Bijdragen tot de Dierkunde, 59 (1) 3-25 (1989)

SPB Academic Publishing bv, The Hague

Phylogenetic relationships of the triclads (Platyhelminthes, Seriata,

Tricladida)

Ronald Sluys

Institute of Taxonomic Zoology, University of Amsterdam, P.O. Box 4766, 1009 AT Amsterdam,

The Netherlands

Keywords: Plathyhelminthes, Tricladida, phylogeny

la Abstract da; parmi ceux-ci, un développementembryonnaire unique et

présence d’une zonemarginale adhésive.

4. On considère les Maricola comme group-frère plus primitif 1. A phylogenetic hypothesis for the triclads is presented and de la paire de taxa Terricola + Paludicola, et les Paludicola the characters on which it is based are discussed. le le dérivé des Tricladida. Sont comme représentant groupe plus formed the Bothrio- 2. The sister group of the Tricladida is by

discutés les caractères venant à l’appui de ces hypothèses (Fig. planida, and together the two taxa share a sistergroup relation- 1, caractères 14—16 et respectivement 20—22). ship with the Proseriata. 5. Au sein des Paludicola, les Planariidae et les Dendrocoelii- 3. The monophyletic status of the suborder Tricladida is sup- dae représentent ensemble le groupe-frère des Dugesiidae (Fig. ported by several derived features (Fig. 1., characters 9—12), in- 1, caractère 24). cluding a uniqueembryological developmentand the presence of 6. A l’appui du statut monophylétique des Maricola et des a marginal adhesive zone.

Terricola on mentionne un caractère, et respectivement trois 4. It is postulated that the Maricola is the primitive sister caractères apomorphes (Fig. 1, caractère 13, et respectivement the that group of the Terricola and Paludicola together and the 17—19). advanced within the Tri- Paludicola represents the most group 7. Sont discutés les cas contradictoires ou insuffisamment cladida. Characters supporting these hypotheses are discussed clairs de distributions de caractères; ceci permet d’aboutir à (Fig. 1, characters 14-16, and 20-22, respectively).

l’arbre phylogénétique le mieux en accord avec les données 5. Within the Paludicola the Planariidae and the Dendrocoeli-

prises en considération. the the dae together are sister group of Dugesiidae (Fig. 1,

character 24).

6. The monophyletic status of the Maricola and the Terricola

is supported by one and three apomorphic characters, respec- I. Introduction

tively (Fig. 1, characters 13, and 17—19).

7. Cases of conflicting or not sufficiently resolved character At present, phylogenetic research on the flatworms

distributions are discussed and are evaluated in order to arrive (Platyhelminthes) is in a state of flux. This is wit- at a phylogenetic tree providing the best fit to the data set con- nessed studies with the sidered. by dealing relationships

among the orders within the Platyhelminthes (cf.

Ehlers, 1985) and by studies which tackle sub-

of the such for Ball Résumé groups phylum, as, example,

(1974a) on the Dugesiidae, Tajika (1982a) on the

Coelogynoporidae, and Brooks et al. (1985a, b) on 1. On présente une hypothèse phylogénétique pour les tri-

the clades, et on discute les caractères sur lequels celle-ci est fondée. parasitic flatworms.

2. Le groupe-frère de Tricladida et celui des Bothrioplanida; The present paper deals with the phylogenetic ces deux taxa ensemble ont comme groupe-frère les Proseriata. relationships of the triclads or planarians, repre- 3. Plusieurs caractères dérivés (Fig. 1, caractères 9—12) vien- senting a group of flatworms which has been sub- nent à l’appui du statut monophylétique du sous-ordre Tricladi-

a wide of jected to range studies, involving mor-

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Fig. 1. Phylogenetic hypothesis for the Tricladida. Numbers refer to postulated derived characters: 1, serial arrangement of testes and vitellaria; 2, backwards directed tubiform and plicate pharynx; 3, elongate body shape; 4, loss of lamellated rhabdites; 5, tricladoid intestine;6, crossing-over of pharynx muscles; 7, parthenogeneticreproduction; 8, four pairs of longitudinalnerve cords; 9, embryolo-

cerebral female serial of adhesive Haftpapillen gy; 10, position gonads; 11, arrangement many nephridiopores; 12, marginal zone; 13, in annular zone; 14, loss of Haftpapillen; 15, resorptive vesicles; 16, reduction number of longitudinalnerve cords; 17, creeping sole;

18, pharynx musculature; 19, diploneurannervoussystem; 20, four subepidermalmuscle layers; 21, spermatophore; 22, probursal con-

dendrocoelid anterior adhesive dition; 23, dugesiideye; 24, common oviduct opening into atrium; 25, pharyngealmusculature; 26, organ

(for further explanation, see text).

in the phology, physiology, karyology, ecology and re- perienced difficulties analyzing phylogeny generation. The Tricladida, which is best consi- and historical biogeography of the freshwater dered a suborder according to Ehlers' (1985) planarians of the family Dugesiidae because of the scheme, subsumes three subgroups or infraorders, lack of a well-substantiated hypothesis on the af- viz. thePaludicola, Terricola, and Maricola. To the finities between the Maricola, Terricola, and Palu-

Paludicola belong the well-known freshwater tri- dicola. clads, whereas the Terricola and Maricolarepresent In this paper I review the phylogenetic status of the land- and marine Al- planarians, respectively. the Tricladida and put forward an hypothesis on though in the majority of cases there is no prob- the phylogenetic relationships between the three in-

in whether triclad fraorders. The aim of this lem recognizing a particular study is to present a belongs to the Paludicola, Terricola, or Maricola, phylogenetic tree based on the strongest possible these infraorders always have been poorly defined evidence available at present and to discuss the from a phylogenetic point of view. Further research characters involved. This will enable, and hopefully

the has been the fact on planarians hampered by stimulate, workers in this field to test a specific

the between the that phylogenetic relationships hypothesis against future investigations. In a study three infraorders at such this were virtually unknown, or as one, hypothesized apomorphic or least highly problematical, as has been pointed out plesiomorphic characters are always based on only

Ball For by (1981). example, Ball (1974a) ex- a sample of all the taxa involved, and it is only

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effort that be able check to assess more the relation- through a joint we may to came possible precisely

of features between these Ax and whether the derived or primitive status ship taxa. (1961) Karling

first workers conclude that the applies to all species and species groups for which (1974) were the to

hold triclads the sister of the Proseria- they are supposed to true. represented group

the Seri- ta, both groups constituting monophylum

ata. According to Karling (1974) autapomorphic

II. Material and methods characters for the Seriata are (a) the serial, longitu-

vitellaria fol- dinal arrangement of testes and (yolk

directedtubiformand The characters used were selected by a combination licles), (b) the posteriorly pli- of literature search and specimen examination. cate pharynx, and (c) the elongate body shape (Fig.

which infor- characters There are only a few publications give 1, 1, 2, 3).

of characters relevant the of the various mation on possible suites to Recently, phyletic status

of taxa within the Seriata has been re- various aspects of the phylogenetic relationships proseriate concluded the Tricladida, viz. Steinbock (1925), Meixner examined by Sopott-Ehlers (1985). She

that of the viz. the Bothrio- (1928), Kenk (1930), Karling (1974), Ball (1981), one proseriate taxa, with the and Sopott-Ehlers (1985). Other information was planida, shares a sistergroup relationship

instead of related the obtained from primary literature sources. Tricladida being closely to

I have been able to examine the majority of the other members of the Proseriata. According to species of marinetriclads but from theother two in- Sopott-Ehlers all proseriate taxa, excepting the

characterized ab- fraorders 1 studied only various representatives. Bothrioplanida, are by secondary

rhabditesof the lamellated which fea- The species of freshwater and land planarians sence of type,

is considered be for the which were studied by specimen examination will ture to an autapomorphy

Bothrio- be mentionedin the relevant sections discussing the taxon Proseriata(Fig. 1, character 4). The

Proseriata because distribution of particular character states. planida does not belong to the

the characteristics of The methodology applied in the present study the former lacks apomorphic

Proseriata and has neither the derived features concerns the phylogenetic technique developed by the

Hennig (1966). The theory and practical applica- of any of the proseriate subtaxa (Ehlers 1985: 172). tion of phylogenetic systematics have been amply The Bothrioplanida and the Tricladida, on the

the tricladoid which discussed in recent literatureand it suffices to refer other hand, share (a) intestine

and to the to Wiley (1981), Saether(1983), Hennig (1984), runs laterally pharynx (Sopott-Ehlers, 1985),

Ax (1984). Relative degree of apomorphy and (b) the crossing-over of muscle layers at the tip of plesiomorphy of characters was determinedby out- the pharynx (Steinbock, 1925), and (c) the absence

which has been of epidermal collar-receptors (Sopott-Ehlers, group comparison, a technique

detailed in Watrous & Wheeler (1981) and Maddi- 1985). The phylogenetic importance of these last-

mentioned characters will be discussed in the fol- son et al. (1984).

lowing sections.

