Frontal glands and frontal sensory structures in the Macrostomida (Turbellaria)

Zoologica Scripta, Vol. 16, No. 2, pp. 95-110, 1987 Printed in Great Britain

0300-3256187 $3 .OO + .OO Pcrgamon Journals Ltd.

The Norwcgian Academy of Science and Letters

Frontal glands and frontal sensory structures in the Macrostomida (Turbellaria)

MARIANNE. D. KLAUSER and SETH TYLER

Accepted 10 June1986

Klauser. M. D. &Tyler, S . 1987. Frontal glands and frontal sensory structures in the Macrostomida (Turbellaria).-Zool. Scr. 16: 95-110.

The ultrastructure of the frontal gland complex o f six species o f Macrostomida is investigated. In all species it comprises an array o f discretely emerging gland nccks of at least two gland types, including one with rhammite secretion granule$ and one with rhabdite granules. Moreover, mucous glands and glands containing other secretion granules arc found in Microstomum SP. No intermeditate form which wou\d allow hridging o f thc present \ack of u\trastructural, histochemical and positional similarities between the Macrostomida and the Acoeln is found in the examined species. Therefore, the probability of homology between the frontal organs o f the Acoela and the frontal glands of the Macrostomida remains low. Even though two o r three tyes of sensory receptors are found distributed over the anterior end of all examined species, the frontal gland complex does not appear to be sensory. Because of the uniformity in frontal gland ultrastructure. relationships within the Macrostomida bascd on this character alone cannot bc detected.

Marianne D . Klauser, Department o /Zoology , Spuulding Lifc S(~iencc. Building, University of New Hampshire, Durham, N H 0.3824, U.S.A. Seth Tyler, Department of Zoology, Murruy f la l l , C‘niversity of Maine, Orono, M E 0446Yv U.S. A.

Introduction

A complex of glands and sensory receptors variously known as ‘frontal organ’, ‘frontal glands’ or ‘frontal gland complex’ is of widespread occurrence among taxa of Platyhelminthes (Luther 1905, 1947; Karling 1940, 1974; Ax 1961; Ehlers 1984,1985,1986). The taxonomic distribution of this complex, in fact, led Ehlers (1985, 1986) to propose that its existence distinguishes the major part of the Platyhelminthes from the single taxon Catenulida, and he has erected the taxon Euplatyhelminthes using the character ‘presence of frontal organ’ as an autapomorphy.

However, in comparing the morphology of this gland complex in representatives of the order Acoela with that of a representative of the order Macrostomida (specifi- cally, the genus Macrostomum), it has been concluded that frontal glands are not homologous in the two orders (Klauser et al. 1986). The frontal organ typical of the Acoela is a relatively large set of mucoid glands opening through the exact apical terminus of the body, the frontal pore; in Macrostomum, there are no mucoid glands in such a position and instead rhammite, rhabdite and mucoid glands open separately in a broad band across the anterior tip of the body. Whether the form of these glands in Macrostomum is representative of the order as a whole, or of the Rhabditophora in general, is unresolved.

To discover whether other members of the Macro- stomida possess different arrangements of frontal glands that could be regarded as intermediate between those of Acoela and those of Macrostomum, supporting homology of these otherwise very different forms, we have studied the ultrastructure of the frontal region in six other species of Macrostomida. Together with Macrostomum, these

species represent three family level taxa of the order Macrostomidae, Microstomidae, Dolichomacro- stomidae, and two genera (Myozona and Myomacro- stornum) having no clear affinities with any existing families (and which are best considered representatives of as yet undefined families; R. M. Rieger, personal com- munication).

Frontal glands of turbellarians of the order Macro- stomida tend to be organized into a characteristic arrangement, the so-called ‘Stabchenstrasse’ (Luther 1905,1947; Karling 1940; Hyman 1951; Rieger 1971; Klauser et al. 1986) (Fig. 36). ‘Stabchenstrassen’ consist of adrenal rhammite glands whose cell bodies may either lie dorsally on both sides and posterior to the pharynx or they may be located caudal to the brain (Luther 1905; Rieger 1971). In either case, their gland necks converge just posterior to the brain and then either pass straight through the brain, as in the Dolichomacrostomidae and Macrostomidae, or bypass it ventrally, as in the Microstomidae (Rieger 1971). Anterior to the brain the gland necks separate again, forming four distinctive bundles (Luther 1905) which continue rostrally. These bundles, in turn, may further divide and the gland necks fan out as they extend towards the anterior end of the animal, where they open subterminally.

