.An additional feature of Fuhrmann‘s (1933)description of cestode larval stages was that he referredto both Dithyridium and Gryporhynchus asplerocercoids; that is, he applied the term plerocercoidto bothriate and acetabulate metacestodes, andhe (p. 202) clearly distinguished between metacestodeswith invaginated scoleces (zurükgezogen) andwithdrawn scoleces (zurückzieht).Fuhrmann’s (1933) terms for metacestodes werewidely adopted in western Europe and were addedto by Joyeux & Baer (1945), who proposed the termmerocercoid for the metacestode of the cyclophyllideancestode Catenotaenia pusilla, characterised bythe possession of an apical sucker which is lost duringdevelopment in the adult. They were apparentlyunaware of its prior use by Rosen (1917) for pseudophyllideans.Dollfus’ (1942) classic monograph onthe Trypanorhyncha firmly established the use of theterm plerocercus for trypanorhynch metacestodes, althoughthe term was ignored by Joyeux & Baer (1961)and Wardle & McLeod (1951) in favour of plero-

4Figure 1. Schematic representation of patterns of larval development in the orders (A) Caryophyllidea, (B) Pseudophyllidea, (C) Haplobothriidea,(D) Trypanorhyncha, (E) Tetraphyllidea and (F) Nippotaeniidea.

5Table 1. Names of larval cestodes utilised by Braun (1894) in one of the earliestsynopses of terminology together and their origins.Group I Cysticerci Original use of term:1. Cysticercus Zeder (1800)2. Coenurus Rudolphi (1819)3. Echinococcus Rudolphi (1819)Group II Cysticercoids Original use of term: Leuckart (1867)Sub-group (a) - with endogenous development1. Polycercus based on the description of a larval cestode in anannelid, Lumbricus, by Metchnikoff (1869) (=Paricterotaenia) (Dilepididae).2. Monocercus based on a cysticercoid from a mollusc, Arionempiricorum, by von Siebold (1850), nowMolluscotaenia (Dilepididae).Sub-group (b) - with exogenous development1. Cercocystis based on cysticercoids developing in a beetle,Tenebrio molitor, described by Stein (1975),probably the larva of Rodentolepis microstoma.2. Staphylocystis based on cysticercoids found in a myriapod,Glomeris limbatus, by Villot (1877), adultStaphylocystis pistillum, in shrews.3. Urocystis based on cysticercoids found in myriapods G.conspers and G. marginata by Villot (1882).4. Cryptocystis based on the larvae of Dipylidium caninum(= Taenia cucumerina) in a louse, Trichodectescanis, described by Melnikov (1869).cercoid. Dollfus (1946) also excluded the athecatetrypanorhynchs (Homeacanthoidea) from the types ofcestodes characterised by a plerocercoid, referring tothem instead as postlarvae. The most comprehensivesummary of cestode life-cycles published in the subsequentdecades, that of Joyeux & Baer (1961), furtherestablished the use of the terms procercoid, plerocercoid,cysticercus and cysticercoid in the westernEuropean literature (Figures 1,2).Skrjabin and colleaguesA significant elaboration of the traditional terms wasmade by Russian workers under the leadership of K.I.Skrjabin. Skrjabin & Mathevossian (1942) divided thedevelopment of the metacestode of hymenolepididsinto six stages: (1) the oncosphere; (2) the megalosphere(with a central cavity termed the primarylacuna); (3) the metamere, subdivided into caput, collum,soma and cerca or cercomer of other authors;(4) scolexogeny, during which the rostellum and suckersbegin development in the caput; (5) the stage of‘invagination’ in which the caput and collum are retractedwithin the soma; and (6) the fully-developedcysticercoid, termed a larvicyst. The term larvicysthad been coined by Skrjabin (1937) to denote anymetacestode of the order Cyclophyllidea, irrespectiveof its final structure. Skrjabin & Mathevossian (1945)also used the spelling ‘larvocyst’.Larvicysts of hymenolepidids were subdivided bySkrjabin & Mathevossian (1942) into various morphologicalcharacters based in part on the work of Villot(1883) (Table 2), the key characters being: (1) presenceor absence of a cercomer; (2) ratio of length ofcercomer to the rest of the cysticercoid; (3) structureof the membranes investing the scolex; and (4) modeof scolex formation (e.g. by budding). The termsthey adopted to describe cysticercoids, taken in partfrom earlier authors, were staphylocyst, urocyst, cer-

6Table 2. Terms used in the literature, other than procercoid, plerocercoid, plerocercus, cysticercoid and cysticercus, to describecyclophyllidean larval stages. The table excludes terms used by Jarecka (1970) and Freeman (1973).Family Term Description, example ReferenceHymenolepididaestaphylocyst mycelium-like, polycephalic Skrjabin & Mathevossian (1942)urocyst new cysts budded from base Skrjabin & Mathevossian (1942)cercocyst long cercomer Skrjabin & Mathevossian (1942)ramicercus branched cercomer Skrjabin & Mathevossian (1942)microcercus reduced cercomer, Hymenolepis nana Skrjabin & Mathevossian (1942)diplocyst no cercomer, Aploparaksis crassirostris Skrjabin & Mathevossian (1942)floricyst caudate diplocyst, Aploparaksis birulai Bondarenko & Kontrimavichus (1976)Dilepididaeacerocyst no primary lacuna, Dilepis undula Gulyaev (1997b)monocercus cercomer degenerates into globules Villot (1883); Gabrion & Helluy (1982);Gulyaev & Kornienko (1998)cryptocercus cercomer degenerates into globulespolycercus cercomer forms enclosing cyst Villot (1883); Gulyaev & Kornienko (1998)cercoscolex Gryporhynchinae Jarecka (1971a,b)strobilocyst segmented region in metacestode, Lateriporus Shapkin & Gulyaev (1973)Anoplocephalidaeamphicyst Linstowiinae Spasskii (1951)Taeniidae (s.l.)coenurus polycephalic cysticercus Abuladze (1964)strobilocercus segmented region of metacestode, Taenia taeniaeformis Abuladze (1964)fimbriocercus T. martis, T. mustelae, T. twitchelli, T. brachyacantha Kornyushin & Sharpilo (1986)armatetrathyridium T. polyacantha Abuladze (1964)hemistrobilocercus T. rileyi Rausch (1981)coenurostrobilocercus T. krepkorgorski Agapova (1950)hydatid Echinococcus granulosus Rudolphi (1819); Abuladze (1964)alveohydatid Alveococcus multilocularis Abuladze (1964)Paruterinidaecladothyridium Cladotaenia, Paruterina Abuladze (1964)Mesocestoididaetetrathyridium Mesocestoides spp. Voge (1967)Amabiliidaeascocercus Gulyaev (1989)Catenotaeniidaemerocercoid Catenotaenia pusilla Joyeux & Baer (1945)cocyst and monocercus, but included the new termsramicercus, microcercus and diplocyst.In the series of texts, Essentials of cestodology, additionalterms were utilised (Table 2). Spasskii (1951)in a review of the Anoplocephalata utilised the termamphicyst first proposed by him (Spaskii, 1949) forthe larvae of linstowiids. Abuladze (1964) utilised avariety of terms for taeniid larvae (then encompassingthe genera Cladotaenia and Paruterina, whichare currently placed in the Paruterinidae) (Table 2),using in addition to the traditional terms cysticercus,coenurus and echinococcus (= hydatid), those of strobilocercus,alveohydatid, armatetrathyridium andcladothyridium. To these have been added fimbriocercusby Kornyushin & Sharpilo (1986), hemistrobilocercusby Rausch (1981) and coenurostrobilocercusby Agapova (1950).

Figure 2. Schematic representation of patterns of larval development in the orders Proteocephalidea and Cyclophyllidea, the latter beingillustrated by representatives of the families (or sub-families) Paruterinidae, Taeniidae, Linstowiinae, Dipylidiinae, Gryporhynchidae,Hymenolepididae, Davaineidae, Dilepididae, Anoplocephalidae and Amabiliidae.7