III. Phylogenetic relationships of the Tricladida

2. On the phyletic status of Bothrioplana semperi

I. Relationship between the Tricladida and the

the Proseriata Bothrioplana semperi, representing single mem-

ber of the family Bothrioplanidae, has always been

It has long been recognized that triclads and thought to be very closely related to the triclads (cf. proseriate flatworms share a close relationship (cf. Vejdovsky, 1895; Hofsten, 1907). Most workers,

the Hofsten, 1907, 1918), but the exact nature of this however, assigned Bothrioplana to Proseriata,

its taxonomic remained affinity remained obscure for many years. With the although proper position rise of Hennigian phylogenetic systematics it be- problematic.

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Fig. 2. Diagrammatic sagittal view of pharynx musculature. A: Proseriata and Caspioplanapharyngosa, B: planariid type, C: den-

fibers indicated short horizontal circular muscle fibers dots. Abbreviations: inner drocoelid type. Longitudinal muscle by lines, by ipe,

pharynx epithelium; ope, outer pharynx epithelium.

The presence of the typical tripartite configura- However, anastomoses between the posterior intes-

tion of the intestine of planarians usually has been tinal branches occur quite frequently in marine and

char- lit- considered a very characteristic, apomorphic freshwater planarians; there appears to be very

acter of the Tricladida (cf. Karling, 1974; Ball, tle constraint on either the acquisition or the loss of

1981). However, this neat picture has always been this feature. Therefore, I consider presence or ab-

confounded by the presence of a tricladoid intesti- sence of a connection betweenthe posterior intesti-

nal system in B. semperi (cf. Sluys & Ball, 1985). nal rami to be a very weak character on this level of

and triclads Moreover, in both Bothrioplana the the phylogenetic analysis. In view of this, I support

posterior intestinal branches run laterally to the Sopott-Ehlers' (1985) suggestion that the tripartite

in the Proseriata intestinal is for Bothrio- pharyngeal pouch, contrast to system a synapomorphy

where the gut trunk runs dorsally to the pharynx plana and the Tricladida. However, in contrast to

(Sopott-Ehlers, 1985). In Bothrioplana the posteri- the afore-mentioned worker I postulate that the

rami intestine unite in or of the the hind end of the tricladoid intestine forms a symplesiomorphy for

body to form a single branch, but this is known also the triclads.

from some marine triclads (e.g. Syncoelidium pel- The second synapomorphous character for

lucidum, Procerodes trigonocephala, Procerodes Bothrioplana and the Tricladida mentioned by

harmsi) and from some freshwater planarians such Sopott-Ehlers (1985) concerns a particular change

as Dendrocoelum mrazeki, D. infernale, and D. al- in the musculature of the pharynx. It has been

bum (cf. Bresslau, 1933: 103). In view of this, it pointed out by Steinbock (1925) that in both

indeed seems justified to postulate that the tricla- triclads and B. semperi a crossing-over of muscle

doid intestine of represents a synapomorphy B. layers takes place at the tip of the pharynx. In semperi and the triclads, as has been done by Bothrioplana, marine triclads, and freshwater

Sopott-Ehlers (1985). This implies that the trifur- planarians of the families Planariidae and Dugesii-

cate intestine represents a plesiomorphic character dae the musculature of the pharynx is as follows

for the Tricladida. (Fig. 2B): outer longitudinal muscle layer, outer cir-

still Nevertheless, Sopott-Ehlers (1985) postu- cular muscle layer, inner longitudinal, and inner lates that the tricladoid intestine forms a syn- circular muscle layer. Kenk (1930) has called this

for the triclads. of that apomorphy In support the planariid typeof pharynx. In freshwater planar-

viewpoint she argues that for triclads it is charac- ians of the family Dendrocoelidae the situation is

teristic that the branches do somewhat in of two caudal gut not different that the inner zone mus- meet in the hindend of the body and that the excep- cles of the pharynx consists of alternating rows of

tions to the rule are the result of secondary change. circular and longitudinal muscle fibers (Fig. 2C). In

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land planarians the inner zone of pharynx muscles ter 2) with other types of plicate or composite

and between of muscle shows a great complexity variability pharynx. Consequently, crossing-over

This for of al- of the could indeed species. zone may, example, consist layers at the tip pharynx very ternating rows of circular and longitudinal fibers, well be an apomorphic feature at the Seriate level of

of interwoven circular and longitudinal muscle organization (Fig. 1, character 6).

fibers with beneath the and fibers, of interwoven just As a synapomorphy for the Tricladida epithelium a thin layer of longitudinal fibers, or of Bothrioplana Sopott-Ehlers (1985) also mentioned

rows of circular muscle fibers of which only the in- secondary absence of collar-receptors, but she ad-

nermost ones are interwoven with longitudinal run- mitted that the presumable absence of these recep-

fibers the Proseriata ning (Graff, 1912-1917). In tors in the two taxa may be based only on lack of there is no change of muscle layers at the tip of the sufficient information.

pharynx, the arrangement of the layers being as fol- B. semperi is characterized by an aberrant, par- lows: outer longitudinal muscle layer, outer circular thenogenetic mode of reproduction (cf. Sluys & muscle layer, inner circular muscle layer, and inner Ball, 1985) and by its four pairs of longitudinal

muscle characters longitudinal layer (Fig. 2A). nerve cords (Reisinger, 1925) (Fig. 1, 7

The change of muscle layers at the tip of the and 8). pharynx must be distinguished from the 'Schichten- wechsel' that may occur at its root. The result of the last-mentioned change is that the outer pharynx 3. Monophyly of the Tricladida musculature does not match the arrangementof the muscle layers underneath the body wall, i.e., the The monophyletic status of the Tricladida is sup- longitudinal muscles are now situated directly un- ported by at least one very complex, apomorphic derneath whereas the outer pharynx epithelium, the character, viz. a unique embryological develop- circular muscles lie the which is entally to longitudinal mus- ment completely different from that of cle layer. This change in configuration at the root close relatives such as the Proseriata and B. semperi of the pharynx occurs in many flatworms, viz. poly- (Bresslau, 1933; Reisinger, 1940; Thomas, 1986) clads, Seriata, some cylindrostomids, many (Fig. 1, character 9). The most characteristic aspect plagiostomids (Karling, 1940), and also in several in the development of triclads concerns a tem- typhloplanids (cf. Luther, 1963; Karling & Mack- porary embryonic pharynx (for summaries, see

Fira, 1973; Rieger, 1974), and in the Dalyelliidae Skaer, 1971; Benazzi & Gremigni, 1982). This par-

(cf. Luther, 1955). ticular mode of development was known already

character mentioned Steinbock for freshwater triclads the Thus, the state by at turn of this century,

and in of and later it established that similar mode of (1925) Sopott-Ehlers (1985) support a was a close relationship between Bothrioplana and the development occurs in land planarians (Carié,

Tricladida involves changes of muscle layers both 1935) and marine triclads (Seilern-Aspang, 1956).

the and the of the This This at root tip pharynx. particu- strong synapomorphous character for lar type of crossing-over is not at all uncommon triclads has not been discussed in earlier studies among the platyhelminths since it occurs in dalyel- dealing with the phyletic status of the Tricladida

Iiids (cf. Luther, 1955), kalyptorhynchids (cf. (cf. Karling, 1974; Ball, 1981), but recently the im-

Schockaert and of the Karling, 1931, 1949; Karling, portance embryonic development as a uni-

1970), and in some typhloplanids (cf. Karling & quely derived character has been mentioned by

Mack-Fira, 1973) and polyclads (cf. Bock, 1913: Sopott-Ehlers (1985) and Ehlers (1985).

303). However, it has been suggested that the vari- Several other synapomorphies of the triclads also ous types of composite pharyngés may not be have been mentioned in the literature, viz. cerebral homologous organs (Karling, 1974; Ehlers, 1985). position of the female gonads (Steinbock, 1925;

Therefore, it may be invalid to comparethe unique, Karling, 1974; Ball, 1981; Sopott-Ehlers, 1985; Eh- tubiform of the Seriata pharynx (cf. Fig. 1, charac- lers, 1985; Fig. 1, character 10), serial arrangement

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of many nephridiopores (Sopott-Ehlers, 1985;

Ehlers, 1985; Fig. 1, character 11).

that in Character 10 concerns the situation many triclads the ovaries are situated directly behind the

Steinbock brain. It was already pointed out by

(1925) that the position of the ovaries is rather vari- able. In marine triclads, for example, the ovaries

be situated at a short distance behindthe brain, may half-way between the brain and the root of the

of the be- pharynx, near the root pharynx, or even hind the pharyngeal cavity. According to Steinbock this variable position of the female gonads does not

necessarily reduce the value of character 10 if the ovaries are situated at the anterior end of the