Rhammites are rhabdoid secretion granules; they are 4-30 p m long, slender, rod-shaped granules with pointed ends. They may either be straight, slightly curved or hook-shaped, and they usually occur in groups of four to seven, rarely individually (Luther 1905, 1940; Reisinger & Kelbetz 1964). The ultrastructure of rhammites is known only for Macrostomum sp. I11 (Klauser etal. 1986).

A second type of rhabdoid gland, the rhabdite glands,

95 Zoologica Scripta 16

96 Marianne D. Klauser and S . Tyler

also open at the anterior end of the body in Macrostomida. These glands may either be epidermal, having their gland cell bodies wedged in between the cells of the epidermis, or they may be adenal, with cell bodies located in the parenchyma (Hyman 1951; Reisinger & Kelbetz 1964). Rhabdite glands also occur in other areas of the body wall.

In this study we mapped the distribution of all components of the anterior end of six species of Macrostomida, showing all gland neck openings, sensory receptors and epidermal cells. In addition, the ultrastructure of rhammites and rhabdites was compared to determine whether these two types of secretion granules can be considered homologous.

Material and methods

The species studied wcre collected in Maine, North Carolina and Bermuda. A MgClz-anesthesia-decantation technique was used to extract the animals from the sediment (Hulings & Gray 1974). Animals were fixed in either of two fixation procedures (Table I). Fixation (a) consisted of phosphate-buffered 4 % glutaraldehyde and 1% formal- dehyde (“Trump’s”); fixation (b) contained 2.5% glutaraldehyde in 0.1 M phosphate buffer with 10% sucrose and 0.05% CaC1, added. All specimens were post-fixed in Os04, dehydrated in an ethanol series and embedded in an Epon-Araldite mixture. Serial thin sections for T E M were stained with uranyl acetate and lead citrate.

Micrographs of cross-sections were used to reconstruct planar projec- tions of the arrangement of gland necks, epidermal cells and sensory structures of the anterior end. Frontal views in a chosen frontal plane were also reconstructed from cross-sections and some representative frontal sections. Total body length of MgCI,-relaxed, fixed and plastic embedded animals was considered 100 units (U), with the anterior tip of the body being 0 U. Then any structure within the animal can be localized as a proportion of the total body length.

Results

tors were found in Microstomum sp., Paromalostomum coronum, Myomacrostomum bichaeta and Myozona sp.

Type I sensory receptors consisted of a single cilium which was free standing above the epidermis, its basal body at the level of the surface of the epidermis and a long single striated rootlet extending straight into the sensory cell (Fig. 17). Sensory receptors of this type rarely occurred individually; usually they were clustered (e.g. in Myom. bichaeta and Paramyozonaria simplex, Figs. 2,4), and in Microstomum sp., Parom. coronum and Macro- stomum hystricinurn marinum they tended to be distributed across the anterior margins of the animals in relatively wide bands. Moreover, type I receptors appeared to be most commonly found in close proximity or even adjacent to gland cells.

Type I1 or collared sensory cells, on the other hand, never occurred in groups. Even where numerous (e.g. in Microstomum sp., Figs. 1, 15), they always were sepa- rated by epidermal or gland cells. The basal part of the cilium in this type emerged from a slight pit at the epidermal surface and the basal body was located below the level of the basal bodies of epidermal cilia. At the epidermal surface the cilium was surrounded by a ring of microvilli (Figs. 18, 19). A mucoid-like network spanned the space between the microvilli and between the microvilli and the central cilium. Below the basal body, a ‘tubular body’ (Tubularkorper; Ehlers & Ehlers 1977) was found (Fig. 20). Collared sensory receptors were never found in close proximity to gland cells. They usually emerged between epidermal cells.

Balloon-like cilia were prominent and numerous at the anterior ends of Microstomurn sp., Parom. coronum, Myom. bichaeta and Myozona sp. (Figs. 1-4, 14). These sensory receptors, situated in a slight pit, consisted of cilia whose cell membranes were distended like a balloon (Fig. 14). The axoneme splayed, its component microtubules following the cell membrane; towards the apex the doub- lets became singlets. A striated rootlet extended proximally into the cell.