8Jarecka and FreemanTwo additional systems of larval cestode terminologywere developed essentially contemporaneously(Jarecka, 1970a,b, 1975; Freeman, 1973) and sharea common feature, derived from Moniez (1880) andVillot (1883), namely that features observable duringdevelopment, particularly the presence or absence ofa cercomer and a primary lacuna are given considerablesignificance. Beyond this commonality, theydiffer in that the system of Freeman (1973) subsequentlyrelied on larval cestode morphology alone,while that of Jarecka (1975) incorporated, as a feature,whether the cestode larva occurred in its first or secondintermediate host (Table 3).In the system proposed by Jarecka (1970a,b,1975), larval cestodes in the first intermediate hostwere termed cercoids, while those in a second intermediatehost were termed metacercoids. Cercoidscould possess a cercomer, but, by definition, metacercoidslacked a cercomer. Cercoids were sub-dividedinto the: (1) procercoid, which is bothriate but lacksa primary lacuna (gymnosomic in the terminologyof Jarecka, 1975); (2) cercoscolex, which is acetabulate,lacks a primary lacuna and has a withdrawnor retracted scolex (= Gryporhynchus of earlier authors);(3) cysticercoid, which has a primary lacuna(cystosomic in the terminology of Jarecka, 1975), isacetabulate and has a withdrawn scolex; and (4) cysticercus,which is acetabulate, invaginated and lacks acercomer. The metacercoid, in the second intermediatehost, lacks a cercomer and may be either a bothriateplerocercoid or an acetabulate plerocercus. Thesystem of terminology proposed by Jarecka (1970a,b,1975) thus retains the traditional terms cysticercus,cysticercoid and plerocercoid. Procercoid was originallyapplied to the caudate (= with cercomer) stagesof pseudophyllideans in the first intermediate hostprior to development of the bothria (Janicki & Rosen,1917). The re-definition of the term by Jarecka (1975)meant that it also included the caudate, bothriate larvalcestodes of caryophyllideans and overcame theanomaly, for pseudophyllideans, of development ineither two intermediate hosts (e.g. Diphyllobothrium,Ligula; see Janicki & Rosen, 1917; Rosen 1920) ora single intermediate host (e.g. Bothriocephalus; seeRobert et al. 1988; Scholz, 1997). Her term ‘cercoscolex’described proteocephalidean metacestodes(Scholz, 1997) as well as those of the family Gryporhynchidae.The term plerocercus, previously appliedto trypanorhynch metacestodes retracted withina bladder-like cysts (Dollfus, 1942), was used forunspecified acetabulate cestodes in the second intermediatehost. Under her system, trypanorhynchanmetacestodes would have been termed plerocercoids.A subsequent modification of this system was proposedby Gulyaev (1997a) to include presumed stagesin the evolution of larval cestodes, in which Spasskii’s(1951) term amphicyst, for linstowiid metacestodes,was added to the range of cercoids, tetrathyridiumwas added to the range of metacercoids and theterm plerocercoid was replaced by blastocyst for trypanorhynchmetacestodes (Table 4). Gulyaev (1997a)introduced two additional terms (Table 4), protolarvafor metacestodes lacking a primary lacuna and larvacystoidsfor metacestodes lacking a cercomer orbladder, but retained the term larvacyst (= larvicyst)of Skrjabin (1937) for cysticercoids, cysticerci and theblastocysts of trypanorhynchs.The system utilised by Freeman (1973) (Table 3)differed in that, while incorporating the absence orpresence of a primary lacuna (termed ‘primitive’and ‘neoteric’, respectively) and the presence or absenceof a cercomer, the number of intermediate hostswas essentially disregarded and the morphology ofthe larval cestode only was considered. In Freeman’ssystem (1973), the traditional terms procercoid, cysticercus,cysticercoid and plerocercus were retained.Several new terms were used by Freeman (1973). Precysticercuswas coined for metacestodes without acercomer, with a primary lacuna and in which thescolex was invaginated (e.g. Linstowiidae). This termis synonymous with amphicyst of Spasskii (1951)and Gulyaev (1997a). The term neoplerocercoid wascoined for trypanorhynch metacestodes lacking a blastocyst(Freeman, 1973, p. 511), currently allocated tothe suborder Homeacanthoidea by Campbell & Beveridge(1994). However, Freeman (1973, p. 521) alsosuggested that the same term, neoplerocercoid (pp.521, 528-9), could be applied to anoplocephalid andhymenolepidid metacestodes based upon the developmentof the scolex from the ‘fore body’ (p. 521) andlacking a cercomer in their fully-developed form. Itmay be that Freeman intended to use the term neoplerocercusfor trypanorhynchs and neoplercercoidfor cyclophyllideans, but that there are typographicalerrors in the published paper. Freeman’s term postplerocercoidwas coined for larval cestodes such as thoseof Ligula, in which evidence of segmentation is apparentin the larval stage. The other term coined by Freeman(1973) was strobilocysticercoid for Lateriporus,in which segmentation is present in the larval cestode.

9Table 3. Comparison of the systems of nomenclature of cestode developmental stages adopted by Jarecka (1970a,b,1975) and Freeman (1973a,b).Jarecka (1970a,b, 1975) Freeman (1973)1. Oncosphere 1. Oncosphere2. Cercoid 2. Metacestode(stage in first intermediate host)(a) procercoid(a) procercoid(bothriate, no primary lacuna)(no lacuna or scolex)(b) cercoscolex(no primary lacuna, acetabulate, invaginated or withdrawn)(c)cysticercoid(lacuna, acetabulate scolex retracted)(d) cysticercus(lacuna, no cercomer, inverted scolex, bladder)(b) plerocercoid I, II, III, etc.(no lacuna, with scolex)(c) cysticercoid(lacuna, acetabulate scolex retracted)(d) cysticercus(lacuna, no cercomer, inverted bladder)3. Metacercoid (e) precysticercus(stage in second intermediate host)(lacuna, invaginated, no cercomer or bladder)(a) plerocercoid(bothriate)(b) plerocercus(acetabulate)(f) precysticercoid(? no lacuna, retracted, cercomer)(g) plerocercus(no lacuna, retracted, bothriate)(h) neopleroceroid(no lacuna, bothriate)This term parallels strobilocysticercus (= strobilocercus)for the larval cestode of Taenia taeniaeformis andrelated members of the genus Taenia.The term plerocercoid was used by Freeman(1973) for a wide range of both bothriate and acetabulatemetacestodes, thereby broadening its application,although Fuhrmann (1933) had previously used theterm for certain acetabulate forms. Among the newnames suggested by Freeman (1973, Table IV), themost commonly used term is plerocercoid. However,a precise definition of it is difficult to derive from thetext of the paper (Jarecka, 1975), as Freeman (1973,p. 509) defined it simply as a metacestode without aprimary lacuna. For additional morphological details,Freeman (1973) suggested the addition of a seriesof prefixes to describe the basic morphological features(e.g. caudate, acetabulate, bothriate, rostellate,anacanthate, etc.) (Table 5).Both Jarecka (1975) and Freeman (1973) had theopportunity to comment on one another’s proposalsand their respective criticisms are instructive.(a) Jarecka (1975) criticised the terminology ofFreeman (1973) for not incorporating the intermediatehost stage, although Freeman does deal withparatenic hosts by numbering the plerocercoids, I, IIor III, depending upon the number of second intermediate/paratenichosts in the life-cycle. However, this isimpossible for any cestode whose entire life-cycle hasnot yet been elucidated.(b) Jarecka (1975) also avoided the term metacestode,using cercoid and metacercoid instead. Freeman(1973) restricted the term ‘larva’ to the developmentalstage present within the cestode egg, whileJarecka (1973) considered this stage to be the firststagelarva and those within intermediate hosts tobe second- or third-stage larvae. Metacestode mayappear to be etymologically inappropriate, since itscommon zoological use means behind or hindermostas applied to the thoracic segments of insects (pro-,meso-, meta-). Wardle & McLeod (1952) suggestedthe term metacestode to indicate a ‘changing’ cestode(Freeman, 1973), a meaning for the prefix ‘meta-’encompassed within the various uses of the term ac-

10Table 4. System of nomenclature of cestode larval stages proposedby Gulyaev (1997a) based on that of Jarecka (1975) withevolutionary stages addedFirst intermediate hostMetacestodesSecond intermediate hostCercoid Metacercoids PostlarvaProcercoidCercoscolexPlerocercoidProtolarvaAmphicyst Tetrathyridium LarvacystoidCysticercus Blastocyst LarvacystCysticercoidcepted by the Shorter Oxford Dictionary and utilisedin zoological terms such as metamorphosis. Cercoidis a useful term in that it is a component of many ofthe names of known larval forms, but suffers from thedisadvantage that not all names (e.g. cysticercus) areformed from it. Because of differences of opinion, theneutral term larva is used in this review.(c) Freeman (1973) objected to Jarecka’s (1970)division of larval cestodes into cercoids and metacercoids(cercoids which have lost their cercomer) on thegrounds that many groups of cestodes do not possesscercomers in the early stages of development. Jarecka(1975) and Jarecka et al. (1981), however, have arguedthat, based on the earlier views of Janicki & Rosen(1917), all cestodes possess cercomers but they differin form. Jarecka et al. (1981) argued that the cercomersof procercoids, the cyst walls of cysticercoidsand the bladders of cysticerci are homologous, as theyall possess microvilli on their surfaces and they aretherefore modifications of the cercomer. An additionalpotential objection to the system of Jarecka (1975)would be that it does not deal with paratenic hosts,a phenomenon which is common within the Pseudophyllidea(e.g. Mueller, 1938; Robert et al., 1988) andin the Proteocephalidea (e.g. Biserkov & Genov, 1988;Biserkov & Kostadinova, 1997).(d) One particular term, cercoscolex, warrantsspecific comment as it has an extremely confusedusage. It was coined by Jarecka (1970a,b) for caudate,non-lacunate cestode larvae with invaginatedscoleces, which lose their cercomers in a secondintermediate host and was applied to the generaValipora, Paradilepis and Neogryporhynchus, currentlyincluded in the family Gryporhynchidae (seeSpasskii & Spasskaya (1973) for definition of theGryporhynchinae) thereby conforming with the usageby Leuckart (1876) and Villot (1883) under the term‘gryporhynchus’ or ‘gryporhynque’. In 1975, Jareckaexpanded the definition to include other acetabulatemetacestodes lacking a primary lacuna (e.g. Proteocephalidea)as well as those in which the primarylacuna was a transitory feature (Dipylidium). Jareckaet al. (1981) subsequently extended the term to includethe dilepidid genera Paricterotaenia and Anomotaenia,which have withdrawn scoleces and to anymetacestode with microtriches rather than microvillion the cyst wall. They subsequently asserted (Jareckaet al., 1984) that this metacestode was typical fordilepidids. Freeman (1973) by contrast used the termprecysticercoid for the metacestodes of Choanotaeniaand other related dilepidid genera. Gabrion & Helluy(1982) reviewed the morphogenesis of metacestodesof the Dilepididae and concluded that the term monocercusof Villot (1883) applied to 31 dilepidid speciesin which an elongate cercomer disintegrated into globuleswhich persist in the metacestode. They consideredthat the monocercus was characteristic of the Dilepididae.The terminology applied to metacestodes of theDilepididae is therefore particularly complex.More recent additionsMore recent modifications to these systems of terminologyare essentally restricted to cysticerci andcysticercoids. However, significant advances in understandingof the life-cycles of terabothriideans,in which the larval stage was recognised as auniacetabulo-plerocercoid (Hoberg, 1987; Galkin,1996), have also been made without the introduction

