Systematic Parasitology 37: 81–92, 1997. 81c 1997 Kluwer Academic Publishers. Printed in the Netherlands.

An alternative classification of trypanorhynch cestodes considering thetentacular armature as being of limited importance

Harry W. PalmMarine Pathology Group, Department of Fisheries Biology, Institut fur Meereskunde an der Universitat Kiel,Dusternbrooker Weg 20, D- 24105 Kiel, Germany

Accepted for publication 22nd November, 1996

Abstract

Based on a light- and scanning electron microscopical study of scolex morphology, tentacles and surface structuresof 31 trypanorhynch species, an alternative classification of the trypanorhynch cestodes, adults, plerocerci andpostlarvae, is presented. The arrangement of the tentacular armature is no longer used as a distinguishing featurefor four different superfamilies. Instead, the presence or absence of ciliated pits and prebulbular organs is used todefine three superfamilies: Tentacularioidea Poche, 1926; Otobothrioidea Dollfus, 1942; and EutetrarhynchoideaGuiart, 1927. A total of 12 families are defined by the characters: the presence/absence of blastocysts, the numberof bothridia and the reduction of the rhyncheal apparatus, together with a new character, complete rows of ten-tacular hooks (homeoacanth and heteroacanth typica) versus rows of hooks partly reduced (heteroacanth atypicaand poeciloacanth). Of the 19 families previously accepted, 10 are retained (Eutetrarhynchidae, Gilquiniidae,Lacistorhynchidae, Mixodigmatidae, Otobothriidae, Paranybeliniidae, Pterobothriidae, Shirleyrhynchidae, Sphyri-ocephalidae and Tentaculariidae, all sensu nov.); one family is reinstated (i.e. Aporhynchidae Poche, 1926 sensunov.) and a new one is added (i.e. Pseudotobothriidae n. fam.). Advantages of this alternative classification oftrypanorhynch cestodes are: (i) the resolution of incongruities and questions caused by the use of the tentaculararmature to distinguish superfamilies; (ii) the criteria for the establishment of higher taxa, superfamilies and familiesare clearly defined; (iii) with the findings of new species with different character combinations, this system can beenlarged up to 4 superfamilies and 48 families without loosing its stability; and (iv) all existing genera are easilyre-assigned to the superfamilies and families.

Introduction

Trypanorhynch cestodes are characterised by the pos-session of a scolex bearing four eversible tentaclesarmed with hooks and two or four bothridia, enablingthese cestodes to move along and attach to the diges-tive tract of their final hosts which are elasmobranchs.In their life-cycles, these cestodes use invertebrates asfirst intermediate hosts, with teleosts and some inver-tebrates as second intermediate or paratenic hosts. Thepresence of the metacestodes (postlarvae and plerocer-ci) in the musculature of fishes decrease the commer-cial value of affected stocks (Deardorff et al., 1984).

Despite their world-wide distribution and impor-tance for commercial fisheries, trypanorhynch cestodesare still a relatively poorly studied group. One reasonfor this could be their classification which complicates

identification of many of the c. 200–250 generallyaccepted species. Wardle & McLeod (1952) stated (andwere recently quoted by Campbell & Beveridge, 1994)that, taxonomically, the Trypanorhyncha are complexand considered to be the most chaotic and confusedof the tapeworm groups. Carvajal & Campbell (1975)saw the general problems within trypanorhynch classi-fication as follows: “The problems of defining naturalaffinities of trypanorhynchs are perplexing because ofour grossly insufficient knowledge concerning life his-tories, larval development, host specificity, etc., andbecause the significance of morphometric charactersmust be weighed by each investigator. [: : : ] As morespecies are discovered, it appears that the currentmethod of trypanorhynch classification is becomingincreasingly unstable because of the variability inher-ent in organisms”. Furthermore, within existing try-

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panorhynch classifications, some characters are usedas major distinguishing features for different taxa atdifferent systematic levels at one and the same time.There are only a few specific character combinationswhich are characteristic for a single taxon.

Campbell & Beveridge (1994) published a newclassification of trypanorhynch cestodes, in which thetentacular armature of the postlarvae, plerocerci andadults was used as a major character for four super-families: Homeacanthoidea Dollfus, 1942, Heteracan-thoidea Dollfus, 1942, Otobothrioidea Dollfus, 1942and Poecilacanthoidea Dollfus, 1942. Additionally, intheir identification key, Campbell & Beveridge (1994)used bothridial form, tentacle length, position of thepars bothridialis relative to that of the pars bulbosa,uterus morphology and the occurrence of a blastocyst(these precede the tentacular armature in the key), lead-ing the user to the different superfamilies. However,this system has grouped some families together thatshare similar tentacle arrangements, but have few oth-er morphological similarities in common.