Steinböcke remark led Ehlers oviducts. probably Fig. 3. Ventral view ofa planarian; marginal adhesive zoneindi-

cated black band. (1985) to reformulate character 10 as follows: 'both by

germaria [ovaries] constantly at the beginning of

of the germo-vitello-ducts [oviducts], i.e. near the Concerning the excretory system, the presence

also situated brain'. But Steinbock (1925) already pointed one pair of ventrally nephridiopores repre- out, in referring to Graff (1912-1917), that in sents the primitive condition within the Platyhel- several triclads the oviducts extend anteriorly to the minthes (Meixner, 1938; Ehlers, 1985). This plesio- ovaries. This holds true especially for some triclads morphous condition is present, for example, in B. in which the ovaries are situated at some distance semperi. In other flatworms, however, the number behind the brain, such as Cercyra hastata, Rhodax of nephridiopores may be increased. In some pro- evelinae, Oahuhawaiiana kazukolinda. But also in seriates several nephridiopores may be present, on

in which ovaries dorsal well the ventral surface Bdellasimilis barwicki, the occur the as as on body

directly behind the brain, there is a branch of the (Hofsten, 1907, 1918;Hyman, 1951; contra Sopott- oviducts extending anterior to the germaria. On the Ehlers, 1985: 164), but the greatest increase in num- other hand, there are also marine triclads with ber of excretion pores occurs in triclads. In planari-

several rather backwards situated ovaries (e.g. Procerodes ans there may be numerous (up to hundred)

and ventral kerguelenensis, Oregoniplana opisthopora, Pen- pores on the dorsal the body surface,

in tacoelumpunctatum, Bdellouracandida), which do arranged a pseudometameric way (Wilhelmi, not possess theanterior oviduct branch. Therefore, 1909; Meixner, 1938; Hyman, 1951), which is here

I suggest that the position of the ovaries should be postulated as a synapomorphy for the Tricladida

weighted independently of the course of the (Fig. 1, character 11). To the best of my knowledge, oviducts. data on the number of nephridiopores in triclads

In the Terricola and the Paludicola the position only stem from studies done on either freshwater of the ovaries is less variable than in the Maricola triclads or on marine planarians, so that the Terri-

(Graff, 1912-1917; Meixner, 1928). cola remain to be tested in this respect.

In view of the above, I propose that the cerebral There is another synapomorphy for the triclads,

mentioned position of the germaria represents a synapomor- in addition to the three above. It con-

for triclads in which of adhesive phy the (Fig. 1, character 10), thus en- cerns the way the openings dorsing the suggestions of previous workers. Devia- glands are arranged on the ventral body surface

from this tions groundplan, consequently, are (Fig. 1, character 12). These openings are situated hypothesized to be the result of secondary change in a marginal adhesive zone, which forms a ring on instead of the retention of the primitive character the ventral body surface, near the margin of the state. body (Fig. 3). This annular zone of adhesive gland

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openings is unique to the triclads because in other of a so-called anchor cell and two types of gland

the thebrush-like flatworms the openings of the glands have a much cells, the 'necks' of latter forming

In the of the For adhesive with two types of more irregular distribution. majority projections. organs coined the otoplanids adhesive glands are confined to the gland cells Tyler (1976) name duo-gland posterior body region (Ax, 1956), and also in other adhesive system.

cells known from proseriate taxa the arrangement of the openings is Duo-gland adhesive are many

of flatworms, and it has been hypothesized totally differentfrom that of triclads. For example, groups

- for the in the Coelogynoporidae the adhesive papillae that this character forms a synapomorphy through which the secretion of adhesive glands is large taxon Rhabditophora (Ehlers, 1985). From

studies it known - into 'Haftfelder' which discharged are arranged light microscopical was already

of the Proseriata are usually are distributedirregularly on the sides of the that the Haftpapillen very

these 'Haftfelder' similar those of the marine triclads and ultra- body; in some coelogynoporids to

into structural have these find- are arranged irregularly running longitudinal investigations supported neither in the rows (Tajika, 1982a). ings (Tyler, 1976). But proseriates,

in other of the the nor any taxon Rhabditophora are

in adhesive Haftpapillen arranged a marginal zone,

the Tricladida the in the Maricola. This adhesive band is 4. Phylogenese relationships within as is case

about four anchor cells wide, i.e. there are about

(a) Monophyly of the Maricola and phylogeny of four Haftpapillen situated side by side.

the infraorders Thus, for the marine triclads it is not the mere

their presence of Haftpapillen which represents

but it is the According to the phylogenetic hypothesis put for- synapomorphous character, arrange-

marine triclads the of the in band which ward here (See Fig. 1), the were ment Haftpapillen a marginal first to branch off from the main stem, whereas is uniquely derived for the Maricola. subsequently the land planarians and the fresh- In freshwater and land planarians the marginal

charac- water triclads evolved. band of adhesive cells is present also (Fig. 1,

1909: the but it is of different In the Terri- In general (but see Wilhelmi, 386), ter 12) a structure.

monophyletic origin of the marine triclads has been cola and the Paludicola there are no Haftpapillen

and the secretion of the adhesive is dis- accepted, implicitly or explicitly, by numerous wor- glands kers. But autapomorphous characters supporting charged through the epidermal cells. Since it is this assumption remained to be discovered, as has highly likely that the common ancestor of the Seria- been pointed out by Ball (1977a, 1981). It is here ta possessed Haftpapillen, the absence of the latter

of adhesive in Terricola and Paludicola of hypothesized that the presence papillae represents a case which are arranged in a marginal band, is a syn- secondary loss, which is here hypothesized to be a

marine triclads 1, charac- for these 1, char- apomorphy for the (Fig. synapomorphy two groups (Fig. ter 13). acter 14).

For marine triclads adhesive papillae or 'Haft- That the common ancestor of the Seriata had

that papillen' were described and depicted already in Haftpapillen is based on the hypothesis these

1863 by Claparède and in 1881 by Lang. When structures arose in the ancestor common to the Seri- studied under the light microscope these Haft- ata, Typhloplanida, Kalyptorhynchia, Dalyellioi-

small brush-like or mushroom- da, and the flatworms. Absence of Haft- papillen appear as parasitic shaped structures which project above the epider- papillen in the Dalyellioida and the parasitic flat- mis (Fig. 4). Through these Haftpapillen is dis- worms is then explained by secondary loss in their

which the charged the secretion of adhesive glands, common ancestor. Haftpapillen and duo-gland were mentioned already above. The ultrastructure adhesive system are absent in the Catenulida, of the adhesive papillae of marine triclads, among Nemertodermatida, Acoela, Lecithoepitheliata, others, has been studied by Tyler (1976). It ap- and Prolecithophora. Polyclads and macrosto- peared that each adhesive papilla-complex consists mids, the primitive members of the Rhabditophora

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vitellaria of various species of freshwater planari-

ans. The same worker observed that within the

large vacuoles ('Dotterkammern') of the vitellaria

degeneration and resorption of spermatozoa take

place. According to the information provided by

Cernosvitov (1931) resorptive vitellarian follicles

occur in the following species of freshwater planari-

ans: Dugesia gonocephala, D. polychroa, D. bur-

maensis, Dendrocoelum lacteum (see also

Kaburaki, 1918, 1922), Phagocata paravitta, P. ar-

meniaca, D. album, D. subterraneum,Planaria tor-

Baikalobia rad- va, Bdellocephala schneideri, and

dei. Resorptive vesicles have also been described for

Fig. 4. Transverse section through the adhesive papillae of Cer- Dugesia annandalei (Kaburaki, 1918). In more re-

the Abbrevia- cyra hastata, as seen through light microscope. cent literature similar structures were described for

tions: agl, adhesive glands;ap, adhesive papilla; rh, rhabdite; se, Neppia schubarti (Marcus, 1946), Dendrocoelum secretion. maculatum, D. sanctinaumi, Phagocata ochridana,

and P. leptophallus ( Reisinger, 1963; Kenk, 1978).

(cf. Ehlers, 1985: 168), do possess the duo-gland In the two last-mentioned species the vacuolated adhesive system, but the secretions are discharged portion of the vitellarian follicles is developed to via Haftpapillen different from those of the such an extent that they have been referred to as ac-

seminis proseriates, triclads, and rhabdocoels (cf. Tyler, cessory receptacula (cf. Reisinger, 1963,

1976). Fig. 2). I observed resorptive follicles also in

In the Paludicola the marginal adhesive zone has Spathula camara and in another, still undescribed the same function as in marine triclads, i.e. the species of Spathula.

dur- animals use it for attachment to the substrate Concerning the Terricola, resorptive vesicles

ing locomotion. But in the Terricola the marginal have been described for Kontikia orana (cf. Froeh- adhesive zone must have another function, as has lich, 1955; Winsor, 1986), and similar structures been pointed out by Graff (1912—1917), because were reported for Bipalium ephippium, Pel- land planarians use a specialized creeping sole (Fig. matoplana sondaica, Geoplana nasuta (cf. Loman,

1, character 17) for locomotion. 1890), and G. sieboldi (cf. Krsmanovic, 1898). Re-

There is another character supporting the examinationof K. bulbosa revealed that resorptive hypothesis that the Terricola and the Paludicola vesicles are present also in this species. share observed vesicles a unique common ancestor, viz. the presence Because I have never resorptive of resorptive vesicles (Fig. 1, character 15). These in marine triclads, it is here hypothesized that these vesicles are altered vitellarianfollicles which func- vesicles are a synapomorphy for the Terricola and tion in the resorption of excess sperm. Recently, the Paludicola. such resorptive vesicles were described, indepen- The third synapomorphy for the Terricola and

of dently previous studies, for Bdellasimilis bar- Paludicola is the secondary reduction of the num-

wicki & of which the (Sluys Ball, 1989), a species ber of longitudinal nerve cords (Fig. 1, character phyletic status is still uncertain. In the course of the 16), which will be illustrated in the following sec- present study a literaturesearch learned that similar tion on the monophyletic origin of the landplanari- structures, with a similar function, have been ans. Concerning this reduction of nerve cords, a reported for freshwater and land planarians. Cer- parallel development is seen in the Otoplanidae, in nosvitov in his in derived (1931), study on sperm resorption which there are also forms that show the

several observed triclads, mentions authors who condition of two pairs of nerve trunks or of only

in the of the sperm ventral, vacuolated portion one pair of main nerve cords (Ax, 1956).

