Morphology of the Turbellaria at the ultrastructural level

Reinhard M. Rieger
Dept. o/Zoology, Univ. o/North Carolina at Chapel Hill, Wilson Hall 046 A. Chapel Hill. NC 27514, U.S.A.

Keywords: Turbellaria, morphology, ultrastructure, body wall, nervous system, protonephridia, paren-
chyma, digestive system, reproductive system

Abstract

The paper reviews the following systems: body wall, nervous system, protonephridia, parenchyma,
digestive system, reproductive system, and includes a summary of the literature. New information is
presented for the catenulid and neoophoran body wall-construction, the kalyptorhynch proboscis, the
catenulid and haplopharyngid proto nephridial construction, and the prolecithophoran spermatozoon and
female germ cell. Examples of new features, as well as examples of how electron microscopy has clarified the
relative position of structures and their substructures are given from the subcellular level to the organization
of whole organs. Fine structural features linking different turbellarian orders are summarized. They
apparently support Karling's (1974) latest assessment of the affinities between the turbellarian orders which is
based primarily on light histological data, they add the recognition of a special link between the
Macrostomida and Haplopharyngida and they suggest the existence of three main evolutionary lines within
the Turbellaria.

Introduction (Eakin 1962; Ktimmel 1962; Reisinger & Kelbetz

Over 270 papers on various aspects of turbella-
rian fine structure have been published since the
first published electron micrograph of turbellarian
tissue, namely that of a planarian eye by Wolken
(1958). The vast majority of these papers have used
transmission electron microscopy. Only recently
has scanning electron microscopy been applied
increasingly to the Turbellaria (e.g. Reuter 1978;
Smales & Blankespoor 1978; Williams 1978). The
order Tricladida figured greatly in the early phase
of Turbellarian fine structural research (e.g., Klima
1959, 1961; Pedersen 1959a, b, 1961a; Skaer 1961)
but the interest soon expanded to include other
orders, especially the Acoela (e.g. Pedersen 1964;
Dorey 1965; Klima 1967). The turbellarian photo-
receptor, cyrtocyte, rhabdite and spermatozoon
became the first ultrastructural features used for
investigating various systematic relationships
1964; Hendelberg 1965). Although fine structural
information was used early in combination with
light microscopy for a species description (Reisinger
1968), it is only recently that this approach has been
used more frequently (e.g. Sterrer & Rieger 1974;
Rieger & Sterrer 1975; Crezee 1975; Crezee & Tyler
1976; Lanfranchi 1978). Today about one third of
the ultrastructural information deals with some
aspect ofthe body wall, about one fifth with gametes
and another fifth with regeneration. The last sub-
ject and related aspects have been excluded from
this present review, since they are summarized by
Gremigni (1981). Relatively little is still known
about the comparative fine structure of the intes-
tine, the parenchyma and especially about the
gonoducts and associated structures.
A complete listing of ultrastructural literature
was not intended in this paper, but the given
references should provide a first summary of the

Hydrobiologia 84,213-229 (1981). 0018-8158/81/0843-0213/$03.40.

©Dr W. Junk Publishers, The Hague.
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available literature. In several instances a new
synthesis of the data is presented to stimulate the
search for further ultrastructural information.
Finally, an attempt is made to relate our present
knowledge of turbellarian ultrastructure to the
understanding of turbellarian systematics as re-
vealed by the light microscope.
Body wall
The fine structure of the epidermis was the
subject of one of the first truly comparative ultra-
structural investigations of free-living flatworms by
Bedini & Papi (1974). Twenty-three species of ten
different families and eight different orders have
been studied by these authors. From these data and
various subsequent studies on turbellarian ultra-
structure, four basic types of epidermis can be
discerned (Figs. 1-4).
The first type can be called the neoophoran
epidermis because it is characteristic for all neo-
ophoran orders (Lecithoepitheliata, Prolecitho-
phora, Proseriata, Tricladida, Rhabdocoela) and
the Polycladida (Fig. 4). The main characteristic
feature of this type of epidermal organization is the
presence of a well-developed basement membrane
(see Bowen & Ryder 1974; Hori 1979) with a 20-40
nm thick limiting layer of granular fibrous appear-
ance at the epidermal base and a microfibrillar layer
of varying thickness (0.2-4 Mm).l Often additional
extracellular materials are deposited between basal
foldings of the epidermis and the outer limiting
layer of the basement membrane (e.g. coagulated
fluid in Gieysztoria and Dalyellia, see Bedini &
Papi 1974; electron-lucent zone in Dugesiajapo-
nica, see Hori 1979).
The microfilaments in the deeper layer average
80-120 nm in diameter; they are most likely col-
lagenous in chemical composition and they may
exhibit complex three dimensional arrangements
(e.g. twisted fiber orientations, Fig. 6, see Bouligand
1972, for discussion). With some exceptions (e.g.
Florianella bipolaris, see Rieger & Sterrer 1975) the
microfibrillar layer lacks an inner limiting layer
towards the body wall musculature; instead the

2 3 4

Fig. 14. Diagrammatic representation of different types of the body wall in Turbellaria as seen in longitudinal sections; rostral end of
animal towards left side of Figure. Diagonal muscle system not considered (1) the catenulid type (2) the acoel-nemertodermatid type (3)
the macrostomid-haplopharyngid type (4) the neoophoran-polyclad type. Cell junctions (zonulae adherentes, septate junctions) are
indicated between epidermal cells only. Septate junctions are not illustrated in (2), since septa. if present, are often indistinct (Bedini &
Papi 1974; Tyler & Rieger 1977). Terminal web and basement membrane are illustrated in relative thickness between the types. Small
circles next to ciliary rootlets represent ultrarhabdites. Cell body below muscle layers symbolize sunken epidermal cells, which are seen
most commonly in Acoela. The neoophoran-polyclad epidermal cells are shown partly in a transition towards a syncytium, which is
common in several lines of the neoophorans.