During a study of trypanorhynchs from all foursuperfamilies, two species with a new character com-bination [Poeciloacanthum oweni Palm, 1995 andPseudotobothrium dipsacum (Linton, 1897)], ciliat-ed pits on the bothridia together with a poeciloacan-thous/heteroacanthous typica armature, were found(Palm, 1995). Both show a strong morphological rela-tionship to species of the Otobothriidae Dollfus, 1942(Otobothrioidea Dollfus, 1942), although lacking thesuperfamily character, a heteroacanthous atypica arma-ture. Following the most recent classification of Camp-bell & Beveridge (1994), which uses the tentaculararmature as a major character at the superfamily lev-el, the species have to be placed in two superfami-lies Poecilacanthoidea Dollfus, 1942 and Heteracan-thoidea Dollfus, 1942, neither of which are related tothe family Otobothriidae.

In the present paper, such incongruities arising fromthe most recent Campbell & Beveridge system togeth-er with the usefulness of ciliated pits and prebulbularorgans as systematic characters are discussed. As aresult, an alternative classification is presented whichconsiders the tentacular armature as being of no impor-tance at the superfamily level and of limited importanceat the family level.

Materials and methods

Light- and scanning electron microscopical studies ofmorphology, tentacles and surface structures of thescoleces of trypanorhynch cestodes belonging to 18genera (a total of 31 species) resulted in the descrip-tion of four new species (Grillotia kovalevae, Poeciloa-canthum oweni, Pseudogrillotia zerbiae, Pseudolacis-torhynchus noodti) and the first SEM studies of 15previously known species (see Palm, 1995).

Fresh postlarvae, plerocerci and adults were col-lected from teleosts and elasmobranchs along thecoasts of Brazil, Nigeria and the southern (Gulf ofMexico) coast of Mississippi, USA. Preserved postlar-vae and plerocerci were obtained from collections inBrazil, England, Russia and the USA (Palm, 1995).Characteristics of the 31 trypanorhynch genera notexamined by Palm (1995) were obtained from theliterature, in the form of the original descriptions,redescriptions and Campbell & Beveridge (1994), withthe latter having priority in cases of discrepancy.

The current classification

Based on the fundamental work of Dollfus (1942),Campbell & Beveridge (1994) grouped 46 genera and19 families of trypanorhynchs within four superfam-ilies, the latter characterised by the possession of aspecific kind of tentacular armature. These authors pre-served Dollfus’ classification scheme and retained hissuperfamily concept. The Homeacanthoidea has hookson the tentacles which form quincunxes or continu-ous spiral rows (homeoacanth, after Dollfus, 1942);the Heteracanthoidea is characterised by hooks on thetentacles which form half spiral rows with a constantnumber of hooks (heteroacanth typica). The Otoboth-rioidea is similar to the latter superfamily but has extrahooks or rows of hooks interpolated on the external sur-face of the tentacle (heteroacanth atypica). Within thePoecilacanthoidea, a distinctive hook file or files formone or more chainettes on the external tentacle surface(poeciloacanth). Finally, using 13 different characters,Campbell & Beveridge (1994) arranged the familiesand superfamilies within a cladogram, showing theirpossible phylogenetic relationships.

An innovation in the classification of Campbell &Beveridge (1994) is the use of pattern isometry forinterpretation of the characteristic armatures. The useof hook arrangements on the tentacle surfaces as themajor distinguishing feature for trypanorhynch classi-

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fication has the advantage that this character is sim-ilar for plerocerci (postlarvae) and adults within thesame species (Richmond & Caira, 1991). Further-more, hooks are hard structures and do not changetheir appearance due to different fixation and prepa-ration methods. However, despite the precision of theCampbell & Beveridge system, some incongruities arepresent, and some questions arise.