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nerve plexus is connected with the ventral nerve

cords and commissures by means of short and thin

bundles of nerve fibers, or so-called 'ventral

bridges'. The situation with three pairs of longitu-

dinal nerve trunks is presumed to be the primitive

conditionwithin the Tricladida, since a similar con-

figuration is characteristic of, at least, the Oto-

Fig. 5. Diagrammatic transverse sections showing the nervous planidae (Ax, 1956).

A: Maricola, B: Paludicola, and C: Terricola (modified system. In the Paludicola(Fig. 5B), the situation is some- from Meixner, 1928). Abbreviations: dc, dorsal commissure; what differentin that the dorsal and lateral pairs of dlc, dorso-lateral commissure; dnc, dorsal nerve cord; dvc, longitudinal nerve cords are very inconspicuous or dorso-ventral commissure; mnc, marginal nerve cord; pl,

almost absent, i.e. their nerve fibers have joined the plexus; vb, ventral bridge; vc, ventral commissure; vlc, ventro-

lateral commissure; vnc, ventral nerve cord; vnp, ventral nerve commissures to form a sort of plexus.

plexus. In the Terricola only the pair of ventral nerve

cords is fibers of the present, whereas the other lon-

(b) Monophyly of the Terricola gitudinal nerve cords and those of the commissures

form a close-meshedplexus. In the land planarians

The monophyletic status of the Terricola is sup- the ventral subepidermal nerve plexus is highly de-

the ported by following autapomorphies: (1) pres- veloped, which probably relates to the presence of

ence of a creeping sole (Fig. 1, character 17); (2) a creeping sole. As in the Paludicolaand the Mari-

different type of pharyngeal musculature, as com- cola the ventral subepidermal nerve plexus of the

with the Maricola and Paludicola pared (character Terricola is connected with the ventral nerve cords

and 18), (3) diploneuran nervous system (character and the ventral commissure through ventral

19). bridges. In the Terricola the pair of ventral nerve

The term creeping sole is here used in a very cords takes a much more internal position in the

broad sense, referring to the complex, protruding body, as compared with the Maricola and Paludi-

well the flat cola. The of type as as to very simple, type of creep- nervous system the Terricola has been

sole found in the called the ing as Geoplanidae (cf. Graff, diploneuran nervous system (Steinbock,

1899, 1912-1917). 1925).

the In above (p. 7) mention was already made of The interpretation of the similarities and differ-

the and different of complex type pharynx mus- ences between the nervous systems of the three

which is here triclad culature, proposed as a synapomor- infraorders, as provided above, follows that

for the terricolans. of Meixner Steinbock phy (1928). (1925), however, con-

The different structure of the terricolan nervous cluded that the ventral nerve cords of the terrico-

and its taxonomic value system were discussed in lans are not homologous with those of the Paludi-

detail by Steinbock (1925). He noted that the ner- cola and Maricola. Steinbock followed Graff

of the Terricola differs from both the in the vous system (1899) assuming that nervous system of the

Maricola and the Paludicola. flat, neotropical geoplanid Terricola formed the

In the Maricola the consists of nervous system a starting point of an evolutionary morphocline. In

number of bilaterally arranged longitudinal nerve these particular geoplanids the nervous system con-

connected various commissures sists of diffuse cords, through a nerve plexus or nerve plate beneath

(Fig. 5A). Further, a fine nerve plexus is situated the gut. In other terricolans fibers and ganglia from

beneath the basement membraneof the just epider- the ventral nerve plate would gradually have con-

mis, the Actu- centrated forming subepidermal nerve plexus. to form the two ventral nerve cords,

ally, the marginal nerve is of this nerve which are part plexus present in many land planarians. Con-

and it is different morphologically from the other nections or commissures between the two ventral

trunks. the ventral nerve Especially subepidermal nerve cords are supposed to be derivatives of the

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thin of polated a very layer diagonally arranged

muscle fibers. This diagonal muscle layer consists

of two, crosswise arranged, rows of fibers and is

usually difficult to observe. According to Graff

(1912-1917: 2746), the subepidermal musculature

of the Terricola shows the same layers, although Fig. 6. Subepidermal musculature. A: Proseriata, Maricola,

each of them be to an extent never Terricola. B: Paludicola. Abbreviations: cm, circular muscle may developed

longitudinalmuscle layer; layer; dl, diagonal muscle layer; lm, found in the Maricola or Proseriata (Fig. 6A).

outer longitudinal muscle layer; vep, ventral epidermis. olm, In freshwater planarians there is an extra, lon-

gitudinal muscle layer interpolated between the cir-

nerve plate and, consequently, are supposed to be cular and the diagonal muscle layer, as was already differentfrom the ventralcommissures in the Palu- pointed out by Meixner (1928). This means that the

dicola and Maricola. subepidermal musculature of freshwater planarians

do not think that there is evidence that I any consists of the following layers (Fig. 6B): layer of

Graff's morphocline concerning the nervous sys- circular muscles directly beneath the basement

tem in the Terricola is polarized from an evolution- membrane, thin layer of (outer) longitudinal mus- phylogenetic perspective. Moreover, there is ary, cles, diagonal layer, and (inner) longitudinal muscle ample morphological evidence (see above) that the layer. The extra layer of outer longitudinal muscles cords the homolo- ventral nerve of Terricola are of is very thin, consisting of only one row fibers, with those of the Maricola and Paludicola. gous and it is usually difficult to discern. Moreover, this Therefore,it is here hypothesized that the diploneu- not on of the body. layer may be present every part ran nervous system only represents a quantitative Generally, modern triclad specialists pay little at-

as compared with the Maricola and differentiation, tention to the subepidermal musculature and, con- Paludicola. In the land planarians the number of sequently, their species descriptions do not give any the ventral sub- nerve cords is reduced, whereas information the absence of the on presence or outer Al- nerve plexus is highly developed. ofthe older epidermal longitudinal muscle layer. In some pub- though the differences with the Paludicola and lications mention is explicitly made of the presence in and Maricola are only quantitative nature not but also of this thin muscle layer, e.g. Neppi (1904) qualitative, i.e. not concerning entirely new struc- Marcus (1955) for Dugesia neumanni, Seidl (1911)

it is still that the nervous of the tures, true system for Polycelis sabussowi, Korotneff (1912, cited in

Terricola has a characteristic and different very Graff, 1912-1917) for Sorocelis, Kenk (1925) and

shape. Therefore, the diploneuran nervous system and Graff Dahm (1960) for Dendrocoelopsis, for the is still hypothesized to be an autapomorphy (1912-1917) concerning references involving other Terricola (Fig. 1, character 19). species.

of the The very indistinct nature outer longitudi- (c) Monophyly of the Paludicola nal muscle layer probably accounts for the fact (1)

of The unique common ancestry of the freshwater that I observed this layer in some specimens a

triclads is based on the following synapomorphies: Paludicolan species, whereas I failed to discern it in

that for (a) subepidermal musculature consisting of four other specimens of the same species, and (2)

transfer between layers (Fig. 1, character 20); (b) sperm some species there are discrepancies my

through spermatophores (character 21); and (c) observations and statements in the literature.As ex-

probursal condition (character 22). amples of the last-mentioned point I mention the

the and the Mari- Weiss did In Proseriata, Bothrioplanida, following cases. (1910) apparently not

muscle in cola the subepidermal musculature consists of an observe the outer longitudinal layer

outer, subepidermal layer of circular muscles and Dugesia hoernesi, D. boehmigi, and D. graffi,

the material an inner layer of longitudinal muscles. For at least whereas I observed this muscle layer in

the Otoplanidae and the Maricola it has been estab- prepared by the aforementioned worker. Accord-

muscle lished that between these two muscle layers is inter- ing to Ball (1970) the outer longitudinal

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layer would be absent in Dugesia nannophallus and ry bursa in front of the male copulatory apparatus

in D. batuensis. However, examination of new (Fig. 1, character 22), whereas in the Maricola the

material revealed that this fourth muscle layer is bursa is situated behind it, the latter condition be-

also present in these two species. ing the primitive situation within the Tricladida.