11Table 5. Nomenclature employed by Freeman (1973) to describe the larval stages of cestodes, as modified byUbelaker (1983).Cestode taxon Definition ExampleTermHymenolepididae/Anoplocephalidae/Davaineidae/Dilepididaerostello-cysticercoidwith rostellumarostello-cysticercoid no rostellum Anoplocephalinaeanacanthorostello-cysticercoid without hooks Hymenolepis diminutaacanthorostello-cysticercoid with hooks Hymenolepis nanacaudate-cysticercoidwith cercomeracaudate-cysticercoidwithout cercomerlongicaudate-cysticercoid with long cercomer Drepanidotaenia lanceolatabrevicaudate-cysticercoid with short cercomer Raillietina spp.circumcaudate-cysticercoidAploparaksis spp.micranthorostello-cysticercoid with small hooks Davainea proglottinaprecysticercoidChoanotaenia spp.Taeniidaeheteracantho-cysticercustwo rows of dissimilar hooks Taenia soliumhomeacantho-cysticercus hooks similar Fossor, Monorodotaeniaanacantho-cysticercus lacking hooks Taenia saginatastrobilo-cysticercus segmentation in metacestode Taenia taeniaeformis, T. polyacanthamulticephalo-cysticercus multiple scoleces Taenia serialisGryporhynchidaeacanthacetabulo-plerocercoidLinstowiinaeprecysticercusMesocestoididaeinvaginated acetabulo-plerocercoidValiporaOochoristicaMesocestoidesNippotaeniideauni-acetabulo-plerocercoidProteocephalideaglandacetabulo-plerocercoidOphiotaenia filaroidesinvaginated acetabulo-plerocercoid plerocercoid I Corallotaenia minutamet-acetabulo-plerocercoid plerocercoid IIculci-acetabulo-plerocercoidProteocephalus parallacticusPseudophyllideaacaudate bothrio-plerocercoidstrobilobothriate-plerocercoidEubothrium salveliniDiphyllobothrium dendriticumHaplobothriideatentaculo-plerocercoidCaryophyllideacaudate post-plerocercoidSpathebothriidea(a)caudate–adultArchigetes, CaryophyllaeusCyathocephalus, BothrimonusTetraphyllideabothrio - plerocercoidTrypanorhynchatentaculo - plerocercoidneoplerocercoidLacistorhynchus tenuis

12of novel names.Cysticerci and their modificationsA variety of terms have been utilised to describemono- and polycephalic cysticerci (Table 2), andthese have recently been reviewed by Hoberg et al.(2000). They recognised, apart from the cysticercus,the coenurus in which new scoleces develop by invaginationinto a central bladder (Taenia multiceps, T.serialis), the fimbriocercus, an elongate unsegmentedlarva (T. brachyacantha, T. martis, T. polyacantha)(includes armatetrathyridium) and strobilocercus, witha strobilate collum (including hemistrobilocercus andcoenurostrobilocercus) (T rileyi, T. parva, T. taeniaeformis).They identified a further group of species(T. endothoracicus, T. selousi, T. twitchelli) in whichscoleces are borne on long stalks that arise by exogenousbudding from a central bladder which laterregresses, but for which no name was provided. Inaddition, the terms echinococcus and alveococcusremain for specialised larval cestodes of the genusEchinococcus which are also modified cysticerci.Cysticercoids and their modificationsA number of new terms have been introduced for cysticercoidssuch that the literature on this topic is confusing.Not only have numerous terms been coined,often without acknowledgment of a pre-existing term,but existing terms have been applied incorrectly andthe identity of cestodes described based on larvalforms has often been disputed, thus jeopardising theapplication of the terminology. Consequently, theprincipal terms used to describe cysticercoids arebriefly reviewed.(a) Monocephalic cysticercoids1. Cercocyst (Figure 3A)The cercocyst, originally described by Villot(1883), was based on a larval cestode with a prominent,broad cercomer found in the beetle Tenebriomolitor. It was presumed to be Hymenolepis microstoma,the development of which was describedin greater detail by Caley (1974). Cysticercoidswith cercomers longer than the soma, but withoutlateral outgrowths were considered to be cercocystsby Skrjabin & Mathevossian (1942). Considerablevariation occurs within this group as thecercomer may be long and slender or may be extremelybroad. Numerous hymenolepidid generahave cysticercoids of this type, including Cladogynia(=Flamingolepis) (see Gabrion, 1981), Dicranotaenia(see Neradová-Valkounová, 1971),Diorchis (see Czaplinski & Szelenbaum-Cielecka,1986), Drepanidotaenia (see Ruszkowski, 1932),Fimbriaria (see Neradová-Valkounová, 1971 (describedas a monocercus); Krashnoshchekov &Pluzhnikov, 1984), Fimbriarioides (see Maksimova,1976), Gastrotaenia (see Wisniewski,1971), Hymenolepis diminuta (see Voge, 1960;Gabrion, 1981), H. (s.l.) haldemani (see Bondarenkoet al., 1987), H. citelli (see Voge, 1956),Microsomacanthus (Hymenolepis (s.l.) hopkinsi)(see McLaughlin & Burt, 1970), (H.(s.l.) stylosa)(see Gabrion, 1981, 1977), Nematoparataenia(see Wisniewski, 1971), Parabisaccanthes (seeJarecka, 1960, cited as Drepanidotaenia; Kotecki,1967; Maksimova, 1972), Pseudhymenolepis (seeGabrion, 1981; Jiang et al., 1990), Retinometra(see Jarecka, 1960; Maksimova, 1972; Szelenbaum,1972), Rodentolepis (see Prokopič,1971; Ebermann, 1976), Triodontolepis (seeMatsaberidze et al., 1986), Staphylocystis (seeGabrion, 1981), Wardoides (see Kotecki, 1967);and some species of Wardium (e.g. W. aequabile,W. arctowskii, W. fusa, W. paraporale) (seeGabrion, 1981; Jarecka, 1960, 1984; Maksimova,1986). Cercocysts are thus widespread in the Hymenolepididaeand the majority known are fromcestodes occurring as the adult stage in aquaticbirds. No differentiation has been made betweenspecies which undergo scolex development priorto retraction (‘protocephalic’ scolex developmentof Greaves et al., 1989) (e.g. H. diminuta, seeVoge, 1960) and those in which scolex developmentoccurs following retraction (‘epicephalic’scolex development) (R. microstoma, see Goodchild& Stulken, 1970). Greaves et al. (1989) andJarecka (1975) considered the former mode of developmentprimitive or plesiomorphic. Cercocystsalso occur in the life-cycle of the progynotaeniidgenus Gynandrotaenia (see Gvozdev & Maksimova,1979).2. Microcercus (Figure 3B)Microcercus was a term used initially by Skrjabin& Mathevossian (1942) to designate cysticercoids‘whose caudal annex is greatly reduced, being considerablyshorter than the soma’ (p. 85). Theyselected Rodentolepis fraterna as the exemplarfor this type of cysticercoid. R. fraterna has ashort, broad cercomer in mammalian hosts, but a

13broad and elongate cercomer in coleopteran hosts(Voge & Heyneman, 1957; Schiller, 1959; Voge,1961; Joyeux & Baer, 1961). In addition, bothH. citelli and Microsomacanthus ductilis have cercomersjust slightly shorter than the soma (Voge,1961; Burt & Jarecka, 1984), indicating that therelative size of the cercomer may be difficult toevaluate in certain cases. The intention of thedefinition proposed by Skrjabin & Mathevossian(1942) to distinguish cysticercoids with a greatlyreduced cercomer is readily applicable to those ofthe davaineid genera Raillietina (seeWetzel, 1934;Voge, 1960; Bartel, 1965) and Davainea (see Wetzel,1932; Abdou, 1958). The criterion does notapply to all davaineids as Ophryocotyle has anelongate cercomer (Burt, 1962). Therefore, the definitionof a microcercus is potentially useful, buthas been misapplied in the literature.3. Diplocyst (Figure 3C)The diplocyst was defined initially by Skrjabin& Mathevossian (1942) as a cysticercoid with nocercomer or ‘caudal annex’ in which there aretwo separate retractions into the soma. The descriptionwas based on a cysticercoid describedby Mrázek (1906) from earthworms. Skrjabin& Mathevossian (1942) nominated Aploparaksiscrassirostris as a representative of this type ofcysticercoid.Most species exhibiting the development of adiplocyst belong to Aploparaksis, a hymenolepididgenus parasitic mainly in charadriiform birdsand the diplocyst is found in oligochaets. Bondarenko& Kontrimavichus (1976a,b) consideredthat five species of Aploparaksis (A. bulbocirrus,A. groenlandica, A. furcigera, A. polystictae andA. taimyrensis) exhibited this type of development(see also Demshin, 1976; Gulyaev, 1977)to which can be added A. australis (see Bondarenko,1989), A. clangulae (see Bondarenko &Kondratyeva, 1985), A. filum (see Demshin, 1981;Bondarenko, 1990), A. kulachkovae (see Bondarenko,1987), A. pseudofilum (see Bondarenko,1990) and A. sanjuanensis (see Demshin, 1985).Bondarenko & Kontrimavichus (1976) describedfour variants of the typical diplocyst. A ‘caudatediplocyst’ was considered to be present inA. brachyphallos and A. crassirostris (see Bondarenko& Kontrimavichus, 1976a; Demshin,1984), while a variant, the floricyst, in which thecysticercoid was partially embedded in the cercomer,resembling a closed flower, was present inA. birulai (see Bondarenko & Krasnoschchekov,1978). The ramicercus (Figure 3D), in which thecercomer has 6-10 digitate appendages, was firstnamed by Skrjabin & Mathevossian (1942), basedon a cysticercoid described from Lumbriculus byMrázek (1907). Bondarenko & Kontrimavichus(1976b) identified a ramicercus in A. orientalis andA. secessivus as well as in Wardium chaunense,while Demshin (1971) identified a similar caudatelarva in A. dujardini. Finally, a larval form wasfound in A. xemae in which multiple cysticercoidsbud from the cercomer, becoming detached at anearly stage of development (Bondarenko & Kontrimavichus,1976b); this larval stage was termedan autotomicrocercus and was compared with thestaphylocyst and urocyst (vide infra). A comparablelarval form was also described in Wardiumfreyei by Bondarenko (1977).Gulyaev (1989) coined the term ascocercus forthe larval stage of amabiliids. However, the larvaappears to be identical with a diplocyst exceptthat the scolex may only be partly retracted, orthere may be some indication of segmentation. Theterm ascocercus alludes to the elongate stalked cystwithin which the larva develops. However, ascocercusis simply a minor variant of the diplocyst.4. Monocercus (Figure 3E)The term ‘monocercus’ was originally erected byVillot (1882) for Cysticercus arionis found ina mollusc by von Siebold (1850), characterisedby numerous globular structures around the cysticercoid.Mrázek (1907) indicated that during itsdevelopment the cercomer fragmented into globuleswhich persisted within the larval cestode.Gabrion et al. (1976), Gabrion (1981) and Gabrion& MacDonald (1980) studied the development ofsimilar larval cestodes of Anomotaenia constricta,A. brevis, Paricterotaenia porosa and Eurycestusavocati, all of which exhibited a similar form ofdevelopment and defined a monocercus as being amonocephalic cysticercoid in which a primary lacunais present, the scolex develops externally andretracts, following which the cercomer detachesand fragments. They considered that this type oflarval development was restricted to the Dilepididaeand, in a review of the literature, showedthat a similar mode of larval development occurredadditionally in the genera Amoebotaenia(see Joyeux & Baer, 1936), Trichocephaloides (see