Different kind of armatures are present within closelyrelated species

Within one superfamily or family, some closely relatedspecies (as far as other morphological characters otherthan the tentacular armature are considered) can havedifferent characteristic armatures. For example, thesuperfamily Otobothrioidea sensu Campbell & Bev-eridge (1994) has a heteroacanthous atypica armatureand therefore contains the family Otobothriidae Doll-fus, 1942. This family is additionally characterised bythe possession of ciliated pits on the bothridial borders(Campbell & Beveridge, 1994). Palm (1995) describeda new trypanorhynch species with ciliated pits, Poe-ciloacanthum oweni Palm, 1995, having a distinct sin-gle chainette on the external tentacle surface (Figures1a–b), and thus exhibiting the features of a poeciloa-canth. The species Pseudotobothrium dipsacum (Lin-ton, 1897) (formerly Otobothrium dipsacum Linton,1897) has a heteroacanthous typica armature (Figures1c–d), without extra hooks or rows of hooks interpo-lated on the external side of the tentacle (Palm, 1995).According to the Campbell & Beveridge system, thesetwo species have to be placed into two different super-families, the Poecilacanthoidea and Heteracanthoidea[sensu Campbell & Beveridge (1994)]. However, bothspecies show a strong morphological relationship tomost species of the Otobothriidae (Otobothrioidea),sharing the following suite of characters: the occur-rence of a blastocyst, a craspedote scolex with appen-dix, two patelliform bothridia with horse-shoe-shapedciliated pits (Figure 2a), a similar form of the bulbs (notP. dipsacum), a similar position of the pars bothridialisrelative to the pars bulbosa, the origin of the retrac-tor muscles in the anterior part of the bulbs, and thepresence of three-fingered palmate microtriches on thebothridia and filamentous microtriches only on the restof the scolex (see Palm, 1995). Considering morpho-logical characters other than the tentacular armaturefor characterising the Otobothriidae, there are threedifferent armatures, heteroacanthous typica, heteroa-

canthous atypica and poeciloacanthous, within a rangeof closely related species.

Have ciliated pits developed independently or do theycharacterise a monophyletic taxon?

Only a few species of trypanorhynchs have ciliated pitson the borders of the bothridia, thus presenting someevidence for a monophyleticorigin. Based on this char-acter, Linton (1890) established the genus Otobothri-um, and Dollfus (1942) established the family Otoboth-riidae. Using the classification scheme of Campbell &Beveridge (1994), which relies on the tentacular arma-ture as a major distinguishing character, species withciliated pits would be separated into all four super-families (see above), thereby implying an independentdevelopment of this organ in several unrelated lineages.

Thus, we are confronted with conflicting evidence.Most species with ciliated pits have heteroacanthousatypica armatures and therefore belong to the Otoboth-rioidea (sensu Campbell & Beveridge, 1994). In con-trast to this, two species Pseudonybelinia odontacan-tha Dollfus, 1966 and Paranybelinia otobothrioidesDollfus, 1966 have homeoacanthous armatures andconsequently have to be placed within the Homeacan-thoidea. The armature of Pseudotobothrium dipsacumis heteroacanthous typica (Heteracanthoidea), whereasPoeciloacanthum oweni has a poeciloacanthous arma-ture and therefore belongs to the Poecilacanthoidea.However, the non-tentacular morphology of the latterspecies shows a strong relationship to the otobothri-ids (see above). Therefore, a monophyletic origin oftrypanorhynch cestodes with ciliated pits is likely.

Unique position of the Tetrarhynchobothriidae withinthe Homeoacanthoidea

Members of the homeoacanth family Tetrarhyn-chobothriidae Dollfus, 1969 have several characteris-tics shared with those of the Eutetrarhynchidae Guiart,1927, a family belonging to the Heteracanthoidea.Such characters are an elongated scolex with oval both-ridia, long tentacles as well as tentacle sheaths andthe occurrence of a blastocyst and prebulbular organs.For this reason the group was placed together withthe Eutetrarhynchidaeby Dollfus (1969). Furthermore,Schmidt (1986) synonymised TetrarhynchobothriumDollfus, 1969 with Eutetrarhynchus Pintner, 1913.Beveridge & Campbell (1988) re-assessed the familyTetrarhynchobothriidae, discussed in detail its similar-ity to the Eutetrarhynchidae, and placed the family in

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Figure 1. Trypanorhynch cestodes, scanning electron micrographs: a–b. External tentacle surface of Poeciloacanthum oweni, note thecharacteristic single chainette; c–d. External tentacle surface of Pseudotobothrium dipsacum, note the lack of interpolated hooks or rows ofhooks. Abbreviation: C, chainette. Scale-bars: a, b, d, 10 �m; c, 20 �m.

the suborder Cystidea Guiart, 1927, although it has ahomeoacanth tentacular armature like species of theAcystidea Guiart, 1927. In contrast to this, but consis-tent with their classification, the Tetrarhynchobothri-idae is allocated to the Homeacanthoidea in Campbell& Beveridge (1994), mainly based on the homeoacan-thous armature (see Campbell & Beveridge, 1994, p.67). This interpretation is still open for discussion.