Sensory receptors

Three types of monociliated sensory cells were observed in the species investigated. Types I and I1 were found in varying numbers in all species. Balloon-like ciliary recep-

Table I . Material used in the present study. Fixations explained in text

Number of Family Location of specimens

Species collecting site Fixation examined*

Microstornidae

Dolichomacrostornidae Microstomum sp.

Paramyozonaria simplex Rieger & Tyler, 1974

Paromalostomum coronum Spurr, 1983

Macrostomidae Macrostomum hystricinum

rnarinum Rieger, 1977

Reid Marine State Park, Maine, phytal (a) 2

Sand Beach, Mount Desert Island, Maine, (a) 2

Reid Marine State Park, Maine (a) 2

Hulls Cove, Mount Desert Island, Maine, (a) 4

medium sand, between MTL and LTL

LTL(type locality)

poorly sorted sand

Myomacrostomum bichaeta

Myozona sp. t Rieger, 1986t$

Bogue Bank, North Carolina (b) 2

Castle Roads, Bermuda, coarse, coralline (a) 2 fine sand, subtidal from 2 m depth

sand, from 10 m depth ~

* At least one set of cross-sections and one set of frontal sections were used for each species except for Myozona sp., for which two sets of cross-sections were examined. t These two genera show no clear affinities with any of the existing families of the Macrostomida. Myozona, while now classifiede in the Macrostomidae, is an aberrant member of that family (Rieger 1986). Both Myozona and Myomacrostomum may best be considered representatives of as yet undescribed families (R. M. Rieger, pers. commun.). $ Species identified on the basis of the length of its rhammites (see Rieger 1986, p. 43, fig. 5).

Zoologica Scripta 16

Frontal glands in the Macrostomida 97


98 Marianne D. Klauser and S. Tyler

3

Figs. 3-4. Diagrams as in Figs. 1-2.-3. Myozona s p . 4 . Paramyozonaria simplex.



5

Figs. 5 4 . Diagrams as in Figs. 1-2.-5. Parornalostomum c o r o n u m . 4 . Macrostornurn hystricinurn rnarinurn. P glands containing perimaculate granules; A glands containing aster-like granules.



Gland types tron-dense and, except in the case of Mac. hystricinum marinum, the core lamellae were formed (Fig. 28).

(a) Rhammite and rhabdite glands. All of the examined species contained rhabdite and rhammite glands. How- ever, only rhammite glands were involved in the formation of the ‘Stabchenstrasse’ (Figs. 7-13, 16). The gland cell bodies of these rhammite glands were mostly located dorsally, behind and on either side of the pharynx. In Param. simplex though, some of the gland necks extended far back, placing the gland cell bodies in the vicinity of the muscle ring that surrounds the intestine. Also in Parom. coronum, gland cell bodies were found about 350 p m back (i.e. at 77 U) (Fig. 11). In no species were rhammite gland cell bodies found anterior to the brain. From the cell bodies, gland necks extended forward, diverging to open subterminally in a band-like zone across the anterior margins. In Myozona sp. chordoid tissue almost filled the entire anterior end and gland necks were confined to small channels (Fig. 9). In Myom. bichaeta and Parom. coronum there was a distinct separation between dorsal openings of rhabdite glands and a more ventral location for the gland openings of rhammite glands (Figs. 2, 5) . The rhammite glands of Mac. hystricinum marinum opened subterminally in an arc, of which the concavity was towards the ventral side of the animal (Fig. 6). In none of the specimens examined did we observe the convergence and grouping of gland necks as described by light microscopists (Luther 1905, for Macrostoma tuba and M . hystrix; Rieger 1971, for the dolichomacro- stominae).

Rhammites generally were long, slender rods ranging from 4.5 p m (e.g. in Parom. coronum) to 8.5 p m (e.g. in Microstomum sp.). Except for those of Mac. hystricinum marinum, all rhammites had an electron-dense cortex surrounding a lighter core (Figs. 21-25). Two morphologically distinct kinds of rhammites could be identified in Mac. hystricinum marinum : one containing a finely granular matrix (Fig. 27), the other a coarsely granular matrix (Fig. 26). It is possible that these two kinds of rhammites were two forms of the same rhammite type in different stages of secretion.

The cell bodies of the rhabdite glands were located just below the body wall musculature. However, the openings of these glands were not confined to the anterior end; they opened over the entire body, and seemed to be particu- larly concentrated on the dorsal side. In Microstomum sp. no rhabdite glands opened directly at the anterior end (Fig. 1).