14Tomilovskaya, 1975), Rauschitaenia and Sacciuterina(see Demshin 1968, 1976). To these specieshave subsequently been added Anomotaenia globulusby Demshin (1977) and A. micracantha byJarecka et al. (1984) (as a cercoscolex).Other dilepidid cestodes exhibit relatively minorvariations on the basic pattern of morphogenesisshown in a monocercus. In Dilepis undula, a shortcercomer develops, detaches from the soma butdoes not become subdivided into a series of globularstructures (Gulyaev, 1997). The term acerocystwas used for this mode of development (Gulyaev,1997).The development of the larvae of Lateriporus resemblesthat of Dilepis, the only difference beingthat the collum of the larva is segmented (Shapkin& Gulyaev, 1973; Gulyaev, 1989). The termsstrobilocercoid (see Gabrion, 1981, p. 130) orstrobilocysticercoid (see Freeman, 1973) havebeen applied to this larval form.In other dilepidids, Choanotaenia infundibulum(see Horsfall & Jones, 1937; Voge, 1961) aswell as in Molluscotaenia crassiscolex and M. estavarensis(both formerly species of Choanotaenia)(see Jourdane, 1972; Gabrion, 1981), there isno cercomer at any stage of their development. Theterm microcyst would be an appropriate apellationfor these larval cestodes.The adult stages of Villot’s original cysticercoidsplaced in the genus Monocercus, M. arionisand M. glomeridis, have not been establishedwith certainty. Villot (1883) suggested that theymight be ‘Taenia arionis’, a cestode of birds, andTaenia crassiscolex, now Molluscotaenia, respectively.Joyeux & Baer (1936) attributed Monocercusglomeridis to Anomotaenia constricta, aconclusion rejected by Gabrion (1981, p. 93) onthe basis of lack of experimental completion of thelife-cycle.Gulyaev & Kornienko (1998) concluded thatMonocercus glomeridis was the intermediate stageof Molluscotaenia crassiscolex and made thegenus Molluscotaenia a synonym of Monocercus.They also concluded that it was no longer appropriateto use the term monocercus as Gabrion(1981) had done, and proposed the replacementterm cryptocercus. Their synonymy is not followedhere since the ‘type-species’ of the genusMonocercus is presumably M. arionis and its adultstage remains to be determined.(b) Polycephalic cysticercoids1. Polycercus (Figure 3F)The genus Polycercus was erected originally byVillot (1883) for a polycephalic larval stage foundin an earthworm by Metchnikoff (1869) under thename Polycercus lumbrici. The adult was subsequentlyidentified as Paricterotaenia paradoxa(Dilepididae), which is currently treated as a synonymof P. lumbrici (i.e. Bona, 1994). The developmentof the larval stages has been describedby Scott (1965), Demshin (1981), Gulyaev & Kornienko(1998) and Gulyaev (2000). There is nocercomer, the cysticercoid develops at one poleof the larva following retraction, a primary lacunaforms and the scolex is subsequently retracted. Thepolycercus is therefore a polycephalic form of thediplocyst.2. Staphylocyst (Figure 3G)The genus Staphylocystis was created by Villot(1877) for the larval stage of S. (= Hymenolepis)pistillum, a cestode parasite of shrews. The larvalstage, found in the diplopod Glomeris conspersa,was characterised as being a polycephaliclarva with individual cysticercoids in the form ofa bunch of grapes (Villot, 1877). The illustrationsprovided here are based on those of Joyeux & Baer(1961). Skrjabin & Mathevossian (1942) describedthe larvicyst as resembling ‘a kind of mycelium’,which is not consistent with the description givenby Villot (1883).3. Urocyst (Figure 3H)Urocystis Villot, 1880 was created for a polycephaliccysticercoid found in Glomeris limbatusin which cysticercoids bud and detach from thematernal tissue. The adult of Urocystis proliferwas identified by Kisielewska (1960) as Pseudodiorchisprolifer in shrews. The urocyst is a multilobedparenchymatous mass from which cysticercoidsdevelop on elongate pedicels, detaching priorto the completion of development. This phenomenonresembles that of the autotomicrocercus describedin the monocephalic Aploparaksis xernaeby Bondarenko & Kontrimavichus (1976b).The development of the larval stage of Hymenolepis(=Staphylepis) cantaniana was describedin detail by Jones & Alicata (1935) and wastermed a urocyst by Wardle & McLeod (1952).The fully-developed larva resembles a mycelium

15from which cysticercoids bud off. If this larva isincluded under the term urocyst, then the definitionneeds to be broadened to include larval bodieswhich are either compact or filamentous.The above review of systems of nomenclature for larvalcestodes demonstrates that they are both complexand confusing. One possible method for eliminatingthe current confusion is to analyse the specific morphologicalor developmental characters which havebeen utilised in the systems erected to date, to selectdifferential characters on the basis of their robustnessor their intrinsic predictive values and to develop asystem of nomenclature based on explicit characters,appropriately ranked. The following section thereforeanalyses these values in the characters whichhave been used to describe different types of larvalcestodes.Characters used in the analysis of cestode larvaHistorically, the principal characters used to differentiatelarval cestodes have been: (1) the presence orabsence of a primary lacuna; (2) the presence or absenceof a cercomer; (3) whether the cestode scolexis retracted or invaginated; (4) whether a ‘bladder’ ispresent in the metacestode; (5) the type of host and(6) whether the larva is mono- or polycephalic. Aseventh character, whether metacestodes are bothriateor acetabulate, warrants little further comment as thischaracter (or character pair) is relatively well defined.The primary lacunaIn many groups of cyclophyllidean cestodes, a cavity,termed a primary lacuna, develops in the earlystages of morphogenesis, the megalosphere stage ofSkrjabin & Mathevossian (1942). The term, as ‘lacunaprimitiva’, was first proposed by Grassi & Ravelli(1892) and its formation has been reviewed in detail byVoge (1967) and Šlais (1973). In the genus Dipylidium,the primary lacuna is a transitory structure andbecomes filled with parenchymatous cells (Venard,1938; Marshall, 1967).The potential difficulty in utilising this characteris that detailed studies of cestode morphogenesis maybe required to determine its existence and inconsistenciesexist in descriptions of its occurrence in theLinstowiinae, the Dilepididae and the Paruterinidae.In addition, it is not always possible to determinefrom the published descriptions of cestode life-cycleswhether or not a primary lacuna has actually been observed.However, Gabrion (1975, 1981) has shownthat it is possible, by careful histological or ultrastructuralexamination of fully-developed larvae, todemonstrate the presence of a primary lacuna. Difficultiesencountered in the Linstowiinae, Dilepididaeand Paruterinidae are therefore considered in greaterdetail:(a) Linstowiinae. A primary lacuna has been reportedin Oochoristica vacuolata (see Hickman, 1963),O. deserti (see Milleman, 1955) and Atriotaenia procyonis(see Gallati, 1959), but was considered ‘indistinct’in O. osheroffi by Widmer & Olsen (1967). Conn(1985) did not observe a primary lacuna in O. anolisbut attributed this to a lack of serial histologicalsections of developing metacestodes. Rendtorff (1948)did not observe or illustrate a primary lacuna in Mathevotaeniaratti.(b) Dilepididae. A primary lacuna has been describedin a number of genera, such as Anomotaenia (seeGabrion, 1975; Gabrion & Gabrion, 1976), Paricterotaenia(see Krasnoshchekov & Tomilovskaya,1978; Gabrion & Helluy, 1982) and Choanotaeniainfundibulum (see Gutberlet, 1916; Horsfall &Jones, 1937). The structure was not reported in Molluscotaeniacrassiscolex and M. estavarensis (bothformerly members of Choanotaenia) (see Jourdane,1972, 1977) although it was observed in M. crassiscolexby Rawson & Rigby (1960). In a re-investigationof the life-cycle of this cestode, Gabrion (1981) provideda micrograph of a histological section of thedeveloping larva (plate 13d) which clearly shows aprimary lacuna. It may be that in some dilepidids, aswith linstowiids, that sections are required to demonstratethe existence of a lacuna. Gulyaev (1997b) failedto find a primary lacuna in the developing larva ofDilepis undula, describing the alacunate final form asan acerocyst. However, no sections appear to havebeen examined.(c) Paruterinidae. Freeman (1957, 1959) did not observea primary lacuna during development of themetacestodes of members of the genera Paruterinaand Cladotaenia. However, Šlais (1973) has suggestedthat, since Freeman (1959) first examined developingmetacestodes 8-10 days after infection, a temporary lacunamay have developed and disappeared during this