Two different kind of armatures on a single tentacle

In 1982, Dailey & Vogelbein described Mixodigmaleptaleum Dailey & Vogelbein, 1982 as possessing apoeciloacanthous basal armature together with a het-eroacanthous typica armature in the metabasal part ofthe same tentacle. According to the scheme of Doll-fus (1942), who used only the metabasal armature, M.leptaleum would be considered as having a heteroacan-thous typica armature. However, in the 1994 classifica-tion of Campbell & Beveridge, where the armature is

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Figure 2. Trypanorhynch cestodes, scanning electron micrographs: a. Horse-shoe shaped ciliated pit of Poeciloacanthum oweni; b. Externaltentacle surface of Otobothrium cysticum, note the hooks marked with arrows, forming a file of alternating hooks along the tentacle. Scale-bars:5 �m.

interpreted as possessing a chainette of reduced length,M. leptaleum is unequivocally a poeciloacanth. M. lep-taleum is not alone in having different hook patternson different parts of the tentacles; other examples areDasyrhynchus talismani Dollfus, 1935 and Pseudo-grillotia peruviana Escalante & Carvajal, 1984 (seeCampbell & Beveridge, 1994, p. 67).

M. leptaleum has a strong resemblance to theHeteracanthoidea, especially to the ShirleyrhynchidaeCampbell & Beveridge, 1994, with its metabasal arma-ture, the presence of prebulbular organs, elongate bulbsand gland-cells around the retractor muscle, as wellas its terminal genitalia (see Beveridge & Campbell,1989). However, the Mixodigmatidae Dailey & Vogel-bein, 1982 are placed together with the Gymnorhynchi-dae Dollfus, 1935 within the Poecilacanthoidea in thecladogram of Campbell & Beveridge (1994). Besidethe distinct chainette on the external surface in thebasal part of the tentacles, the two families have fewcharacters in common. Thus, this implication of phy-logenetic relationship between these two families onthe basis of the poeciloacanthous armature can be con-sidered doubtful.

Have prebulbular organs developed independently ordo they characterise a monophyletic taxon?

Several trypanorhynch cestodes are known which haveprebulbular organs around the tentacle sheaths at the

entry to the bulbs. Campbell & Beveridge (1994) listedthe following families belonging to all four superfam-ilies: Eutetrarhynchidae; Shirleyrhynchidae Camp-bell & Beveridge, 1994; (both Heteracanthoidea);Tetrarhynchobothriidae Dollfus, 1969 (Homeacan-thoidea); Grillotiidae Dollfus, 1969 (Otobothrioidea);and Mixodigmatidae Dailey & Vogelbein, 1982 (Poe-cilacanthoidea). As a consequence, the prebulbularorgans could not be used as a systematic characterfor defining higher taxa. However, considering theTetrarhynchobothriidae to be closely related to theEutetrarhynchidae and the species Mixodigma lep-taleum to the Shirleyrhynchidae (see above), the enig-matic prebulbular organ characterises a large group ofclosely related species. Thus, it is concluded, althoughthe function of this organ is still unclear, that pre-bulbular organs have developed only once within thetrypanorhynchs.

Do intermediate forms of hook patterns exist?

Some trypanorhynchs are known which have featuresthat indicate some relationships between the majorgroupings (tentacle armature types – currently at thesuperfamily level), and present a problem for the sys-tematist. An example of such a worm is Otobothriumcysticum (Mayer, 1842). Its tentacular armature is con-sidered to be heteroacanthous atypica (Dollfus, 1942;Campbell & Beveridge, 1994; Palm, 1995). However,

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in the metabasal part of the tentacle, the last princi-pal hooks on the external tentacle surface could beinterpreted as a file of alternating hooks (Figure 2b),thus fulfilling part of the criteria for a chainette (ifall criteria for a chainette were met, the O. cysticumarmature would be poeciloacanthous). As it is thoughtthat a poeciloacanthous armature has evolved from aheteroacanthous atypical armature (Campbell & Bev-eridge, 1994), such a longitudinal hook arrangementmight already represent a precursor of a poeciloacan-thous hook pattern, with the principal hooks 6 and 6’thought to form a chainette. Thus, O. cysticum can beinterpreted as an intermediate form between heteroa-canthous atypica and poeciloacanthous species, sup-porting the idea of a relationship between Poeciloacan-thum oweni Palm, 1995 and other otobothriid species(see above).