Except for those of Mac. hystricinum marinum, all rhabdites had a lamellated core, and they ranged from 1.5 pm (e.g. in Myom. bichaeta) to 4.5 p m (e.g. Micro- stomum sp.) in length (Figs. 30-35). The core in rhabdites of Mac. hystricinum marinum appeared to consist of a finely granular paracrystalline matrix embedded with irregular osmiophilic granules (Fig. 35).

Images considered representative of the formation of rhabdites were observed in Microstomum sp., Param. simplex and Myom. bichaeta. Rhabditogen cells were characterized by an extensive rough endoplasmic reticulum (Fig. 29). Protorhabdites exhibited a striated cortex and a homogeneous central region. What are presumed to be more mature rhabdites were more elec-

Zoologicu S c r i p 16

(b) Other secretions. Both Microstomum sp. and Mac. hystricinum marinum contained anterior mucous glands (Fig. 39). These glands opened at scattered positions on the anterior end of the animals. The gland necks of Microstomum sp. were difficult to follow posteriorly, due to a lack of mucus in them at deeper levels, however, two gland necks in Mac. hystricinum marinum could be fol- lowed posteriorly along the mid-sagittal plane. They diverged just in front of the pharynx (Fig. 12). Other mucous glands only stretched back about 40-50 p m and their cell bodies lay halfway between the anterior edge of the pharynx and the anterior end of the animal.

General body glands with cell bodies wedged in between the cell bodies of epidermal cells were also observed in Microstomum sp. These glands, though, did not open at the immediate anterior end of the animal (Fig. 1). Secretion granules of the general body glands varied from spherical to ellipsoidal in shape and ranged from electron-dense to electron-lucent, sometimes within the same gland (Figs. 37,38).

Glands containing aster-like granules and glands containing what we call perimaculate granules opened within the curvature of the rhammite arc in Mac. hystricinum marinum (Fig. 6). Asters were clumps of small, electron- dense granules aggregated into larger granules (Fig. 40). Perimaculates were ellipsoids whose edges were studded with darker spots (Fig. 41). We did not locate the cell bodies of these two gland types.

Discussion

The ‘Stabchenstrassen’ of the Macrostomida are part of a complex of glands and sensory receptors emergent at the anterior tip of the body. The ‘Stabchenstrassen’ them- selves are rhammite glands opening only in this region of the body, but other components of this anterior complex can be found at other sites in the body as well. Sensory receptors, for example, occur in relatively high density at the anterior tip, but are indistinguishable from sensory receptors in other areas of the epidermis and show no special relationship to rhammite glands. Similarly, rhabdite glands occur among rhammite gland necks and may be at higher density here than at other sites in the body, but otherwise show no special features in the frontal complex. In only some species were other types of glands or sensory receptors, such as mucoid glands and balloon- like receptors, found in the frontal complex.

Therefore, frontal glands of Macrostomida are best distinguished from those of the Aceola by referring to them as ‘frontal complex’ rather than as ‘frontal organ’ (cf. Klose 1984). The latter term is better reserved for the mucoid glands opening at the exact apical pole of the body, the point marked by the convergence of the pattern of epidermal ciliary rootlets (Klauser et al. 1986; Smith & Tyler 1985,1986). There is no consistent gland or receptor type occupying the comparable point in Macrostomida (Figs. 1 4 ) .

14

22

c-------( 20 prn

Fig. 7. Microstornurn sp. Reconstruction of frontal view with representative cross-sections. Numbers to the right of cross-sections indicate distance in pm from the anterior tip. Dotted line indicates interface between epidermal cells and muscle layers. Closed circles, rrn rhammitc glands; open circles, rh rhabdite glands; open triangles, M mucous glands; closed triangles, P glands containing perimaculate granules; closed squares, A glands containing aster-like granules; open squares, hg general body glands; p h pharynx; cf chordoid tissue. The position of the rm gland cell bodies were detcrmincd from LM observations of the block. EM reconstructions were done to the levels indicated by the last serial cross-sections and therefore the absence o f rb glands near the rm cell bodies docs not mean that there are none there.

8 I 10pm

2

16

28

32

- 20 prn

T

Fig. 8. Myomacrostomum bichaeta. Reconstruction as in Fig. I .


4

6

10

13

Fig. 9. Myozona sp. Reconstruction as in Fig. 7.