16period. Development during this early period has notbeen examined since. In the paruterinid Metroliastheslucida, a primary lacuna, termed an ‘invagination cavity’,is apparently present (Jones, 1936), thus differingfrom other known paruterinid life-cycles.The presence or absence of a primary lacuna canusually be determined from careful observation offully-developed larvae, but there is obviously bothconfusion within taxa (e.g. Linstowiinae) and inconsistencieswhich require more detailed investigation(Dilepididae), preferably with the aid of serial sections.Reviews by Brooks et al. (1991), Hoberg et al.(1999) and Beveridge (2001) suggest that the absenceof the primary lacuna is plesiomorphic, whileits occurrence may be a homoplasious character.The cercomerFreeman (1973) defined the cercomer, following traditionalusage of the term, as a ‘tail’ formed at the posteriorend of a larval cestode, usually containing theoncospheral hooks. Jarecka et al. (1981), by contrast,defined the cercomer as the region of the metacestodecovered with microvilli rather than microtriches. Theyconsidered that all cestodes thus possess a cercomerwhich may be modified and may not always exhibitthe classical form of a ‘tail’. Because ultrastructuralobservations are unavailable for most cestodes, theclassical definition, adopted by Freeman (1973), is themore practicable. The phylogenetic significance of thecercomer in eucestodes has been discussed by Gulyaev(1996).The presence of a cercomer appears to be characteristicof many but not all basal cestodes, althoughit may be lost during development. A study of earlymetacestode development is often necessary to determinewhether or not the cercomer has been present(Scholz, 1999). Difficulties of interpretation or inconsistenciesoccur currently within the Proteocephalidea,Trypanorhyncha, Dilepididae, Davaineidae and Paruterinidaeand these difficulties warrant comment:(a) Proteocephalidea. In species of Proteocephalus,the cercomer may remain attached to the metacestodeor may detach as early as 1-3 days after infection ofthe intermediate host (Scholz, 1999). No cercomer hasbeen observed in certain species, but these observationsrequire confirmation (Scholz, 1999).(b) Trypanorhyncha. A cercomer was described inGrillotia (see Ruskowski, 1934) but not in Lacistorhynchus(see Mudry & Dailey, 1971; Sakanari &Moser, 1989). However, in Prochristianella and Poecilancistrium,Mattis (1986) noted the existence ofa short, stout cercomer, which may have been overlookedin the earlier studies or not interpreted as acercomer.(c) Dilepididae. Gabrion (1981) and Gabrion & Helluy(1982) noted that in the genera Amoebotaenia,Trichocephaloides, Rauschitaenia, Paricterotaenia,Eurycestus, Sacciuterina and Anomotaenia, the cercomerdisintegrates into globules which persist withina metacestode, termed a monocercus by Villot (1882)and described in greater detail by Mrázek (1907).According to Wardle & McLeod (1952), the termcryptocystis would be used to describe such metacestodes.It should be noted, however, that cryptocystiswas first applied to the metacestode of Dipylidiumcaninum (see Villot, 1882, 1883). Gulyaev & Kornienko(1998) recognised three types of metacestodeswithin the Dilepididae, the monocercus in which acercomer is vestigial, the cryptocercus (cryptocystis)defined above as a monocercus and the polycercus,defined by them not merely as a polycephalic formas proposed originally (Villot, 1882, 1883) but onein which the cercomer forms part of the wall of thecyst which encloses the developing metacestode. Thelatter form of development was also shown to occurin the formation of the diplocyst of the hymenolepididAploparaksis furcigera by Gulyaev (1997c).In Dilepis and Lateriporus a cercomer is presentinitially but becomes detached from the body of thelarva (Gulyaev, 1997b, 1998). A cercomer is lackingin Molluscotaenia crassiscolex and M. estavarensis(formerly Choanotaenia) (Jourdane, 1972, 1975).Gabrion (1981, p.123) noted that the apparent observationof a cercomer in M. crassiscolex by Rawson &Rigby (1960) was due to their misidentification of thecystic vesicle prior to scolex retraction.In a further type of dilepidid larval stage, thepolycercus, the scoleces develop endogenously. Thereis no tail-like cercomer (Scott, 1965; Demshin, 1981)but the outer ‘cyst wall’ could be considered thecercomer (sensu Jarecka, 1975).Gabrion & Helluy (1982) cited five species ofdilepidid cestodes in which the cercomer persistedin fully-developed larvae. Of these, Dilepis undulahas been discussed and Metroliasthes lucida is currentlyplaced in the Paruterinidae. The three remain-

17ing species are Choanotaenia infundibulum, C. citrusand Anomotaenia cumillaris. A small, possibly detachedcercomer was shown in C. infundibulum byVoge (1961, figure 2), although Gutberlet (1916, figure12) illustrated a fully-developed cercomer. In appearstherefore that an intact, persistent cercomer isuncommon in the Dilepididae.(d) Davaineidae. In Davainea and Raillietina (seeWetzel, 1932, 1934) the cercomer may be very shortand may not persist in fully-developed metacestodes.Wardle & McLeod (1952) regarded davaineids as agroup in which there may be no cercomer and usedthe term cercocystis to describe their metacestodes,although, as originally defined (Villot, 1883), thisterm was for cysticercoids which had a prominent cercomer.(e) Paruterinidae. No cercomer develops in the generaParuterina and Cladotaenia (see Freeman, 1957,1959), while a cercomer develops in Metroliasthes lucida(see Jones, 1936).In summary, the presence or absence of a cercomerremains to be determined in several cestode groups,its lack of persistence or reduced size probably contributingto some of the differences of interpretationobserved in the literature. Both Hoberg et al. (1999)and Beveridge (2001) presented evidence that loss ofthe cercomer may be a homoplasious condition.Scolex retraction and invaginationIn most basal orders of cestodes, the scolex developsexternally and there is no retraction or invaginationof the scolex. However, in a number of groups, someform of invagination or retraction of the scolex occurs.Whether fully-developed scoleces are invaginated orretracted figured prominently in classical definitionsof cysticercoids and cysticerci (e.g. Leuckart, 1876;Fuhrmann, 1933), although the terms were used interchangeablyby Wardle & McLeod (1952). It was aprominent feature in the discussions of types of larvalcestodes in the reviews of Voge (1967) and Šlais(1973). Freeman (1973), by contrast, did not includethis character in his phylogenetic analysis. Freeman(1973) (p. 502) stated that the scolex is labile and‘there is some evidence that the scolex of the metacestodemay evert and retract as need be’. The evidencepresented for this statement was derived from paperson proteocephalidean life-cycles, but problems alsoexist in some tetraphyllidean cestodes and possibly thelecanicephalideans.(a) Proteocephalidea. Freeman’s (1973) concerns ofthe value of this character stem from data published byHerde (1938), Befus & Freeman (1973) and Rysavy(1961). The paper of Herde (1938) reported the developmentof Ophiotaenia perspicua and describedhow developing metacestodes, examined under a microscope,may evert their scoleces and in doing so,pass through a transitory phase in which the scolexappears to be ‘withdrawn’. Herde (1938, p. 288)stated that ‘older specimens show a tendency to keepthe scolex continuously invaginated’, indicating thatthe variation noted is related primarily to developingmetacestodes. Befus & Freeman (1973, p. 252) notedthat in fully-developed metacestodes of Corallobothriumparafimbriatum, ‘scoleces ... may extend outand pull back into the body repeatedly’. The photographthey presented (figure 2) of a metacestode ‘withretracted scolex’ is, however, that of an invaginatedscolex. In the case of Corallotaenia minutia, theystated (p. 253) that "the scoleces either retract or invaginateinto the mid-body’, but no illustrations wereprovided. Thus there is evidence that in some proteocephalideanmetacestodes the scolex may invert orevert, but there is no evidence that it is consistentlyretracted.(b) Trypanorhyncha. Similar limited evidence is availablefor the Trypanorhyncha (see Dollfus, 1942), butagain, systematic evidence is lacking.(c) Pseudophyllidea. In pseudophyllidean cestodes,the scolex of the plerocercoid is not inverted or invaginated(Rosen, 1919). There is however a smallapical invagination which has even been interpretedas a third bothrium (Rosen, 1919). The presence ofthis small apical invagination may have contributed toconfusion over whether or not the scolex of pseudophyllideanplerocercoids is invaginated (Wardle &McLeod, 1952).(d) Tetraphyllidea. In most known tetraphyllideancestodes, the scolex is neither withdrawn nor invaginated(e.g. Scolex polymorphus, S. pleuronectis)(Euzet, 1959; Chambers et al., 2000). In Phyllobothrium,Monorygma, Rhinebothrium and Rhodobothrium,however, the scolex appears to be invaginated(Dollfus, 1942, 1964; Anthouard, 1963; Chamberset al., 2000), although this is not always clear (Doll-

18fus, 1964; Campbell & Carvajal, 1979; Carvajalet al, 1982). Phyllobothrium delphini, Monorygmaand Rhodobothrium have relatively long ‘invaginationcanals’ and, as the scolex begins to evaginate, it mayappear to pass through a stage in which the scolex is‘retracted’. An analogous situation exists with taeniidmetacestodes in which the scolex of the cysticercus isinvaginated with a fluid-filled bladder. A partly evaginatedscolex may appear to be ‘retracted’, as is shownin the illustration of the evaginating scolex of Taeniapisiformis by Benham (1901) (reproduced by Wardle& McLeod, 1952, figure 56E).(e) Lecanicephalidea. Information for some of thesmaller cestode groups is limited, but scanningelectron micrographs of Polypocephalus and Tylocephalumby Butler (1985) show clearly that in thelecanicephalideans, the scolex is retracted within asolid blastocyst.Freeman’s (1973) extrapolations from observations onspecies of proteocephalideans may therefore provideinsufficient grounds for rejecting the use of the characterof the scolex being ‘invaginated’ or ‘retracted’(= withdrawn), particularly in other cestode groups.One difficulty with utilising this character is that terms‘invaginated’, ‘retracted’ and ‘withdrawn’ are usedapparently interchangeably in some publications (e.g.Wardle & McLeod, 1952) and the illustrations ofmetacestodes often do not permit the reader to determinewhether the scolex is withdrawn or inverted (e.g.Jones, 1936). However, in contrast to opinions in somerecent literature, it may be a useful character.BladdersIn cysticerci, in ‘cystidean’ trypanorhynchs (membersof the suborders Heteracanthoidea, Otobothrioideaand Poecilacanthoidea in the classification ofCampbell & Beveridge, 1994) and in the tetraphyllideanspecies Monorygma grimaldii and Phyllobothriumdelphini, as well as in the genus Rhodobothrium,the scolex of the metacestode is surrounded by afluid-filled ‘bladder’.The ontogenesis of the bladder has been extensivelystudied in taeniid cestodes (Šlais, 1973) andrepresents a secondary enlargement of the primarylacuna (Wardle & McLeod, 1952). Trypanorhynchslack a primary lacuna (Ruskowski, 1934; Riser, 1956;Mudry & Dailey, 1971; Mattis, 1986) and the bladderis presumed therefore to be a secondary development(Dollfus, 1942; Freeman, 1973, p. 503), followingthe albeit speculative scheme of larval developmentfor this group proposed by van Beneden (1850). Mosttetraphyllideans lack a bladder, the known early developmentalstages lack a primary lacuna (Euzet, 1959;Mudry & Daily, 1971), and the development of thebladder in P. delphini, M. grimaldii and Rhodobothriumis presumed to be a secondary character. Thebladder of metacestodes is probably therefore not homologousacross orders, but lack of detailed studies oftetraphyllidean and trypanorhynch life-cycles preventsany firm conclusions from being drawn. Evidence infavour of the bladder being a homoplasious characteris provided from the molecular studies reviewed byMariaux & Olson (2001).HostsTwo features of the hosts of larval cestodes have beenutilised in the current schemes of terminology, thesebeing whether the larva is in the first of second intermediatehost (Jarecka, 1970, 1975) and whether thehost is an invertebrate or a vertebrate. The variousproblems associated with determining whether or nota host is the first or second intermediate host have beenalluded to above. The type of host currently presentsintractable problems. There is evidence unquestionablyof restriction of certain types of larval cestodesto particular host groups, such as Aploparaksis inoligochaets or cysticerci (and their modifications) inmammals. However, numerous exceptions to generalisedpatterns also exist; for example, the occurrenceof ‘linstowiine’ type larval cestodes in both coleopterans(Milleman, 1955; Hickman, 1963; Widmer &Olsen, 1967; Conn, 1985) and mammals (Beveridgeet al., 1975). The extent to which the host of a larvalcestode can be incorporated into a system of terminologyis therefore disputable both from theoreticaland practical perspectives, and warrants much moredetailed investigation.Mono- and polycephalic larvaePolycephalic larvae occur within the cysticercoid andcysticercus groupings. These characteristics are relativelywell defined and are obviously homoplasious,but may have utility as secondary characters.Having described the various morphological charactersused to characterise larval cestodes, their strengthsand deficiencies, the subsequent step is to choose