I found the outer longitudinal muscle layer to be The probursal condition appears to apply well for

present also in specimens of the following species: the Paludicola as defined in this study (see Fig. 1),

Cura pinguis, C. patagonica, Dugesia andina, D. excepting those species in which a copulatory bursa

lugubris, Bdellocephala brunnea (from Russia), is completely absent. In view of the fact that a

Sorocelis hepatizon, and an unidentifiedDugesia copulatory bursa is considered to be a basic struc-

(Girardia) species from Colombia. ture in the organization of flatworms (Remane,

It is evident that within the Paludicola the char- 1951), absence of the bursa is here assumed to be

acter of the outer longitudinal muscle layer deserves the result of secondary loss, which has occurred in-

much more attention thanit receives at present. The dependently in the Paludicola, Maricola and Ter-

distribution of this character should be checked ricola.

carefully over the various paludicolan taxa. Pend-

ing further information, the phylogenetic hypo- (d) Relationships within the infraorders thesis proposed here assumes the outer longitudinal

muscle layer to be a synapomorphy for the fresh- In his study of the Paludicolaand the Dugesiidae in water triclads (Fig. 1, character 20). particular, Ball (1974a) suggested that the Den-

During the copulation of marine triclads free drocoelidae couldbe characterized by two apomor- sperm is discharged into the partner, whereas in the phies, viz. the different type of inner pharyngeal

with Paludicola as a rule sperm is transferred by means musculature, as compared other planarians

With character and the of of spermatophores. respect to the freshwater (Fig. 2C; Fig. 1, 25), presence planarians, presence of spermatophores has been anterior adhesive organs (Fig. 1, character 26). In mentioned for species of the genera Dugesia, this particular study Ball (1974a) failed to find

Planaria, Polycelis (cf. Weiss, 1910; Graff, 1912- defining, autapomorphous features for the Planari-

1917; Kaburaki, 1917, 1918; Reisinger, 1923), idae and the Dugesiidae, but in later publications

Phagocata (Kaburaki, 1917; Okugawa, 1939), and (Ball, 1974b, c) he noted that the Dugesiidae were

Neppia (Marcus, 1955, 1970; cf. Ball, 1974c). Fur- characterized by a peculiar eye structure (Fig. 1,

character ther, I observed a spermatophore in the bursal 23). In theDugesiidae the pigment cup is canal of an unidentified species of Spathula from multicellular, and contains numerous retinal cells

Australia. The more or less sclerotized wall of these (cf. Ball, 1981, Fig. 4D). This contrasts strongly spermatophores is formed by the secretion of with the unicellular eye cups with usually only a few

in retinal cells which found inthe Maricola glands the penis. An exception may be formedby are and the

Dugesia seclusa in which only 'free sperms' were non-Dugesiid members of the Paludicola. The Ter- observed in a spacious chamberin the penis papilla ricola complicate the picture in that multicellular

with retinal and in the copulatory bursa (Sluys & De Vries, eye cups numerous cells are found also

in land However, the 1988). planarians. dugesiid eye

absent in differs from the of found in Spermatophores are thought to be the types eye the land

Terricola (Meixner, 1928), but Heinzel (1929) ob- planarians in that in the former the dendrites enter served in theatrium the via its thus the a spermatophore-like structure eye cup opening, penetrating cor- of Platydemus victoriae. Pending further studies it neal membrane, whereas in the Terricola the den- is here hypothesized that sperm transfer through drites enter through the openings between the pig- spermatophores forms a synapomorphous charac- ment cells (cf. Hesse, 1902). Autapomorphies ter for the freshwater planarians (Fig. 1, character defining the Planariidae remain to be discovered.

21). That the Planariidae and the Dendrocoelidae

In general, freshwater triclads have the copulato- share a sistergroup relationship is suggested by the

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fact that in these taxa the common oviduct opens porids. Tajika (1982a) points out that with respect into the atrium (Fig. 1, character 24), whereas the to the female genital duct, shell glands, and ovi-

Dugesiidae show the plesiomorphous condition in ducts the situation in the Coelogynoporidae is which the oviducts communicate, separately or essentially conform to Meixner's (1928) type I or- combined, with the bursal canal (Ball, 1974a, ganization in triclads. This wouldindeedimply that

1981). Although I agree with Ball's conclusion I for the triclads type I is primitive and thatthe con-

in which oviduct into the wish to elaborate on the reasoning that led me to en- dition the common opens

Ball dorse his hypothesis because it differs somewhat atrium is derived, as suggested by (1974a). But

if consider the the character from his argumentation. we Otoplanidae state

The condition whereinthe oviducts uniteto form polarity would be reversed! Consequently, assess- a commonoviduct which, after receiving the secre- ment of character state polarity based on distribu- tion of shell glands, opens into the genital atrium, tion of states in the Proseriata, is equivocal.

occurs in many platyhelminth taxa and forms Reference to the Maricola and, more important-

the Terricola enables reach without doubt a primitive character for many ly, to us to a decisive

in In the Maricola the oviducts phylogenetic groups. However, the particular polarity assessment.

case considered here it is probably much more rele- generally communicate, separately or combined, vant to compare the Paludicola with those func- with thebursal canal or equivalent duct, which also tional outgroups which possess a copulatory bursa receives the openings of the shell glands. In terrico-

with the communi- and bursal canal comparable to those of triclads. It lans a copulatory bursa oviducts

of oviducts with the bursal is the 'association' (Ball, 1974a: 344) cate, separately or combined, canal; and bursal canal that is here at stake. Under the the oviducts and/or bursal canal receive the secre-

functional be tion of shell Because in the Terricola and in present hypothesis outgroups are to glands.

found the land the marine the Maricola the oviducts are 'associated', i.e. com- among planarians,

triclads, and the proseriates. municate with the bursal canal, the condition in

According to Ball (1974a: 344) in proseriates the which the common oviduct opens into the genital oviducts 'are usually associated with the bursal atrium forms indeed a synapomorphy for the Den- stalk or equivalent female genital canal'. Due to its drocoelidae and the Planariidae (Fig. 1, character

generality, however, this statement is incorrect. In 24), as proposed by Ball (1974a). otoplanids there is no association between the com- It must be noted that there is a vexed issue in the mon oviduct, which receives the secretion of shell platyhelminth literature which has become known

glands close to its opening into the atrium, and the as the bursa problem (cf. Steinbock, 1924, 1966). In bursal canal. there the the bursa relates the On the contrary, is a distinct present context problem to separation between the openings of the common question whether the bursa and bursal canal in oviduct and the bursal canal into the genital atrium triclads are really homologous with similar struc-

(cf. Ax, 1956). In coelogynoporids the oviducts tures in the proseriates. Ifit can be shown that there open into the distal part of the female genital duct, is no homologous relationship then the compari- which lesser in this between and triclads may be developed to greater or extent son, respect, proseriates

(Tajika, 1982a). According to Tajika (1982a) the becomes irrelevant.

female genital duct results from fusion of the two The intrafamilialrelationships of the Dugesiidae oviducts, so that actually it is a common oviduct, have been studied by Ball (1974a, c), but the the is histology of which different from that of the Planariidae and the Dendrocoelidae have never

genital atrium. This female genital duct receives the been subjected to a detailed phylogenetic analysis.

shell land openings of glands. Posterior (= entally) to Phylogenetic relationships among the the point where the oviducts unite to form the fe- planarians are still to be studied, but in view of the male genital duct, the latter communicates with the copulatory apparatus it is likely that the Micropla- bursal canal or with the genito-intestinal duct, ninae are the most primitive taxon in the Terricola, structures which are present in many coelogyno- as was suggested by Marcus (1953) and Froehlich

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i.e. the reduction of the anterior (1967). The copulatory apparatus of many micro- latter condition,

trunk forms derived character for the Paludi- planids resembles more or less that of the Maricola. gut a

cola As examples 1 mention Microplana scharffi and M. (Meixner, 1928; Ball, 1981). mention here that in terrestris (cf. Ball & Reynoldson, 1981), M. As a short digression I spe-

of mention is monacensis (cf. De Beauchamp, 1961, Fig. 59A), cies descriptions planarians usually but and also ,M. aberana (cf. Meli, 1904) and M. henrici made of extension of the gut beyond the eyes

the brain reference (cf. Minelli, 1977). that it is preferable to use as a

The phylogenetic relationships within the Mari- point and to speak of the presence or absence of a

coecum. This means that the character cola are the subject of an ongoing study of the precerebral

be scored also for triclads which lack present author. states can eyes

in which and can be compared with outgroups eyes

are also absent. Since at least in marine triclads the

situated to the brain there IV. Discussion eyes are usually dorsally

between is in this group an almost exact synonymy

the character coecum and 'exten- With respect to relationships within the Tricladida state precerebral

less sion of the anterior trunk in front of the the results of the present study are more or gut eyes'.

compatible with suggestions expressed by the few The precerebral coecum has also been referred to as

workers who have given this subject detailedatten- cephalic duct.