While the anterior tip of the body in these species of Macrostomida is well endowed with sensory receptors, the ‘Stabchenstrassen’ or other frontal glands cannot be regarded as part of a sensory organ. It must be assumed that the frontal complex is glandular and sensory without those two functions being spatially integrated, as is also true of the frontal organ in the Acoela (Smith & Tyler 1986).

Three types of sensory receptors were found in the frontal complex of these Macrostomida species. Type I sensory receptors, characterized by a long cilium and a long striated rootlet extending proximally into the sensory cell, seem morphologically well adapted to function as mechanoreceptors. The well-developed rootlet in these sensory receptors may serve in anchoring the cilium or in transferring or even registering mechanical displacement. Type I sensory receptors with a similar ultrastructure have been identified in several different turbellarian orders and have been found in almost all areas of the body (Reuter 1975; Bedini el al. 1975).


Embedded sensory receptors like the type I1 receptors in Macrostomida have been compared to receptors responsible for the discharge of cnidarian nematocysts, which are known to have a mechanoreceptive function (Westfall 1970). Similarly, these sensory receptors bear a resemblance to mechanoreceptors in the acoustic and lateral line systems of vertebrates (Flock et al. 1965). These sensory cells consist of one or more cilia surrounded by a ring of stereocilia. This led Ehlers & Ehlers (1977) to conclude that turbellarian type I1 receptors have the same function. However, it seems that a chemosensory function may be just as likely. These sensory receptors have relatively more apical membrane area than the other sensory receptors, because of their sunken position and presence of microvilli around the cilium. This increased membrane area could be related to membrane-associated receptors. In addition, the filamentous strands spanning from the microvilli to the central cilium may aid in trapping molecules.

As Ehlers & Ehlers (1977) correctly pointed out,


Fig. 10. Pararnyozonaria simplex. Reconstruction as in Fig. 7 .

homology of collared sensory receptors among turbellarians does not imply homology to type I1 sensory receptors in other phyla. Therefore, any extrapolative comparisons, even functional ones, to other groups such as the Cnidaria have to be regarded as inferential at best.

Sensory cells with balloon-like cilia have been described in several turbellarians and have been associated with a chemoreceptive function (Kde & Breschiani 1973; Reu- ter 1975; Palmberg 1980). This conclusion is based on the host specificity of the larva of Kronborgia amphipodicola, which possesses only balloon-like cilia on its anterior end. According to KOie & Breschiani (1973), balloon-like cilia are responsible for the specificity of host selection of this larva. Balloon-like cilia have also been described for the acoel turbellarian Diopisthoporus gymnopharyngeus, and Smith &Tyler (1985) consider them to be photoreceptors.

The rhabdites of the six investigated species fulfill the

definition of Smith et al. (1982) for true rhabdites. Of the three rhabdite types identified (Smith et al. 1982), two were represented among the examined animals: The lamellated type was found in Microstomum sp., the dolichomacrostomids, Myom. bichaeta and Myozona sp., whereas Mac. hystricinum marinum possessed Macro- stomum-type rhabdites. Based on criteria of common position, similar fine structure and mode of formation, these rhabdites have to be considered homologous structures.

Similarly, rhammites also fit the definition of a rhabdite of Smith et al. (1982), if the assumption that the darker cortex corresponds to one cortical lamella is made. Rham- mite formation in Myom. bichaeta also occurred within a microtubular sheath and the rhammites of Mac. hystricinum marinum were shown to stain with iron hematox- ylin and fast green (Klose 1984; Klauser et al. 1986). In

Zoologica Scripta I6


11

Fig. 11. Paromalostomum coronum. Reconstruction as in Fig. 7.

addition, rhammite glands occur in fairly well defined and constant positions. Because of the similarities in the mode of formation, the histochemistry and the positions, rhammites are considered a special type of rhabdite.

We consider rhammites to be elongated, straight or slightly curved secretion granules with an electron-dense cortex surrounding a dense, homogeneous core. They are always located in adenal gland cells whose cell bodies are located posterior to the brain and whose gland necks extend anteriorly, protruding between epidermal cells and opening mostly subterminally. Because of similarities in position and substructure, it is highly likely that the rhammites of all Macrostomida are homologous.

Homology of rhammites logically implies homology of all ‘Stabchenstrassen’ in Macrostomida, and possibly also of the rhammite tracts found in Rhabdocoela. Among the Macrostomida ‘Stabchenstrassen’ consist only of rhammite glands, which are always found in the same positions.