19characters upon which a system of cestode larvalterminology can most reliably be based.Selection of charactersOf the principal morphological characters which canbe derived from the development of the larval cestode,none is without problems of interpretation with respectto some cestode taxa. The origins of ‘bladders’ cannotbe resolved until further details of the life-cycles ofmarine cestodes are elucidated, but the fact that tetraphyllideansand trypanorhynchs lack a primary lacunasuggests that ‘bladders’ in these orders are not homologouswith the ‘bladders’ present in metacestodes ofthe Taeniidae.The primary lacuna is a feature of the earlystages of metacestode development, but, as Gabrion& Gabrion (1976) and Gabrion (1981) have shown,histological or ultrastructural sections of the fullydevelopedmetacestode can reveal the prior existenceof a primary lacuna. Thus, while there are some deficienciesin knowledge of the existence of such astructure, they can potentially be overcome by carefulexamination of larval cestodes even if the entiredevelopment of the cestode cannot be observed. Theapparent presence or absence of a primary lacunawithin some Dilepididae remains to be resolved.Similarly, careful examination of the fullydevelopedlarval cestode must reveal whether or notthe scolex is invaginated or withdrawn and developmentalstages are not required to demonstrate this feature.There may be difficulties associated with somespecies of the Proteocephalidea and Tetraphyllidea,but these are currently limited to a small number ofspecies, and in non-mobile stages, the metacestodeis probably either fully-evaginated or inverted; the‘retracted’ stage in these cestodes is presumably a temporarysituation seen only in the cases of cestodes withinverted scoleces in the process of everting the scolex,although further investigations are obviously required.The cercomer may persist in the final stage ofthe larval cestode, but may in some groups becomereduced or disappear. The presence of a cercomercan therefore be established in some groups only bycareful observation of cestode development, since thecercomer of some proteocephalideans is lost as rapidlyas 1-3 days after infection of the intermediate host(Scholz, 1999). Host associations appear to requiremuch more careful analysis before they can be utilisedwith confidence.Based on these observations and due obviouslyto significant deficiencies in knowledge of development,any character-based system for the classificationof larval cestodes is likely to be of greatest utilityif it is founded primarily on the presence of a primarylacuna and the retraction/invagination of thescolex, since these are at least observable in the fullydevelopedlarval cestode. The presence or absence ofa cercomer (apart from the way in which the structureis defined) may only be determinable from detailedstudies of life-cycles (and possibly ultrastructure) and,while of considerable significance, may represent apractical handicap in determining the relationships ofcestodes based on life-cycle characters. From a purelypragmatic point of view, therefore, this character iscurrently of limited use. It may also be an homoplasiouscharacter (Hoberg et al., 1997; Beveridge,2001).An additional feature of developmental stages ofcestodes belonging to the families Hymenolepididaeand Dilepididae is the extent to which the scolex developsprior to retraction. In the Hymenolepididae, scolexdevelopment can be completed prior to retraction, orthe scolex can complete its development following retraction(Šlais, 1973). A similar division exists in dilepididcestodes (Gabrion & Helluy, 1982). Amongstacaudate larval cestodes, taeniids undergo scolex developmentfollowing invagination of the scolex canal(Freeman, 1973), whereas linstowiids, as well asthe unplaced genus Anoplotaenia, undergo scolex invaginationafter partial development of the suckersexternally (Hickman, 1963; Beveridge et al., 1975).Thus this character varies within major groups and,whilst potentially useful in the future, is too poorlyunderstood to utilise in any current character-basedproposals for the terminology of larval cestodes.A number of additional potentially promising morphologicalfeatures of larval cestodes cannot be incorporatedas characters at this time due to lack ofcomparative data. The retraction of the scolex of manyhymenolepidid cestodes is a highly complex process,involving hypertrophy of muscle systems, the developmentof a ‘fibrous’ layer in the cyst wall and theclosure of the opening through which the scolex iswithdrawn (Collin, 1970; Baron, 1971; Cayley, 1974,1976; Richards & Arme, 1984a,b; Rogan & Richards,1987). In addition, the distribution of microtriches andmicrovilli on fully-developed cestodes offers the possibilityof additional characters (Crowe et al., 1974;Gabrion & Gabrion, 1976; Jarecka et al., 1981; Mac-Kinnon & Burt, 1983; Rogan & Richards, 1987), but

20Figure 3. Schematic representation of development of different types of cysticercoids. A, cercocysticercoid (redrawn from Prokopic, 1971:Rodentolepis erinacei); B, microcysticercoid (modified from Freeman, 1973); C, diplocysticercoid (modified from Gulyaev, 1977: Aploparaksisfurcigera); D, ramicysticercoid (caudate diplocysticercoid) (modified from Demshin, 1985: Aploparaksis sachalinensis); E, monocysticercoid(modified from Gabrion, 1975: Anomotaenia constricta); F, polycysticercoid (a polycephalic diplocysticercoid) (modified from Scott, 1965;Demshin, 1981: Monocercus lumbrici); G, staphylocysticercoid (redrawn from Joyeux & Baer, 1961); H, urocysticercoid (modified from Jones& Alicata, 1935: Hymenolepis cantaniana).

21Figure 4. Schematic representations of six forms of larval cestodes. A. Procercoid; B, Plerocercoid; C, Merocercoid (redrawn from Dollfus,1942); D, Plerocercus (redrawn from Dollfus, 1942); E, Cysticercoid (redrawn from Gabrion, 1981); F, Cysticercus (redrawn from Gabrion,1981).the development of too few cestodes has been studiedin detail to date to allow general usage of thesecharacters.The preceding arguments therefore justify the useof only two primary characters for the current classificationof larval cestodes: (1) presence of a primarylacuna; (2) scolex developing externally or retracted/inverted.Secondary characters of potential butcurrently limited in application are (1) presence of acercomer and (2) presence of a bladder, as these eithermay not be determinable (1) or may be homoplasious(2).Using the primary characters identified above, sixputative life-cycles are possible. Since no life-cyclesare known in which a primary lacuna develops butthe scolex is not withdrawn or invaginated (Freeman,