A further example of a trypanorhynch species,showing a tentacular armature that could be interpretedto be an intermediate form, is a species of Pteroboth-rium Diesing, 1850. Within this genus, species have aheteroacanthous atypica armature. Some species, suchas P. hawaiense Carvajal, Campbell & Cornford, 1976and P. lintoni (MacCallum, 1916), lack hooklets on theexternal tentacle surface; however, intercalary hooksare still present along the tentacle (Campbell & Bev-eridge, 1996). Using scanning electron microscopy,Palm (1995) described two specimens of a Pteroboth-rium species which he identified as P. heteracanthumDiesing, 1850. In the metabasal part of all tentaclesboth the hooklets on the external tentacle surface andthe intercalary hooks were absent. Only in the basalpart were some hooklets and 1-4 intercalary hookspresent. Thus, considering the general morphologyas well as the basal armature, the examined speci-mens clearly belong to a Pterobothrium species withthe expected heteroacanthous atypica armature. How-ever, the metabasal part is similar to a heteroacanthoustypica armature.

Comments

These examples outlined above show that the tentaculararmatures as defined by Dollfus (1942) and Campbell& Beveridge (1994) can split closely related species,as determined by other morphological characters, intodifferent superfamilies. Additionally, the value of thepresence of ciliated pits and prebulbular organs in rela-tion to trypanorhynch classification appears to havebeen underestimated.

Carvajal & Campbell (1975) came to the conclusionthat the complex oncotaxy is definitive for specific butnot for familial determination. For this reason, a clas-sification of superfamilies which uses the tentaculararmature as of major importance splits morphological-ly similar species into different families or even super-families. Palm (1995) gave the main reason for thisas a convergent development of tentacular armatures,caused by adaptation of the trypanorhynch tentacularapparatus to their sites of attachment in their final hosts.For example, a homeomorphous and homeoacanthousarmature in combination with short tentacles is mostfavourable for attaching to the muscular tissue of thestomach wall, while the heteromorphous armature onlong and slender tentacles is perfectly adapted to aconnective tissue dominated intestinal wall (see Palm,1995). Further support for this functional hypothesis isthe dominance of worms with the former tentacle typein cephalopods, where they often occur encapsulated inthe walls of stomach and caecum, the mesenteries andgonads, and in the ventral musculature of the mantlewall (Kinne, 1990). The mobile postlarvae of Tentacu-laria coryphaenae even occur in the water-filled man-tle cavity, where they exist embedded (Kinne, 1990)or attached to the mantle tissue, a site from which theyrisk being expelled by turbulence. Cephalopods arevoracious, versatile predators (Rodhouse & Nigmat-ullin, 1996) and should have as trophic opportunists asimilar access to both types of trypanorhynchs.

Summarising the above, it is concluded thattentacular armatures are convergent within the try-panorhynchs. Thus, the tentacular armatures charac-terise superfamilies in an empirical system of try-panorhynchs which is unlikely to reflect their phyloge-ny.

The proposed classification

In the following section, an alternative classificationof trypanorhynch cestodes is presented, which givesthe tentacular armature no importance for superfam-ily and a reduced importance for family determina-tion. Instead, the ciliated pits and prebulbular organsare integrated at a higher systematic level, solvingthe incongruities and unresolved questions discussedabove. A total of six different characters are used toconstruct this alternative classification; ciliated pits onthe bothridia; prebulbular organs; blastocysts; num-ber of bothridia; rows of hooks on the tentacles; andrhyncheal apparatus. In addition, each of these can

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Table I. Characters used for an alternative classification of try-panorhynch cestodes.

Character Plesiomorphic Apomorphic

Ciliated pits on the bothridia� absent present

Prebulbular organs absent present

Blastocyst� absent present

Number of bothridia� 4 2

Rows of hooks on tentacles complete partly reduced

Rhyncheal apparatus present absent

�Interpretation of character state in agreement with Campbell &Beveridge (1994).

be divided into primitive (plesiomorphic) and derived(apomorphic) states (Table I), thereby allowing phylo-genetic interpretation of the order.

Superfamilies

The presence or absence of ciliated pits on the both-ridia and the presence or absence of prebulbular organsis used to distinguish three superfamilies, the Otoboth-rioidea Dollfus, 1942, Tentacularioidea Poche, 1926and Eutetrarhynchoidea Guiart, 1927 (Figure 3).