1

3.5

z5

No rhabdite glands should be included in the definition of the ‘Stabchenstrasse’, because rhabdite glands are not confined to the anterior end of the animals but generally are found on other parts of the body as well (Hyman 1951; Reisinger & Kelbetz 1964; Martin 1978). Using LM infor- mation on rhabdocoel rhammite tracts (von Graff 1904- 1908; Luther 1904; Hyman 1951), combined with the ultrastructural results on the Macrostomida, one might expect ‘Stabchenstrassen’ of all Rhabditophora to be homologous. However, this claim needs to be substan- tiated by electron microscopic studies on other turbellarians possessing rhabdite and rhammite glands.

Frontal glands and frontal organs of the order Acoela have often been equated with frontal glands of the Mac- rostomida (Hyman 1951; Ax 1961; Karling 1974; Ehlers 1985, 1986). However, an ultrastructural and histochemical comparison of frontal glands in two species of Macro- stomida and Convoluta sp. showed that no homology


Fig. 12. Macrostomum hystricinum marinum. Reconstruction as in Fig. 7.

exists (Klauser et al. 1986); in as much as all other species of Macrostomida studied here have a frontal complex quite similar to that of Macrostomum, none showing similarities with the Acoela, the probability of homology of the frontal organ in Acoela and the frontal gland complex in Macrostomida remains low. The acoel frontal organ has to be regarded as a separate, specialized structure secreting alcian blue-positive mucus (Smith & Tyler 1986; Klauser et al. 1986). Similarly, the ‘Stabchenstras- sen’ of the Macrostomida as defined here are a separate entity with only a few ultrastructural or positional similarities to the acoel frontal organ. The only acoel known so far not to have a true frontal organ is Paratomella sp. (Klose 1984; Smith & Tyler 1986). Instead, three different types of frontal glands open in a scattered fashion across the anterior end of the animal, much as in the Macrostomida. According to Klose (1984), however, the secretions of Paratomella sp. are unlike the secretions in Macrostomida, because they do not stain with fast green. Klose (1984) and Smith & Tyler (1986) see the arrangement in Paratomella sp. as a result of the asexual mode of reproduction in this species.

10pm

If frontal glands of Acoela and Macrostomida are not homologous they are at least analogous, both probably serving to produce mucus for locomotion (Martin 1978) and feeding. An experimental study of the acoel Con- voluta sp. indicates that mucus, such as that produced in the frontal glands, is important for establishing repeatedly used trails, for stabilizing the sediment in which the animals live and for ‘gardening’ food items (Klauser 1986). Rhabdites and rhammites of Macrostomida and other rhabditophorans are also assumed to be mucoid secretions (Hyman 1951; Reisinger & Kelbetz 1964; Martin 1978) and so could play similar roles for these turbellarians.

Frontal glands and other components of the frontal complex are fairly similar among species of Macrostomida and, for the moment, do not provide sufficient character states to elucidate relationships within the order. Differ- ences among species were mainly in cell body positions of rhammite and rhabdite glands, number of gland types and the morphology of secretion granules. On the basis of other characters, any of the non-dolichomacrostomid genera studied could be considered most similar to the


106 Marianne D . Klauser and S . Tyler

Figs. 13-20.-13. Anterior end of Param. simplex. Dark secretion bodies are rhabdites in gland necks.-ll. Anterior end of Myom. bichaeta with type I sensory receptor (arrow) and balloon-like ciliary receptor ( B C ) and epidermal cells.-l5. Anterior end of Microstomum sp. with type I1 sensory receptors (arrows) and ultrarhabdites.-l6. Anterior end of Parom. coronum with rhammite gland neck openings, epidermal cells and ultrarhabdites.--17. Longitudinal section of a type I sensory receptor at the apical surface (arrow) showing basal body (bb) and striated rootlet.-l8-20. Cross-sections of type I1 sensory receptors.--18. Level above the epidermis showing circle of microvilli surrounding a central cilium.-19. At the level of the basal body showing expansion of the microvilli into ridges.-20. At the level of the tubular body (tb) showing microtubules (arrows). ec epidermal cells; ur ultrarhabdites.

Scales: 13-16 2 pm; 17-20 0.5 pm.