Meixner that tion (cf. Meixner, 1928; Ball, 1981). The present It was already pointed out by (1928)

have treatment differs from previous studies in that it the Maricola usually a precerebral coecum

broader data base in whereas such a structure is absent in the Paludicola, provides a more rigorous, sup-

the worker. In Meixner's view port of the proposed phylogenetic hypothesis, and according to same

that it results in the recognition of monophyletic the triclads evolved from otoplanid-like ancestors

either defined and therefore he homologized the precerebral coe- groups which previously were poorly

of the Maricola with the or not defined at all by apomorphic characters. cum 'Kopfdarm' (= pre-

The phylogenetic hypothesis formulated in this cerebral coecum) of the Otoplanidae. According to

of ad hoc Meixner the Maricola characterized a further study attempts to minimize the number are by

and the assumptions concerning parallel and convergent development of the precerebral coecum

a reduction of the latter. However, evolution. Nevertheless, the phylogenetic tree pre- Paludicola by

information indicatesthat evaluationof the sented (Fig. 1) still subsumes a number of interest- present

confound- absence of in ing cases of parallelism as well as a few presence or a precerebral coecum

ing instances of supposedly independent develop- triclads is now more complex than suggested by

Meixner ment, of which some were already mentioned in (1928).

and the previous sections. A few other cases of parallelism In otoplanids coelogynoporids histology

from that of will be detailedbelow. Furthermore, attention will of the precerebral coecum is different

characteristics which the of the intestine in that it shows be paid to a few to phylo- rest usually no

genetic importance has been assigned in previous lumen but is filled with cells or with a syncytial

In that Meixner still be in studies, but which have not been used in the con- mass. respect may correct

struction of the phylogenetic tree here presented. his suggestion that the Maricola show a derived

condition of the precerebral coecum because in

it functions of the these planarians as a proper part

of 1. Precerebral coecum intestine, while its histology is similarto the rest

the the gut. But when more taxa within Seriata are

and of One case of parallelism concerns the situation that taken into account assessment of homology

derived status of the in triclads the anteriorly running gut trunk may the primitive or precerebral

terminate becomes less clear. either extend in front of the eyes or just coecum behind the It has been that the In the and the Otomesostomidae eye cups. postulated Bothrioplanida

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the intestine does not extend in front of the brain Actually, there are more Australianand Tasmanian

& In the freshwater with (cf. Hofsten, 1907; Sluys Ball, 1985). planarians a precerebral coecum

Monocelididae the majority of species of the the gut than is apparent from the literature.In descrip-

terminates dorsally to the brain but in the genera tions of these species the forward extension of the

Asilomaria and Archimonocelis the intestine forms anterior gut trunk is being assessed relative to the

diverticulum of the of a precerebral (Karling, 1967; Tajika, position eyes. However, examination

do of in 1981). The Nematoplanidae have a precerebral specimens several of these species showed that

with the coecum which in some species communicates genera Spathula and Romankenkius the eyes

in it does situated brain and the intestine, but others not so. Moreover, are anteriorly to the not directly

it is not certain whether the precerebral coecum of dorsally to the brain, as in marine triclads. This im-

that the Nematoplanidae is derived from the intestineor plies that in species for which it is mentioned

the from chordoid tissue which builds also the chorda the anterior gut trunk extends to or between

animals it well be the that the forms intestinalis in these (cf. Meixner, 1938; eyes may case gut a

Tajika, 1979, 1982b). Thus, it may be that at least cephalic duct. For example, in Romankenkius

the precerebral coecum of the Nematoplanidae is kenki, for which it is mentionedthat 'the anterior

intestine forwards the level non-homologous with that of the Maricola. Ac- ramus of the extends to

chordoid the situated far cording to Ax (1957) the precerebral coe- of the eyes' (Ball, 1974c: 7), eyes are

which is devoid of from in front of the brain, so that the cum, a lumen, originated species actually

the intestine independently of the similar origin of possesses a well-developed precerebral coecum.

is the precerebral coecum with a resorptive function. Because presence or absence of a cephalic duct

Therefore, Ax (1957) denies a homologous relation- variable in the ingroup and the outgroups, assess-

of of relative of the ship between the chordoid precerebral coecum ment apomorphy or plesiomorphy

proseriates and the 'Kopfdarm' of other platyhel- character states becomes arbitrary for the Tricladi-

minths. da. Consequently, the cephalic duct has not been

It is clear that presence or absence of a precere- used as an apomorphic feature in thepresent phylo-

bral character which variable such coecum are states are genetic hypothesis. However, once an hypo-

in the But also within the thesis hasbeen formulated it be that Proseriata. Tricladida may postulated there is variability. With respect to land planarians the precerebral coecum forms an underlying syn-

a precerebral coecum may be present in one species apomorphy, supporting the monophyletic status of and absent in another, but the distribution of the the Seriata.

character states over the species(groups) is less well-

known than in the Maricola and the Paludicola.

Although Meixner (1928) was correct in his state- 2. Probursal condition ment that the majority of species of marinetriclads show a precerebral coecum it is also true that there That freshwater triclads usually have the copulato- are several maricolanswhich lack the cephalic duct, ry bursa in front of the male copulatory apparatus

Procerodes e.g. kerguelenensis, Micaplana misae, is an apomorphic character for the Paludicola, ac-

Cercyra teissieri, Puiteca rigida, Bdelloura candi- cording to the phylogenetic hypothesis formulated

da, B. propinqua, and Syncoelidium pellucidum. above. But there are a few species which confound

And Meixner's conclusion that the Paludicola are the picture. The most extreme case is found in the

characterized by a reduced cephalic duct has lost its marine triclads Probursa veneris and P. moei. In

general validity because it is now known that there both species the bursa is situated in front of the

Tasmanian and are Australian paludicolans with a male copulatory apparatus, just as is the case in

distinct there precerebral coecum, e.g. Spathula trucu- many paludicolan planarians. Further, are lenta. S. gourbaultae, S. fontinalis, S. tryssa (cf. several marine triclads in which the bursal canal

Ball, 1977c), S. dittae, and S. ochyra (cf. Ball & curves antero-dorsad, with the result that the copu-

Tran, 1979), Eviella hynesae (cf. Ball, 1977d). latory bursa lies above the male atrium or above the

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hastata, drocoelidae (Fig. 1, character 25). But there are a genital duct, e.g. Cercyra Obrimoposthia

number of in which the muscles of wandeli, Pacifides psammophilus. As confounding dendrocoelids

mentioned Bdellasimilis bar- the viz. Caspio- cases Ball (1981) also pharynx are differently arranged, Acromyadeni- wicki Eviella hynesae, the genus Opisthobursa, plana pharyngosa, Polycladodes,

and the Kenkiinae. In Caspioplana and Balliania thetisae. However, these four cases um, subfamily

to the situa- be too after all. In the first the pharyngeal musculature conforms may not problematical in the Proseriata In place, the copulatory bursae of Bdellasimilis and tion found (Zabusova, 1951).

and the outer Eviella are no true bursae since in the first-men- Polycladodes Acromyadenium

musculature is different in that it con- tioned species the supposed bursa concerns an ac- pharyngeal and circular cumulationof resorptive vesicles (cf. Sluys & Ball, sists of alternating rows of longitudinal

1989), whereas in E. hynesae the bursa actually is muscles (Gourbault, 1972).

of muscles in the the expanded portion of the female genital duct The arrangement pharynx does conform (Ball, 1977b: 153). Secondly, the taxonomic posi- paludicolan genus Macrocotyla not situations in 2. The tion of the two species of Opisthobursa, Balliania to any of the depicted Fig.

in inner of thetisae and similar species like Rhodax evelinae, difference resides the zone pharynx mus-

this zone consists of two and Mitchellia sarawakana are still highly proble- cles. In Macrocotyla lay-

viz. one of circular fibers immediately un- matical. Except for Rhodax, these species have ers, layer and been assigned to the Maricola, but always with derneath the inner pharynx epithelium a sur-

of circular many reservations. However, there are also a num- rounding layer composed intermingled

muscle fibers It has ber of characters which point to a closer relation- and longitudinal (Kenk, 1975).

been debated whether should be ship with the Paludicola, which would indeed com- Macrocotyla

dendrocoelids should be clas- plicate the phylogenetic interpretation of the pro- ranked among the or

there is sified in fourth bursal condition. But in that case, always a separate, (sub)family, together

with the Kenkia and the possibility that the bursa of Opisthobursa, for genera Sphalloplana (cf. Ball, example, is different from that of other aquatic 1974a; Kenk, 1975; Kawakatsu & Mitchell, 1981).