221973), this possibility has been eliminated, leavingfive life-cycle types for which examples are known(Figure 4):1. No primary lacuna, scolex of metacestode everted(plerocercoid) (Figure 4B);2. No primary lacuna, scolex retracted (plerocercus)(Figure 4D);3. No primary lacuna, scolex invaginated (some plerocercoids,tetrathyridium, cladothyridium, cercoscolex)(Figure 4C);4. Primary lacuna present, scolex retracted (cysticercoid)(Figure 4E);5. Primary lacuna present, scolex invaginated (cysticercus)(Figure 4F).Terms exist already for several of these developmentalseries. Cestodes with no primary lacunaand with everted scoleces (e.g. Pseudophyllidea) (1)have previously been termed plerocercoids. Cestodes(usually) with a primary lacuna and a retractedscolex have been termed cysticercoids (4).Cestodes with a primary lacuna and an invaginatedscolex have been termed cysticerci (5). Cestodes withno primary lacuna and a retracted scolex (2) havebeen termed plerocerci (Trypanorhyncha, see Dollfus,1942), blastocysts (Trypanorhyncha, see Gulyaev,1997a), or merocerci (some lecanicephalideans, seeFuhrmann, 1933; Joyeux & Baer, 1961). Cestodeswith no primary lacuna and an invaginated scolex(3) have been termed plerocercoids (Phyllobothriidae),tetrathyridia (Mesocestoides, see Voge, 1967), merocercoids(Catenotaenia, see Joyeux & Baer, 1945),cladothyridia (Cladotaenia, Paruterina, see Abuladze,1964) or cercoscoleces (gryporhynchids, see Jarecka,1970a,b). Thus using these five broad categoriesfor larval development, it is evident that all knownmetacestodes can be accommodated within them (Table6). The sources on which the allocation of the varioustaxa of cestodes to a particular morphologicallydefined group of metacestodes are as follows:plerocercoid: Spathebothriidea (see Sandeman &Burt, 1972), Caryophyllidea (see Mackiewicz, 1972(Figure 1A); Demshin, 1978; Demshin & Dvoyadkin,1981; Scholz, 1991, 1993), Pseudophyllidea (seeFreeman, 1973) (Figure 1B), Trypanorhyncha (Homeacanthoidea)(see Dollfus, 1942), Haplobothriidea(see Essex, 1929 (Figure 1C); Thomas, 1930), Proteocephalidea(see Scholz, 1999) (Figure 2A), Tetraphyllidea(see Euzet, 1959; Cake, 1976; Mudry & Dailey,1971) (Figure 1E), Nippotaeniidea (see Demshin,1985) (Figure 1F), Nematotaeniidae (see Joyeux,1924); plerocercus (= merocercus): Diphyllidea (seeRuskowski, 1928; Cake, 1976), Trypanorhyncha (Heteracanthoidea,Otobothrioidea, Poecilacanthoidea)(see Dollfus, 1942) (Figure 1D), Lecanicephalidea(Tylocephalum, Polypocephalus) (see Cake, 1976,1979; Butler, 1985; Brockerhoff & Jones, 1995); merocercoid(= tetrathyridium): Mesocestoididae (seeVoge, 1967), Catenotaeniidae (see Joyeux & Baer,1945), Gryporhynchidae (see Jarecka, 1970a,b) (Figure2F), Paruterinidae: Paruterina, Cladotaenia (seeFreeman, 1957, 1959) (Figure 2B), Proteocephalidea(in part) (see Scholz, 1999) (Figure 2A), Tetraphyllidea:Anthobothrium, Phyllobothrium, Monorygma,Rhodobothrium (see Dollfus, 1964; Cake,1976) (Figure 1E); cysticercoid: Anoplocephalinae(see Stunkard, 1937, 1961; Denegri et al., 1998)(Figure 2G), Thysanosomatinae (see Denegri et al.,1998), Progynotaeniidae (see Gvozdev & Maksimova,1979), Dioecocestidae (see Ryzhikov & Tolkacheva,1981), Amabiliidae (see Rees, 1973a,b; Gulyaev,1989) (Figure 2H), Davaineidae (see Freeman, 1973;MacKinnon & Burt, 1983), Dilepididae (see Gabrion& Helluy, 1982), Hymenolepididae (see Šlais, 1973);cysticercus: Taeniidae (Abuladze, 1964) (Figure 2C),Linstowiinae (see Hickman, 1963; Milleman, 1955;Conn, 1985) (Figure 2D), Dipylidiidae (see Venard,1938; Marshall, 1967) (Figure 2E), Paruterinidae:Metroliasthes (see Jones, 1936).Some orders such as the Tetrabothriidea aredifficult to accommodate since although the fullydevelopedmetacestode is well described (see forexample Hoberg, 1987; Galkin, 1996), whether aprimary lacuna is present or absent remains to bedetermined.Of the various names available for each group,cysticercus subsumes the terms amphicyst (Spasskii,1949, 1951) and precysticercus (Freeman, 1973), cysticercoidsubsumes precysticercoid (Freeman, 1973),ascocercus (Gulyaev, 1989), multicercus and monocercus(Gabrion & Helluy, 1982), while plerocercoidcovers the collective larval names Scolex pleuronectisand S. polymorphus. For group names of Type 2 larvalcestodes, plerocercus is the oldest name. For theType 3 group of cestodes, tetrathyridium, coined as ageneric name by Rudolphi (1819), is the older name,but merocercoid is more consistent with related terms,and is preferred on this basis.The arrangement of cestode taxa under these collectivelarval names warrants several comments. Thefirst and most obvious comment is that all known,

23Table 6. Suggested terms for larval cestodes derived from the primary morphological characters (primary lacuna, scolex retracted or invaginated) applied to know cestode taxa (orders,families, genera or species).Proceroid Pleroceroid Plerocerus Merocercoid Cysticercoid CysticercusLarval cestodes lacking Lacking primary Lacking primary Lacking primary Primary lacuna Primary lacunasolex and primary lacuna, scolex lacuna, scolex lacuna, scolex present, scolex present scolexlacuna, requiring external retracted invaginated retracted invaginatedadditionalintermediate hostSpathebothriideaCaryophyllidea Diphyllidea Mesocestoides Anoplocephalinae TaeniidaeThysanosomatinae LinstowiinaePseudophyllidea CatenotaeniidaeHomeacanthoidea (Trypanorhyncha) Heteracanthoidea, Otobothrioidea, Poecilacanthoidea Progynotaeniidae(Trypanorhyncha) Gryporhynchidae DipylidiidaeAmabiliidaeHaplobothriidea Paruterina/Cladotaenia Dioecocestidae (?)MetroliasthesDavaineidaeProteocephalidea (p.p.) Proteocephalidea DilepididaeTetraphyllidea (p.p.) Monorygma HymenolepididaeNippotaeniidea Lecanicephalidea RhodobothriumNematotaeniidae PhyllobothriumRhinebothriumOther namesapplied in the Scolex pleuronectis merocercus tetrathyridium precysticercoid amphicystliterature Scolex polymorphus blastocyst cladothyridium ascocercus precysticercuspost-larva tentaculo-plerocercoid cercoscolex monocercus cryptocystmulticercus

24Figure 5. Schematic representations of types of taeniid larvae apart from the cysticercus. A, coenurus; B, hydatid; C, strobilocercus withdistinct segmentation; D, fimbriocercus (=armatetrathyridium) redrawn from Šlais (1973); E, un-named polycephalic larva of Taenia twitchelliredrawn from Rausch (1977).completely developed larval forms can be groupedwithin five simple, if broad, categories for whichnames already exist. The sole major example of larvalcestode development not encompassed by this seriesof categories is the larval stage which is typically caudate,lacking a primary lacuna or a scolex, and whichdoes not proceed in its larval development until ingestedby a subsequent intermediate host. The termprocercoid has traditionally been employed for thisgroup of larval cestodes (Figure 4A) and is utilisedhere in this form (Freeman, 1973), but not as utilisedby Jarecka (1975) for fully-developed, bothriate, caudatemetacestodes (e.g. Caryophyllidea).Secondly, the correlation between larval formand cestode taxonomic group is not absolute. TheTrypanorhyncha have plerocerci as metacestodes ifthey belong to the suborders Heteracanthoidea, Otobothrioideaor Poecilacanthoidea, but plerocercoids(or post-larvae) if they belong to the Homeacanthoidea.Most Tetraphyllidea have plerocercoids asmetacestodes, but those with scoleces inverted (Monorygmagrimaldii, Phyllobothrium delphini, Rhinebothrium,Rhodobothrium) have merocercoids. Proteocephalideansmay have two types of larval cestodes,plerocercoids or merocercoids. The distinction presentedhere between plerocercoids and merocercoidsis the most tenuous of the proposed divisions andwarrants considerably more study before it should beaccepted. However, the lack of correlation betweenmetacestode type and taxonomic groups provides no

25new difficulties for this system of metacestode nomenclatureand also exists in the classifications of Rudolphi(1819) and Fuhrmann (1933).A third feature of the proposed groupings is the factthat the character of the adult holdfast being differentfrom that of the larval stage, as occurs in the Onchobothriidae,the Catenotaeniidae and the Tetrabothriidea,has been ignored. Inclusion of the ontogeny ofthe holdfast could alter the proposed groupings.The aggregation of cestode taxa with cysticercoidsas metacestodes presents no novelties. By contrast,the collection of cestode taxa considered as havingcysticerci as metacestodes is novel as it includes thetraditional group of taeniid cestodes, with bladders,but also includes linstowiids, whose metacestodeshave formerly been described as amphicysts (Spasski,1951) or precysticerci (Freeman, 1973) as well asthat of Dipylidium which has had various appellationsbut which was originally termed a cryptocyst (Villot,1883).While the suggested system of classification ofmetacestodes has obvious major advantages, the principalof which is that all known larval cestodes canbe accommodated within six categories, there are alsopotential deficiencies. These are (1) that the charactersof the cercomer and bladder are not taken intoaccount; (2) that one traditional category, cysticercus,which is widely utilised in the applied literature,has been violated by the addition of cestode taxawhich do not possess the characteristic bladder ofthe taeniid cysticercus or its polycephalic modifications;and (3) that the nomenclature of the variouslarval stages, particularly the endings of names, isinconsistent.(1) The potential difficulty of the secondary characterof ‘presence of a cercomer’ can be easily overcomeusing the model of Freeman (1973) in whichthe prefix ‘caudate’ is applied. This is useful withinthe cysticercoids since some are caudate at the end oftheir development, some are acaudate or the cercomermay be reduced. The plerocercoids of pseudophyllideans(acaudate) can be distinguished readily fromthose of caryophyllideans (caudate) with this prefix,as can various forms of metacestodes within the Proteocephalidea.Similarly, the singular metacestode ofDipylidium can be distinguished from traditional cysticerciby the addition of the prefix ‘caudate’. Thus,the optional use of the prefix ‘caudate’ can overcomemost of these objections. In the case of the larva ofD. caninum, the extent of differences between its developmentand a traditional cysticercus could be usedto argue for a special term, in which case cryptocystwould be the most appropriate (Villot, 1883).(2) The feature of a ‘bladder’ presents the greatestdifficulty within the group of metacestodes heredefined as cysticerci, since the taeniid cysticerci havetraditionally been defined as possessing bladders, orsecondary enlargements of the primary lacuna (Wardle& McLeod, 1952), while the newly added linstowiid‘amphicysts’ do not. In this instance, the use of Freeman’s(1973) term ‘precysticercus’ would allow a distinctionbetween the taeniid cysticerci and linstowiidprecysticerci, with an allusion to the hypothesis thatthe bladder is a secondary development (Gulyaev,1997a), although this evolutionary hypothesis has yetto be established.The presence of a bladder is less significant a problemin plerocerci, since plerocerci without bladders arecurrently restricted to species of Polypocephalus andTylocephalum (Lecanicephalidea). ‘Pre-plerocercus’would be a possible term for such metacestodes.Within the merocercoid group, only four phyllobothriidgenera of tetraphyllideans of the 54 known genera(Euzet, 1994) possess bladders.Thus, while no uniformly satisfactory formula forterminology exists, the use of the prefixes ‘caudate’and ‘pre-’ suitably accommodates most of the difficultiesarising from the inclusion of the secondarycharacters. It has the advantage that the use of prefixesis optional and does not abrogate the broad classesof metacestodes defined. It also overcomes the secondobjection raised above, namely that traditional,widely applied terms such as cysticercus for taeniidlarval cestodes do not have to change to conform withthe proposed system.(3) The third potential objection, namely that theterminology of the proposed larval cestodes is etymologicallyinconsistent, is a separate matter. Mostterms for larval cestodes are based on the Greek‘cerca’, meaning tail. The Latin suffix ‘-oid’ simplyindicates a likeness. Thus a procercoid, etymologically,is a larval cestode which is not fully developed.A plerocercoid is a larval cestode which has a ‘repletetail’, or is a non-lacunate larval cestode. Whilesomewhat inappropriate to describe acaudate pseudophyllideanlarval cestodes, it is firmly entrenched. Inthe usage of Wardle & McLeod (1952), both typesof larval cestodes with primary lacunae have the prefix‘cysti-’. ‘Cysticercus’ may allude appropriately tothe bladder of taeniid metacestodes, but since theylack a cercomer, the suffix (‘– cercus’) is somewhatinappropriate. However, it is firmly entrenched. ‘Cys-