The Otobothrioidea is characterised by ciliated pitson the bothridial borders and the absence of prebulbu-lar organs. The presence of ciliated pits is consideredto be a synapomorphic character of this monophylet-ic taxon, relative to the absense of this character inall other trypanorhynchs. All species of the Otoboth-riidae Dollfus, 1942 as well as the ParanybeliniidaeSchmidt, 1970 are included into the Otobothrioidea.For the species Pseudotobothrium dipsacum (Linton,1897), the family Pseudotobothriidae Palm, 1995 isadded to this superfamily.

The Eutetrarhynchoidea is characterised by theabsence of ciliated pits on the bothridia and the pos-session of prebulbular organs, as defined by Pintner(1880). The presence of prebulbular organs is consid-ered to be a synapomorphic character of this mono-phyletic taxon, relative to the absense of this characterin all other trypanorhynchs. The Eutetrarhynchoideaincludes the families Eutetrarhynchidae Guiart, 1927,Shirleyrhynchidae Campbell & Beveridge, 1994 andMixodigmatidae Dailey & Vogelbein, 1982, as definedby Campbell & Beveridge (1994). Additionally thethree genera, DidymorhynchusBeveridge & Campbell,1988, Zygorhynchus Beveridge & Campbell, 1988 andTetrarhynchobothrium Diesing, 1854, of the former

Tetrarhynchobothriidae Dollfus, 1969 are added to theEutetrarhynchidae.

The third superfamily, Tentacularioidea, containstrypanorhynchs having neither ciliated pits nor pre-bulbular organs. A character providing evidence fora monophyletic origin of this superfamily could notbe demonstrated. Therefore, this superfamily mustbe considered paraphyletic. The Tentacularioidea con-tains all remaining genera listed by Campbell & Bev-eridge (1994) and Palm (1995) rearranged in six dif-ferent families: Tentaculariidae Poche, 1926; Sphyrio-cephalidae Pintner, 1913; Gilquiniidae Dollfus, 1942;Aporhynchidae Poche, 1926; Pterobothriidae Pintner,1931; and Lacistorhynchidae Guiart, 1927 (Figure 3).

Families

The following characters are used as criteria at thefamily level: the presence or absence of a blastocyst;the number of bothridia (two or four); the tentacu-lar armature [complete rows of hooks (as exempli-fied by homeoacanthous and heteroacanthous typicaarmatures) or rows of hooks partly reduced (as exem-plified by heteroacanthous atypica and poeciloacant-hous armatures)]; and the reduction of the rhynchealapparatus (see Palm, 1995). The penultimate charac-ter, rows of hooks complete or rows of hooks partlyreduced, is new and refers to the metabasal armature.Rows of hooks are considered complete if the armatureconsists of only complete spirals or of only principalrows (respectively, homeoacanthous and heteroacan-thous typica, as defined by Dollfus 1942). Rows ofhooks are considered partly reduced if the armatureincludes any of the following: intercalary hooks, hooksor rows of hooks interpolated on the external surface(band of hooks), and a chainette. The common featureof these elements on the external tentacular armature istheir interpretation as relicts of former complete spiralsor principal rows.

In order to characterise the families, specific com-binations of these characters are used. Of the 19families previously accepted by Campbell & Bev-eridge (1994), 10 are retained (EutetrarhynchidaeGuiart, 1927; Gilquiniidae Dollfus, 1942; Lacis-torhynchidae Guiart, 1927; Mixodigmatidae Dailey& Vogelbein, 1982; Otobothriidae Dollfus, 1942;Paranybeliniidae Schmidt, 1970; Pterobothriidae Pint-ner, 1931; Shirleyrhynchidae Campbell & Beveridge,1994; Sphyriocephalidae Pintner, 1913; Tentaculari-idae Poche, 1926 (all sensu nov.). One family is rein-stated (Aporhynchidae Poche, 1926 sensu nov.) and

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a new one is established (Pseudotobothriidae Palm,1995). The following families are considered to be syn-onymous: Hepatoxylidae Dollfus, 1940 with Sphyri-ocephalidae; Tetrarhynchobothriidae Dollfus, 1969with Eutetrarhynchidae; Gymnorhynchidae Dollfus,1935, Molicolidae Beveridge & Campbell, 1989 andRhinoptericolidae Carvajal & Campbell, 1975 withPterobothriidae; and Dasyrhynchidae Dollfus, 1935,Grillotiidae Dollfus, 1960, Hornelliellidae Yamaguti,1954 and Mustelicolidae Dollfus, 1969 with Lacis-torhynchidae.