This Kenkiinae is characterized the planarians, as has been pointed out by Ball (1977b: subfamily by

internal muscle of the 154). fact that the zone pharynx

consists of circular muscle direct- In contrast to Ball (1981: 10), who stated 'that two layers, a layer

underneaththe inner and en- there are no compelling reasons for assuming the ly pharynx epithelium

inter- probursal conditionof the Paludicolato be unique- tally to this layer either longitudinal fibers or

and circular muscles. ly derived', it is here postulated that the probursal mingled longitudinal

of of the land condition asserts the unique common ancestry of In the majority species planarians

the musculature is much the Paludicola. The confounding cases of paral- pharyngeal more complex

than in the and the dendrocoelid of lelism mentionedabove, in particular Probursa, are planariid types

in the Maricola and Paludico- considered to be the result of independent evolu- pharynx which occur tionary pathways. Species like Probursa veneris, la (see above). Exceptions are formed by some spe-

Obrimoposthia wandeli, and Cercyra hastata do cies of the terricolan family Rhynchodemidae such

characteristic of as henrici and (Micro- possess Haftpapillen and features Microplana Rhynchodemus

dendrocoelid of marine triclads and be- which have a type more restrictive groups of plana) richardi,

other of the cause of parsimony these characters have been pharynx (cf. Bendl, 1909). In members

the is neither of the den- given priority over the probursal condition. family, however, pharynx

drocoelid type nor like that of the planariid type.

of musculature That a comparison pharyngeal

3. Pharynx should take into account not only the inner muscle

layers but also the outer zone of muscles is exempli-

It has been postulated that the dendrocoelidtypeof fied by the land planarian Microplana purpurea.

for the Den- In this the inner musculature is pharynx represents an autapomorphy species pharyngeal

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similarto that of the planariid pharynx but the out- reproduction is primitive for the Platyhelminthes as

is different in that it has and another er muscle layer an extra a whole (Rieger, 1986), hypothesis row of longitudinal fibers entally to the row of cir- postulates that asexual reproduction has arisen in-

cular muscles (Bendl, 1909). dependently and secondarily in several groups of

flatworms (Ax & Schulz, 1959). The last-mentioned

authors specifically mention the Tricladida as a

in which several members have 4. Reproduction group secondarily

acquired the asexual mode of reproduction. In view

According to Calow & Read (1986) the phylogeny of these conflicting hypotheses it is not easy to of the Paludicola as proposed by Ball (1981; see evaluate the occurrence of sexual reproduction in also Fig. 1) parallels the trend fissiparity — non- the Maricola, the Terricola, and the Dendrocoeli- fissiparity. In this section it will be examined dae and the presence of asexual reproduction in the

the the and terricolans. whether this trend indeed supports hypothesis. Planariidae, Dugesiidae, some

Meixner (1928) already mentionedthat a charac- Since reproduction through fission is not known in

teristic feature of the Maricola is that they repro- the Proseriata I favor the hypothesis that asexual

duce only sexually through the formation of co- reproduction is a derived condition within the

triclads which coons, in contrast to freshwater may Tricladida. This implies that under the present

multiply also through fission. According to the phylogenetic hypothesis (Fig. 1) sexual reproduc-

same worker the land planarians usually show a tion in the Maricola, the Terricola, and the Den- sexual mode of reproduction. drocoelidaeis postulated to result from retentionof

For the Maricola indeed I know of no cases in the primitive character state and that the capacity which animals have observed been to use fissioning of fission has evolved independently in several taxa as a mode of reproduction, but for the Terricola within the Tricladida.

Graff (1912—1917) already mentioned a few excep- tions to therule. According to this worker, success-

in ful cases of fissioning were observed specimens 5. Yolk globules of Dolichoplana, Pelmatoplana sondaica, and

Bipalium kewense. Recently, Makino & Shirasawa According to Gremigni (1979) the proposed rela-

(1986) reported that asexual reproduction occurs tionships between the three paludicolan families also in B. nobile and B. but that fis- multilineatum, (see Fig. 1) is supported by an ultrastructural char- sion is absent in B. Ball viz. the absence of fuscatum. (pers. comm.) acter, presence or autosynthetic observed fission in a species of Microplana. yolk globules in the oocytes. In the Dugesiidae the

Evidence is now accumulating from which it be- oocytes contain yolk globules which are widespread

clear within comes that the Paludicola fission is re- throughout the ooplasm and which are synthesized stricted the Planariidae and to the Dugesiidae and within the cells, whereas such structures are absent that it does not occur in the Dendrocoelidae in the Dendrocoelidae and Planariidae. In the two

Calow & An last-mentioned families the contain dif- (Beveridge, 1982; Read, 1986). excep- oocytes a tion may be formed by Dendrocoelum lacteum for ferent type of inclusion, viz. cortical granules which which Berninger (1911) reported to have observed are located in a monolayer in the cortical ooplasm.

which fissioning, contrasts with information However, a proper interpretation of the phylo- provided by more recent publications (cf. Ball & genetic significance of autosynthetic yolk globules

Reynoldson, 1981). within the Tricladida appears not to be feasible at

Evaluation of the character state distributions of the moment. Apart from problems related to the as- sexual and asexual reproduction within the scope of sessment of homology (cf. Tyler, 1981; Gremigni, the present study is dependent on which state is 1981) there is as yet not enough information about postulated to be primitive for the Seriata or the the distribution of the character states within and

asexual outside Tricladida. Tricladida. According to one hypothesis of the With respect to these yolk

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globules and cortical granules nothing is known 7. Adhesive papillae

about the Terricola, and the few results obtained

for the Maricola are difficultto interpret. Gremigni In the phylogenetic hypothesis formulated in this

& Nigro (1983)reported on the presence of autosyn- paper presence or absence of adhesive papillae (Fig.

which in thetic yolk globules in the maricolan Cercyra hasta- 1, characters 13 and 14) are arranged an

function fea- ta but the oocytes of the marinetriclads Procerodes annular zone, as important defining

lobata and P. dohrni contained cortical granules tures for the appropriate taxa (see above). In previ-

(Gremigni & Nigro, 1982; Gremigni et al., 1986). ous, ultrastructural studies the finding of adhesive

Maricola Autosynthetic production of yolk is a primitive papillae in a single member of the was

character within the Platyhelminthes but before it consideredto be representative for the Tricladida as

can be concluded that the Planariidaeand the Den- a whole (Tyler, 1976; Rieger & Tyler, 1979; Ehlers,

drocoelidae are characterized by the derived ab- 1985). Nevertheless, it was already known to Graff

that sence of yolk globules, i.e. the presence of cortical (1912-1917: 2729, 2770, 2773 ff.) Haft-

in conclusion granules, more information is needed about the papillen are absent the Terricola, a

which able confirm from character state distributions not only in the Marico- I am to my own ex-

la but also in the Terricola and the Proseriata. It ap- perience. Moreover, my studies showed that adhe-

in Paludicola. pears that the oocytes of at least some Otoplanids sive papillae are also absent the

also lack yolk globules (Sopott-Ehlers, 1986). The However, the distribution of the character states is

such that number of further dis- data available at present (cf. Gremigni et al., 1986) a species require

within cussion. point to many cases of parallelism the Neoo-

phora. In Pentacoelum punctatum and P. fucoideum

adhesive papillae are confined to the very hind end

adhesive is of the body, the annular zone absent (cf.

6. Cocoon shell globules Sluys & Bush, 1988). It is here postulated that in

these species restriction of adhesive papillae to the

Ehlers (1985: 130-132) suggested that the Tricladi- tail is a case of reduction of the annular zone of

shell da may be characterized by cocoon globules Haftpapillen. That P. punctatum and P. fucoide-

which are differentfrom those in other taxa of the um are members of the monophylum Maricola is

Neoophora. As a consequence, this differenttype supported by the fact that the species show the of cocoon shell globules could be used as an apo- defining features of a less inclusive group of mari-

morphy for the triclads. However, Ehlers (1985) colans, viz. the family Bdellouridae. also that much information In number of other maricolan pointed out more was a supposedly spe- needed about taxa within the Tricladida and the cies reduction has been restricted to the Haft-

Proseriata. In a more recent publication it was indi- papillen and does not involve the annular zone as cated should be used such. This in there that the presumed apomorphy means that these species is a mar- at a higher levelof universality because cocoon shell ginal adhesive zone but that the secretion of adhe- globules may have a similar structure not only in sive glands is not discharged via specialized Haft- triclads but also in the proseriates, while the Pro- papillen but through the epidermal cells, as is the

and Rhabdocoela have in lecithophora differently case the Paludicolaand the Terricola. Examples structured globules (Sopott-Ehlers & Ehlers, 1986). of such species are Procerodes kerguelenensis, Ne-

Globules in which shell substances are deposited in sion arcticum, Dinizia divae, D. sanctaehelenae, a bowl-shaped, meandering pattern may represent Jugatovaria spinosa, Tryssosoma jennyae, Puiteca an apomorphic characteristic for the Seriata (see rigida. Instead of postulating that in these species

Sopott-Ehlers, 1986; Sopott-Ehlers & Ehlers, absence of Haftpapillen is the result of loss within