26ticercoids’ generally possess a cercomer at some stageof their development but lack a ‘bladder’. The prefixsupposedly alludes to the primary lacuna (Wardle &McLeod, 1952), but this was not known at the timethat the name (‘lacuna primitiva’ of Grassi & Rovelli,1892) was applied by Leuckart (1876). Hence the etymologyis dubious. Likewise, ‘plerocercus’ scarcelydiffers from plerocercoid in meaning (Joyeux & Baer,1961), but also indicates a metacestode lacking a primarylacuna. The argument being developed here isthat several of the current, firmly entrenched termsfor larval cestodes are, from an etymological pointof view, not completely appropriate, but are widelyaccepted. Therefore, to argue for the standardisationof nomenclature purely on etymological grounds ishazardous and could lead to increased confusion.An additional tradition is one in which metacestodenames ending in ‘–us’ (cysticercus, plerocercus)indicate the existence of a bladder, while names endingin ‘–oid’ indicate the absence of a bladder. However,no formal written presentation of this view canbe found! In the current re-arrangement of morphologicalpriorities, the presence of a bladder is of reducedsignificance, since it may be homoplasious, whilethe invagination or retraction of a scolex is accordedgreater significance than in the recent literature. Underthis system, cysticercus, a retained term, is appliedto metacestodes in which the scolex is invaginated,while cysticercoid is applied to metacestodes in whichthe scolex is retracted, although both have a primarylacuna or ‘cyst’ (sensu Wardle & McLeod, 1952).Procercoid and plerocercoid, which have either noscolex development or an everted scolex, have alsobeen retained as names for larval cestodes. Therefore,changing the name ‘plerocercus’ to a term ending in‘-oid’ to be consistent with cysticercoid, the othergroup name in which scoleces are retracted wouldeliminate one inconsistency, but would introduce anotherwith the entrenched term plerocercoid which hasan everted or invaginated scolex. Similarly, attemptingto find an alternative to ‘merocercoid’ for larvalcestodes with inverted scoleces but lacking a primarylacuna presents obstacles since none of the existingnames (tetrathyridium, cladothyridium, cercoscolex)has a ‘−us’ suffix.The most parsimonious solution to this etymologicalmaze is to retain the tradition of ‘cyst-’ indicating(usually) the presence of a primary lacuna and ‘plero-’indicating the absence of a primary lacuna. The existingterm plerocercus can be used in place of merocercus,since this adequately covers both the encystedtrypanorhynchs and lecanicephalideans, and the comparableterm ‘merocercoid’ coined for catenotaeniidsby Joyeux & Baer (1945) can be used for tetrathyridia,cladothyridia and cercoscoleces, all of which lackbladders and are invaginated. Merocercoid favours noorder over the other and while not the older term,provides the greatest etymological uniformity.In the final analysis, terminology represents findingcompromises between entrenched usage and etymologicalconsistency. The proposal suggested here isa compromise but seems to be an appropriate middlecourse between these two ideals, and will undoubtedlyattract criticism from either of the two possibleentrenched extreme positions.Based on the arguments presented above, thefollowing definitions are suggested for metacestodesidentified on the basis of morphological characteristics:Procercoid (Figure 4A) metacestode without scolexand primary lacuna, usually caudate, in which developmentcannot proceed until ingested by a secondintermediate host.Plerocercoid (Figure 4B) metacestode with (at leastpartial) scolex development (bothriate or acetabulate),scolex evaginated, non-lacunate, with or without cercomer,infective to definitive host.Merocercoid (Figure 4C) metacestode lacking a primarylacuna, in which scolex is invaginated, caudateor acaudate, usually without bladder (except inRhodobothrium, Phyllobothrium, Monorygma (Tetraphyllidea)).Plerocercus (Figure 4D) metacestode lacking a primarylacuna, in which scolex is withdrawn; caudate(disputed), with or without bladder.Cysticercoid (Figure 4E) metacestode with primarylacuna, scolex retracted,with cercomer or reduced cercomer.Cysticercus (Figure 4F) metacestode with primary lacuna,scolex invaginated, with or without cercomerand bladder.Within the two latter groups, cysticerci and cysticercoids,considerable morphological diversity exists.Some within-group diversity can be indicatedsimply by the use of prefixes based on existing names.CysticerciThe terms utilised by Hoberg et al. (2000) have beenadopted. These are:for monocephalic cysticerci -cysticercus

27fimbriocercus (including armatetrathyridium)strobilocercusand for polycephalic cysticerci -coenurusechinococcus (including alveococcus)Coenurostrobilocercus and hemistrobilocercus areincluded under strobilocercus.The names of the monocephalic cysticerci haveuniform endings clearly indicating that they belong tothe same group of larval cestodes. This is not true ofthe polycephalic forms, but the terms coenurus andechinococcus are too firmly entrenched to contemplatealtering.For modifications of the cysticercus, the followingterms are proposed: precysticercus for paruterinidand linstowiine cestodes (includes amphicyst,cladothyridium) and cryptocysticercus for the larvaof Dipylidium.CysticercoidsAs described above, numerous terms have been coinedto describe different types of cysticercoids. Two basictypes of larval development are discernible, that exhibitedby the cercocyst, microcyst and monocercus inwhich a scolex forms externally and then is retractedwithin the body of the larva and another, exhibitedby the diplocyst in which two layers of larval tissueeventually surround the scolex. Within each developmentaltype, forms exist which are caudate or acaudateand mono-or polycephalic. All of the names used forcysticercoids (cercocyst, microcyst, diplocyst, ramicercus,monocyst, polycyst, staphylocyst and urocyst)can be altered so that each has the ending - cercoid,thus denoting they are modifications of the basic cysticercoidplan. The proposed terms are:Monocephalic larvae -cercocysticercoid for caudate cysticercoidsmicrocysticercoid for acaudate cysticercoids or forthose with a vestigial cercomer (microcercus)diplocysticercoid for cysticercoids in which thescolex is enveloped by two layers of larval tissue(=diplocyst) (includes ascocercus)ramicysticercoid for caudate diplocysticercoids (includesfloricyst)monocysticercoid for caudate cysticercoids in whichthe cercomer disintegrates into globules during development(= monocercus) (includes acerocyst, strobilocercoid,cryptocercus)Polycephalic larvae -polycysticercoid for polycephalic diplocysticercoids(= polycyst)staphylocysticercoid for polycephalic cysticercoidsdeveloping in the form of a bunch of grapes (= staphylocyst)urocysticercoid for polycephalic cysticercoids exhibitinga mycelium-like development from whichcysticercoids bud off (= urocyst, autotomicrocercus)For all of these types of cysticercoid, the use of theprefix is optional. If the prefix is not used, the larvalcestode is clearly identifiable as a cysticercoid, whileuse of the prefix provides additional information.ConclusionThe current review of terminology of larval cestodesproposes a system based primarily on morphologicalfeatures determinable from the fully-developed larvalcestode, namely the existence of a primary lacunaand the retraction or invagination of the scolex. Thepresence of a bladder is utilised as a secondary characterbecause the structure is probably non-homologousbetween orders of cestodes. The presence of a cercomerduring development is currently utilised as asecondary character because it may be lost during developmentand may therefore be secondarily absent infully-developed larval cestodes. Using these morphologicaland developmental features, six groups of larvalcestodes are recognised, each of which is defined.The advantage of the proposed system is that it reducesthe number of types of larval cestodes to a small numbersof groups, although the most appropriate termsapplicable to these groups are not always apparent.Those applied to minor cestode groups (plerocercusand merocercoid) remain arguable.The current proposals, while undoubtedly imperfect,represent an attempt to simplify the understandingof larval cestodes and their terminology as well asprotecting entrenched usage of terms in applied fieldsof parasitology. They will, hopefully, provide the basisfor a sustained discussion of the rational use of termsin describing known metacestodes. The deficiencies inour current knowledge are also exposed and it is clearthat a comprehensive system of terminology cannot beproposed until some of these gaps are filled. Apartfrom deficiencies in the knowledge of life-cycles oflarge orders of tapeworms, the role of the type of hostas well as homologies between various components oflarval cestodes remains to be resolved. As informationaccumulates, the proposed system will undoubtedlyrequire modification. However, if the reasoning upon

28which it is based is clearly exposed, modifications canbe made relatively easily.AcknowledgementsThe author wishes to acknowledge the contributionsof the following to discussions of metacestode terminologyin Sofia: I. Beveridge, V.Y. Biserkov, R.A.Bray, J. N. Caira, K.S. Eom, L. Euzet, B. Georgiev,T. Genov, D.I. Gibson, V. Ivanov, C.J. Healy, K.Jensen, A. Jones, M.K. Jones, Y. Kong, V. Kornyushin,J. Mariaux, M. von Nickisch-Rosenegk, T. Scholz,S.R. Stoitsova, P. Swiderski, G.A. Tyler, C. Vaucherand G.P. Vasileva, and to R. Campbell, E. Hoberg,S. Gardner, T. Mattis and R. Overstreet, who kindlycommented on the first draft of the manuscript.ReferencesAbdou, A.H. (1958) Studies on the development of Davaineaproglottina in the intermediate host. Journal of Parasitology, 44,484–487.Abuladze, K.I. (1964) [Taeniata of animals and man and diseasescaused by them]. Osnovy Tsestodologii. 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