The proposed new classification of trypanorhynchcestodes, with definitions for superfamilies and fami-lies, is shown diagrammatically in Figure 3. Some gen-era are tentatively placed in superfamilies and familieswithin the proposed classification, despite not know-ing if they have a blastocyst (for example when thespecies description is based on adults). In these cases,assignment was based upon the general morphology,number of bothridia and kind of tentacular armature(see ‘Future studies’ below).

Comments on the proposed classification

The proposed alternative classification of try-panorhynch cestodes allows all known trypanorhynchsto be unequivocally placed on the basis of a definedcombination of characters in superfamilies and fam-ilies. Using evolutionary systematics, and no longerusing the tentacular armature as the major characterfor superfamily separation, both the classification andidentification of trypanorhynchs is simplified. Mayr& Ashlock (1991) pointed out that, for phenetics aswell as for cladistics, a large number of charactersshould be used for classification. However, as the mostusable characters show an enormous variability withinthe Trypanorhyncha, only six of them appear to be use-ful for definition of higher taxa. Thus, an evolutionarysystematic approach was chosen.

Other strengths of this new classification are thatincongruities in the existing classifications, caused bythe use of the tentacular armature as a major characterfor distinguishing superfamilies, are omitted (Palm,1995). Furthermore, with the finding of new specieswith new combinations of the chosen six characters orwith increasing knowledge concerning misdeterminedspecies (see ‘Future studies’ below), this new classifi-cation can be enlarged to up to four superfamilies and48 families without losing its stability. It is also pos-sible to determine all the information required usinglight microscopy.

The major difference between this alternative clas-sification and the system of Campbell & Beveridge(1994) is that the tentacular armature is not used at thesuperfamily level, and, at the family level, the arma-ture has only a third level of priority. However, in thepresent alternative scheme, the armature is limited tobeing described as rows of hooks complete (homeoa-canthous and heteroacanthous typica) or rows of hookspartly reduced (heteroacanthous atypica and poeciloa-canthous). Thus, the four established trypanorhyncharmature types are still recognised as being valid, butthey are used in a different way, and only at the familylevel. Additionally, it is still possible to use the tentac-ular armature for subfamily as well as for genera andspecies definition.

The family Tetrarhynchobothriidae (sensu Camp-bell & Beveridge, 1994) shows this difference veryclearly: considering the armature to be of major impor-tance, this family is allocated to the Homeacanthoideaby Campbell & Beveridge (1994), together with theother homeoacanth families Sphyriocephalidae, Hepa-toxylidae, Tentaculariidae and Paranybeliniidae. Incontrast to this, in the presented classification the gen-era belonging to this family (sensu Campbell & Bev-eridge, 1994) were assigned to the heteroacanthoustypica family Eutetrarhynchidae.

In agreement with Campbell & Beveridge (1994),the presence and absence of blastocysts is nolonger used to distinguish the two suborders Athe-ca and Thecaphora, originally proposed by Guiart(1927), and suborders within the Trypanorhynchaare no longer recognised. Mattis (1986) showed thatthe eutetrarhynchid Prochristianella hispida (Linton,1890) (Eutetrarhynchoidea) develops a different typeof blastocyst than the otobothriid Poecilancistrumcaryophyllum (Diesing, 1850) (Otobothrioidea). Thus,the blastocysts are proposed to be convergent devel-opments within the superfamilies of trypanorhynchs.Therefore, this character was used at the family levelonly.

The characteristics of the genitalia were not used todistinguish higher taxa within the trypanorhynchs, asthey are characteristic only of adults. However, follow-ing the Campbell & Beveridge system, the characteruterus linear/uterus a transverse sac appears to be use-ful to distinguish between families without blastocystand those with blastocyst within the Tentacularioidea.Similarly, the muscles encircling the tentacle sheaths,yet lacking a prebulbular organ as present in several try-panorhynch genera, were not included in this alterna-tive classification. This was because their relationship

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to these organs as well as their occurrence within thedifferent trypanorhynch species could not be clarified.

Phylogenetic implications

The dendrogram constructed from the above proposedclassification (Figure 4), compared with the dendro-gram of Dollfus (1942) and the cladogram of Campbell& Beveridge (1994), shows very different phyloge-netic relationships between the different families. Forexample, in this proposed classification, the Otobothri-oidea is assumed to be a phylogenetically derived try-panorhynch group, which is split from all other formsby the development of ciliated pits. Otobothrioidshave a plesiomorphic tentacular armature (Pseudony-belinia odontacantha Dollfus, 1966; Paranybeliniaotobothrioides Dollfus, 1966; Pseudotobothrium dip-sacum (Linton, 1897)) and an apomorphic (Otoboth-rium spp.) tentacular armature. A second phylogeneti-cally derived group is the Eutetrarhynchoidea, havingprebulbular organs as defined by Pintner (1880). Likethe ciliated pits, these organs are characteristic devel-opments within a single superfamily.