1986). the lineage of the Maricola, which has occurred in-

dependently of the loss of adhesive papillae in the

Terricola and the Paludicola, there is of course

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another way of explaining the data, and that is that 8. Rhabdites

these particular species are postulated to be mem-

bers of the Paludicola. This would indeed remove The importance of the lack of lamellated rhabdites

several cases of parallelism from the phylogenetic as a derived feature of the Proseriata diminishes

tree (Fig. 1), but at the same time it introducesother considerably when it is realized that only very few

cases. For example, the above-mentioned species triclads have been examined with respect to this

lack the probursal conditionand also the outer lon- character. But even the few studies that have been

gitudinal muscle layer in the subepidermal muscula- published already witness considerable hetero-

ture,and spermatophores have never been observed geneity within the Tricladida. Lamellatedrhabdites

in these animals. Moreover, some of these species, have been found in the freshwater triclads Procoty-

such as Dinizia divae, and Nesion arcticum, have lafluviatilis (Dendrocoelidae) and Phagocata para-

eyes with well-developed lenses. Lensed eyes do not vitta (Planariidae) but appeared to be absent in

members of and in the occur in the Paludicola and Terricola but they are other the Dugesiidae only

known from quite a few maricolans. Thus, with memberof the Terricolathat has been studied with

the above-mentioned which this character references respect to planarians respect to (for see Ehlers,

are devoid of adhesive papillae it is postulated that 1985: 57). If loss of lamellatedrhabdites is thought

they belong to the Maricola (1) because that to represent an apomorphy for the Proseriata then

of this hypothesis gives a most parsimonious explanation two ways are open to explain the presence

of the data and because of the of rhabdite in the Planariidae and Dendro- set, (2) some species type

feature which is characteristic for less in- coelidae. It be that either the possess a a may hypothesized (1)

clusive group of marine triclads. common ancestor of the Terricola and the Paludi-

It is interesting to note that also in some proseri- cola lost this feature and that it re-appeared again

in ates loss of Haftpapillen has occurred, viz. Bothrio- the Planariidae and Dendrocoelidae or (2) that plana semperi and Otomesostoma auditivum; the the Terricola and the Dugesiidae independently lost

latter lacks adhesive the lamellated of rhabdite. the even glands (Hofsten, 1907). type Actually, expla-

According to Hofsten (1907) the last-mentioned nation of the absence or presence of lamellated

species would have no use for adhesive glands and rhabdites in the Tricladida may even require more

Haftpapillen because it lives in the mud of fresh- than two ad hoc hypotheses, depending upon the

water bodies, in contrast to its marine relatives character state to be found in the Maricola, which

which need adhesive in order a strong system to sur- remains to be studied with respect to this feature.

vive in the surf-beaten zone. A similar explanation There is also another way of explaining the distri-

could easily be adopted to account for the absence bution of the character state 'absence of lamellated

of Haftpapillen in B. semperi because this species rhabdites' within the Seriata. And that is that loss

also is confined to fresh waters. Since bothDinizia of lamellatedrhabdites is thought to be theresult of

sanctaehelenaeand Tryssosoma jennyae have been a genetic potential inheritedfrom an ancestor com-

described from the fresh waters of St. Helena (Ball, mon to both the Proseriata and the Tricladida. The

the for the loss of this of 1977d) same hypothesis seems to explain satis- genetic basis particular type

the absence of in these rhabdite is in all the descen- factorily Haftpapillen spe- only potentially present

cies. Adaptive explanations of this kind are bur- denttaxa but it is not expressed in every memberof

dened with theoretical and practical problems, the resultant taxonomic groups. In this view ab-

which need not concern us here. But it is clear that sence of lamellated rhabdites is not seen as an

the adaptive hypothesis fails to account for the ab- apomorphy for the Proseriata but is thought to be

of adhesive in in sence papillae planarians living the an underlying synapomorphy (cf. Saether, 1983) as-

intertidal such Procerodes zone, as kerguelenensis, serting the monophyletic status of the Seriata.

and Nesion arcticum.

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9. Taxonomic implications VI. List of species and genera mentioned

Acromyadenium Beauchamp, 1931 Some technical consequences of the present phylo-

Archimonocelis Meixner, 1938 Stein- genetic hypothesis are the following. In 1925 Asilomaria Karling, 1967 bock united the aquatic triclads in the new taxon Baikalobia raddei (Zabusov, 1911) and the basis of the of the Haploneura on position Balliania thetisae Gourbault, 1978

copulatory bursa he coined the new taxon names Bdellasimilis barwicki Richardson, 1968

Ijima Kaburaki, 1916 Retrobursalia and Probursalia for the marine and Bdellocephalabrunnea & Bdellocephalaschneide riKomarek, 1930 freshwater planarians, respectively. In view of the Bdelloura candida (Girard, 1850) phylogenetic hypothesis formulated above and in Bdelloura propinqua Wheeler, 1894

accordance with opinions of previous workers 1890 Bipalium ephippium Loman,

(Marcus, 1963; Holmquist & Karling, 1972; Ball, Bipaliumfuscatum (Stimpson, 1857)

Retrobursalia and Probursalia Bipalium kewense (Mosely, 1878) 1974a), the names Bipalium multilineatum Makino & Shirasawa, 1983 have lost much of their initial usefulness. Since Bothrioplanasemperi Braun, 1881 some definitely probursal triclads (Probursa) as Caspioplanapharyngosa Zabusova, 1951 well with tendencies towards the as planarians Cercyra hastata Schmidt, 1861

probursal condition (e.g. Obrimoposthia ohlini, Cercyra teissieri Steimann, 1930

Cura patagonica (Borelli, 1901) Cercyra hastata) are here postulated to be members Cura pinguis (Weiss, 1909) of the monophyletic group of marine triclads, there Dendrocoelopsis Kenk, 1930 are no compelling reasons to abandon Hallez' old Dendrocoelum album (Steimann, 1910) Maricola and Paludicola. category names Dendrocoelum infernale(Steimann, 1907)

of the A more important consequence present Dendrocoelum lacteum (Müller, 1774)

maculatum 1927 study is that the Haploneura has lost its taxonomic Dendrocoelum Stankovic & Komârek,

Dendrocoelum sanctinaumi (Stankovic & Komarek, 1927) integrity because the category is based on a poly- Dendrocoelum mrazeki (Vejdovsky, 1895) should phyletic group. In principle, category names Dendrocoelum subterraneum (Komarek, 1919)

refer to monophyletic taxa and thereforethere is no Dinizia divae Marcus, 1947

room for the Haploneura. Steinböck's (1925) name Dinizia sanctaehelenae Ball, 1977

Dolichoplana Moseley, 1877 Diploneura still is a valid alternative for Hallez' Dugesia andina (Borelli, 1895) Terricola. Dugesia annandalei (Kaburaki, 1918)

Dugesia batuensis (Ball, 1970)

Dugesia boehmigi (Weiss, 1909)

Dugesia burmaensis (Kaburaki, 1918) V. Epilogue Dugesia gonocephala (Dugès, 1830)

Dugesia graffi (Weiss, 1909)

Dugesia hoernesi (Weiss, 1909) I have attempted to formulatean hypothesis of the Dugesia lugubris (Schmidt, 1861) of the triclads which fits phylogenetic relationships Dugesia nannophallus Ball, 1970

available at For that neumanni best the data set present. pur- Dugesia (Neppi, 1904)

tree has been which Dugesis polychroa (Schmidt, 1861) pose a phylogenetic presented Dugesia seclusa (Beauchamp, 1940) provides the most parsimonious representation of Eviella hynesae Ball, 1977 the character state distributions used in this study. Geoplana nasuta Loman, 1878 the principle of has no bear- However, parsimony Geoplana sieboldi Graff, 1899

ing on the correctness of the end result, it merely Girardia Ball, 1974

Jugatovaria spinosa Sluys & Ball, 1989 enables us to formulatean hypothesis which is most Kenkia Hyman, 1937 is easily subjected to furthertesting. It my hope that Kontikia bulbosa Sluys, 1983 workers with the present study provides future am- Kontikia orana Froehlich, 1955 for either refutation corrobo- ple opportunities or Macrocotyla Hyman, 1956

ration of the proposed phylogenetic tree. Micaplana misae Kato, 1937

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Microplana Vejdovsky, 1890 VII. Acknowledgments

Microplana aberana (Meli, 1904)

Microplana henrici (Bendl, 1909) Literature study and specimen examination at the Department Microplana monacensis (Heinzel, 1929) of Biology, Memorial University of Newfoundland (July-

Microplana purpurea (Bendl, 1909) August 1986) was made possible by grants from the Netherlands Microplana richardi (Bendl, 1909) Organization for Scientific Research (NWO) (grant R87- 204), Microplana scharffi (Graff, 1899) the Dutch Ministry of Education and Science, and the Depart- Microplana terrestris (Müller, 1774) ment of external Affairs of the Government of Canada; Prof. Mitchellia sarawakana Kawakatsu & Chapman, 1983 Dr. Ian R. Ball and the staff of the Department of Biology at Neppia schubarti (Marcus, 1946) for their MUN are thanked putting facilities at my disposal. Nesion arcticum Hyman, 1956 I thank Prof. Dr. l.R. Ball, Drs. U. Ehlers, B. Sopott-Ehlers, Oahuhawaiiana kazukolinda Kawakatsu & Mitchell, 1984 and E.J. de Vries for valuable comments on the manuscript, Obrimoposthia ohlini (Bergendal, 1899) thoughthey cannot be held responsible for obscurities or errors Obrimoposthia wandeli (Hallez, 1906) that remain. Opisthobursa Benazzi, 1972

Oregoniplana opisthoporaHolmquist & Karling, 1972

Otomesostoma auditivum (Plessis, 1874) VIII. References Pacifides psammophilus Holmquist & Karling, 1972

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