Figs. 21-27. Rhammites-21. Cross-section through rhammite of Param. simplex showing distinction between denser cortex and medulla. Scale 100 nm.-22. Longitudinal section through a rhammite of Microstomum sp. Scale 5 pm.-23. Cross-section through a rhammite of Myozona sp. Scale 0.5 pm.-24. Longitudinal section through a rhammite of Myom. bichaeta with denser cortex. Scale 1 pm.-25. Longitudinal section through a Parom. coronum rhammite. Scale 1 pm.-26. Oblique section through a coarsely granular rhammite of Mac. hyslricinum marinurn. Scale 0.5 pm.-27. Oblique section through a finely granular rhammite of Mac. hystricinum marinurn. Scale 0.5 pm.


108 Marianne D. Klauser and S . Tyler

Figs. 28-35. Rhabdites.-28. Rhabdite formation in Microstomum sp. showing an early protorhabdite (below) and a maturing protorhabdite (above). Scale 1 pm.-29. Rhabditogen cell of Param. simplex showing endoplasmic reticulum. Scale 2 pm.-30. Oblique section through a rhabdite of Parom. coronum sp. showing concentric lamellae. Scale 1 pm.-3I. Oblique section through a rhabdite of Myozona sp. showing core lamellae. Scale 0.25 pm.-32. Longitudinal section through a rhabdite of Myom. bichaeta. Scale 1 pm.-33. Longitudinal section through a rhabdite of Param. simplex. Scale 1 pm.-34. Oblique section through a rhabdite of Microstomum sp. Scale 1 pm.-35. Near-longitudinal oblique section through a rhabdite of Mac. hystricinum marinurn. Note absence of central lamellae. This specimen was taken from a laboratory culture of several years of age; cortical lame!lae in rhabdites of freshly collected animals are not as distinct Scale 1 pm.


hypothetical stem species for the Macrostomida: Myomacrostomum for its reproductive system and asexual reproduction (Rieger 1986), Microstomum for its asexual reproduction and pharynx morphology (Doe 1981), Myozona for characters of the adhesive organs (Tyler 1976) and Macrostomum for its similarities with Ax’s earlier hypothetical turbellarian archetype as a whole (Ax 1961). Yet it is difficult to identify any characters in the frontal gland complexes of these genera that could be interpreted as being a more primitive state. These complexes are remarkably uniform in the order.

On the basis of characters discerned at the light micro- scopical level it appears that the frontal gland complex in Macrostomida is comparable to that of members of higher orders, i.e. other members of the Rhabditophora. We expect that the presence of separately opening rhammite and rhabdite glands in the frontal gland complex charac- terizes the Rhabditophora as a whole.

Acknowledgements

We thank D r J . P. S. Smith for his embedded specimens of Myozona sp. and Parornalostornurn coronurn and for his critical review of the manu- script. This study was supported by NSF grants BSR 8116894 and D E B 77-06058 (Seth Tyler, P.1,). This publication is contribution No. 1091 from the Bermuda Biological Station for Research, Inc.

References

Ax, P. 1961. Verwandtschaftsbeziehungen und Phylogenie der Turbel- larim-Ergebn. Biol. 24: 1-68.

Bedini, C . , Ferrero, E. & Lanfranchi, A. 1974. Fine structural observations on the ciliary receptors in the epidermis of three otoplanid species (Turbellaria, Proseriata).-Tissue Cell 7: 253-266.

Doe, D. 1981. Comparative ultrastructure of the pharynx simplex in Turbel1aria.-Zoomorphology 97: 133-193.

Ehlers, U . 1984. Phylogenetisches System der P1athelminthes.-Verh. nuturw. Ver. Hurnb. (NF) 27: 291-294.

Ehlers, U. 1985. Das phylogenetische System der Plathelminthes. G. Fischer, Stuttgart, New York.

Ehlers, U . 1986. Comments on a phylogenetic system of the Platyhel- mint hes.-Hydrohiologia 132: 1-1 2,

Ehlers, U . & Ehlers, B. 1977. Monociliary receptors in interstitial Proseriata and Neorhabdocoela (Turbellaria, Neoophora).- Zoornorphologie 86: 197-222.

Flock, A, , Duval, M. B. & Duval, A. J. 1965. The ultrastructure of the kinocilium of the sensory cells in the inner ear and lateral line organs.-J. Cell Bid . 25: 1-8.