The development of poeciloacanthous armatures isindicated by the present system to have arisen inde-pendently several times: all three superfamilies havespecies with this type of armature. It is interesting tonote that independent evolution of the poeciloacan-thous feature “double-winged chainettes” has previ-ously been proposed by Beveridge & Campbell (1989)based on the examination of oncotaxy and the anato-my of mature segments. Other remarkable similaritiesbetween the present alternative classification and thestudy of Beveridge & Campbell (1989) are that theGymnorhynchidae (synonymous with Pterobothriidaein this classification) may be derived from a commonancestor with the Gilquiniidae, and the Myxodigmati-dae may be derived from a common ancestor withthe Shirleyrhynchidae, including both ShirleyrhynchusBeveridge & Campbell, 1988 and Cetorhinicola Bev-eridge & Campbell, 1988 (Figure 4). In their morerecent work, however, Campbell & Beveridge (1994)indicated that these families were more distantly relat-ed.

Palm (1995, p. 204) demonstrated a reduction-row,a possible direction of development of the tentacu-lar armature within the genus Pterobothrium Diesing,1850. An important consequence of this was that anarmature with spiniform principal hooks and lackinga band of hooks on the external tentacle surface rep-resents a highly developed armature within the genus.

Thus, within the present classification, the total reduc-tion of tentacular hooks on the external tentacle surfaceof heteroacanthous atypica armatures is interpreted asa derived character.

It has yet to be proven by new findings, or with thehelp of molecular techniques, that the present interpre-tations of phylogenetic relationships are viable. How-ever, this alternative classification is considered to becloser to a natural system than the proposed classifi-cations proposed by Dollfus (1942) and Campbell &Beveridge (1994), as it no longer uses the hook arrange-ments on the tentacles (concluded to be convergentdevelopments) as a major character for distinguishingsuperfamilies.

Future studies

Within the present classification, the importance of thecharacter “with or without blastocyst” for distinguish-ing different trypanorhynch families causes problemsif this feature is not known, due to the availabilityof adults only or metacestodes (plerocerci) alreadyremoved from their blastocyst. Such trypanorhynchscan, however, be assigned to a family based on otherfeatures. In many cases, assignment will be to one fam-ily only, but it is possible that a choice of two familieswill occur. In such cases, assignment should be basedupon the general morphology, the number of both-ridia and the kind of tentacular armature. To date thereis a strong correlation between the presence/absenceof blastocysts and the nature of tentacular armature.However, reassignment to another position within thisclassification is possible if increasing knowledge onthe life-cycles of the species provides conflicting evi-dence.

This study shows that it is possible to assign allknown Trypanorhyncha using a classification based onsix different characters. However, in developing thepresent alternative classification, it was apparent thatcertain genera and organs remain poorly known.There-fore, it is suggested for future studies, that the follow-ing topics should be examined by trypanorhynch spe-cialists: (i) the comprehensive characterisation of thesurface ultrastructure of Grillotia Guiart, 1927, Nybe-linia Poche, 1926 and Otobothrium Linton, 1890; (ii)the functional morphology of prebulbular organs; (iii)whether or not the muscular rings around the basalpart of the tentacle sheaths are homologous to prebul-bular organs; and (iv) the functional morphology ofmicrotriches and other tegumental structures, includ-ing ciliated pits and sensory organs.

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Figure 4. Dendrogram, showing a possible phylogenetic relationship between trypanorhynch families. Characters: 1. Ciliated pits; 2. Prebulbularorgans; 3. Blastocyst; 4. Number of bothridia; 5. Reduction of the rhyncheal system; 6. Partial reduction of tentacular hooks. Roman lettersI-IV = numbers of derived characters. The length of the branches does not contain cladistic information.

Acknowledgements

My thanks are extended to Dr T. Mattis, Dr Ch. Nig-matullin and Mr H. Seilert for their valuable discus-sions. I am grateful to Drs I. Beveridge, R.A. Bray,H.-U. Dahms, S. Lorenzen, S.L. Poynton, R.M. Over-street and anonymous reviewers for their constructivecriticism on the manuscript. Financial support wasprovided by the German National Research Council(DFG).

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