Graff, L. von 19041908. Turbellaria Acoela und Rhabdocoela. In

Klassen und Ordnungen des Thier-Reichs., Vol. 4. (ed. H . G . Bronn); 2032-2048. C. F. Winter’sche Verlagshandlung, Leipzig.

Hulings, N. C. & Gray, J. S. 1974. A manual for the study of meiofauna.--Smithson. Contr. Zool. 78: 1 1-83.

Hyman, L . 1951. The invertebrates, Vol. 2 Plaiyhelminthes and Rhyn- chocoelu. McGraw-Hill, New York.

Karling, T. G. 1940. Zur Morphologie und Systematik der Alloecoela Cumulata und Rhabdocoela Lecithophora.-Acia zool. fenn. 26: 1-260.

Karling, T. G. 1974. On the anatomy and affinities of the turbellarian orders. In: Biology ofthe Turbellaria (eds. N. W. Reise & M. P. Morse): 1-16. McGraw-Hill, New York.

Klauser, M. D . Smith, J. P. S. & Tyler, S. 1986. Ultrastructure of the frontal organ in Convoluta sp. and Macrostomum spp.: significance for models of the turbellarian archetype.-Hydrobiologia 132: 47- 52.

Klauser, M. D . 1986. Mucous secretions of the acoel turbellarian Convoluta sp.: An ecological and functional approach.-J. exp. mar.

Klose, R. 1984. Organogenesis of the frontal gland complex during paratomy in Parutomella sp. (Turbellaria, Acoela.) M.S. Thesis, University of Maine at Orono.

Koie, M. & Breschiani, J . 1973. On the ultrastructure of the larva of Kronborgia arnphipodicola Christensen and Kanneworff, 1964 (Tur- bellaria, Neorhabdocoela) .-Ophelia 12: 17 1-203.

Biol. Ecol. 97: 123-133.

Luther, A. 1904. Die Eumesostomiden.-Z. wiss. Zool. 77: 1-273. Luther, A . 1905. Zur Kenntniss der Gattung Mucro.siomu.-Fesfschr. f.

Palmen, Helsingfors 5: 1-61. Luther, A . 1947. Untersuchungen an rhabdocoelcn Turbellarien. VI.

Macrostomiden aus Finn1and.-Acta zool. fenn. 49: 3-37. Martin, G . G. 1978. A new function of rhabdites: mucus production for

ciliary gliding.-Zoomorphologie 91: 235-248. Palmberg, I . , Reuter. M. & Wikgren. M. 1980. Ultrastructure of

epidermal eyespots of Microsfomum lineare (Turbellaria, Macro- stomida).-Cell Tissue Res. 210: 21-32.

Reisinger, E . & Kelbetz, S. 1964. Feinbau und Entladungsmechanismus der Rhabditen.-Z. wiss. Mikrosk. 65: 472-508.

Reuter, M. 1975. Ultrastructure of the epithelium and the sensory receptors in the body wall, the proboscis and the pharynx of Gyrutrix hermaphroditus (Turbellaria, Rhabdocoela).-Zool. Scr. 4: 191- 204.

Rieger, R . M. 1971. Die Turbellarienfamilie Dolichomacrostomidae Rieger. 11. Teil: Do1ichomacrostominae.-Zoo/. Jb. Syst. 98: 569- 703.

Rieger, R. M. 1986. Asexual reproduction and the turbellarian archetype.-Hydrobiologia 132: 35-45,

Smith, J. P. S. & Tyler, S. 1985. Fine-structure and pylogeny of the frontal organ in Turbellaria Acoela. I . Diopisihoporus gymnopharyngeus sp.n.-Zool. Scr. 14: 91-1U2.

Smith, J. P. S. & Tyler, S. 1986. Frontal organs in the Acoelomorpha (Turbellaria): Ultrastructure and phylogenetic significance.- Hydrobiologia 132: 71-78.

Smith, J . P. S. , Tyler, S . , Thomas, M. B . & Rieger, R. M. 1982. The morphology of turbellarian rhabdites: Phylogenetic implications,- Trans. Am. microsc. Soc. 101: 209-228.

Tyler, S. 1976. Comparative ultrastructure of adhesive systems in the Turbellaria.-Zoomorphologie 84: 1-76.

Westfall. J. 1970. The nematocyte complex in a hydromedusan Gonionemus vertens.-Z. Zellforsch. 110: 457470.


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Frontal glands and frontal sensory structures in the Macrostomida (Turbellaria)