Structure and encystment in some fossil cavate dinoflagellate cysts

A study of some peridinioid and gonyaulacoid cavate cysts which develop a dorsal archaeopyle with a double aperture reveals two significant morphological differences. First, the physical separability of the outer and inner body can only be demonstrated in the peridinioid cysts. Second, although the peridinioid double aperture is covered by two opercula, only the inner aperture is operculate in the corresponding gonyaulacoid archaeopyle. These differences reflect two fundamentally different structural and encystment styles. In the peridinioid cysts, the outer and inner bodies are structurally independent and represent the separate development of outer and inner walls. In the gonyaulacoid cysts, the outer and inner bodies are structurally more intimately related, and represent the differentiation of a single wall into outer and inner layers.


INTRODUCTION
Downie & Sarjeant (1 966) introduced the cavate cyst concept to accommodate fossil taxa such as Deflandrea phosphoritica Eisenack (Pl. 1,fig. 5) in which the cyst shows a clear separation into an outer and inner body. Conventional interpretation of this structural arrangement has the outer body formed by the outer cyst wall (periphragm), and the inner body (capsule) formed by the inner cyst wall (endophragrn). The separating space between the outer and inner bodies is termed the pericoel; the encapsulated space is the endocoel.
In terms of thecal affinity, the majority of cavate cysts have apparently been produced by peridinioid and gonyaulacoid dinoflagellates, and the cysts of both thecal groups often appear to be similarly constructed. This similarity is particularly true of some peridinioid taxa of the Deflandrea and Wetzeliella type, and elongate gonyaulacoid taxa such as the genera Tubotuberella Vozzhennikova and Hystrichosphaeropsis Deflandre, and selected species of Gonyaulacysta (Deflandre). However, a study of certain species from these two groups reveals two interesting differences concerning the physical separability of the outer and inner body, and the opercular style of the simple dorsal double-aperture archaeopyle.
The aim of this paper is to describe these differences and discuss their significance in terms of the interpretation of structural and encystment style.
The fossil material illustrated in this paper is housed at two localities, where it is available for examination. In the plate and text-figure explanations, slide numbers prefixed "V" are located in the palaeontological collection of the British Museum (Natural History), London; this material was described in Eaton (1976). Slide numbers prefixed "A" and "S" are located in the palaeontological collection of the Exploration & Production Division, BP Research Centre, Sunbury-on-Thames, Middlesex, England. The co-ordinates following each slide number refer to a reversed 3" x 1" 'England Finder', used with a Leitz Dialux 20 Microscope. Slides were positioned to be read from the right.
The occurence of isolated inner bodies does not require the complete destruction of the outer body. A rich Middle Eocene cyst assemblage from southern England (Sample W40 in Eaton, 1976) yields several inner bodies of Wetzeliella sp. (Pl. 1, fig. 2) as well as their acapsulate outer bodies (Pl. 1, fig. 1). The irregular tear in the latter specimen seems large enough to allow the inner body to be lost. This also suggests that the occurence of acapsulate outer bodies need not always reflect the failure of the inner body to develop. The second illustrated species of Wetzeliella (Pl. 1, fig. 3) is also represented by an acapsulate example. It shows some damage, and therefore its acapsulate state could be either primary or secondary. These observations only serve to confirm how readily the outer and inner cyst body can be separated.
Gonyaulacoid cysts. Late Jurassic, Oxfordian sediments in the North Sea yield particularly rich well-preserved dinoflagellate cyst assemblages. These assemblages are often dominated by gonyaulacoid cavate taxa such as Scriniodinium crystallinum (Deflandre), Gonyaulacysta jurassica (Deflandre) s . l . , and Endoscrinium galeritum (Deflandre) to a degree comparable with peridinioid cavate domination in the Late Cretaceous and Palaeogene. However, despite this cavate dominance, and my deliberate searching, these assemblages have failed to yield any acapsulate examples of gonyaulacoid cavate cyst taxa, or their isolated inner bodies. Furthermore, there are no such records in the palaeontological literature. One form that does require comment here is "Dinoflagellate type 1" of Fenton, Neves & Pie1 (1980) from the Middle Jurassic, which shows some similarity in overall shape to Tubotuberella Vozzhennikova. I have examined the single recorded specimen and I believe its structural affinities are closer to the Chytroeisphaeridia (Sarjeant) cyst type: a simple, single-walled cyst. It may well have been produced by a Tubotuberella-like dinoflagellate, but I do not consider it to represent an acapsulate outer body of Tubotuberella.
It is, of course, possible that this absence of gonyaulacoid acapsulate outer bodies and isolated inner bodies is simply due to the vagaries of palaeontological observation and selective reporting; however, I think this is unlikely. I believe that the absence is a genuine one, and that it reflects a different, more intimate structural relationship between the outer and inner body in gonyaulacoid cavate cysts. As a result, the two bodies are not readily separable.

Explanation of Plate 1
The 'England Finder' co-ordinates follow the slide number.

Eaton
Archaeopyle and opercular style Peridinioid cysts. A characteristic feature of the fossil peridinioid cavate cyst types mentioned in this paper is the development of a simple anterior dorsal archaeopyle involving the displacement of a single apical paraplate, 4' (see Eaton, 1980, p. 675 and fig. 7). An aperture is developed in both the outer and inner body, and both openings (outer, periarchaeopyle; inner, endoarchaeopyle; Lentin & Williams, 1976) are operculate. This is well shown by Dracodinium pachyderma (Caro) (Pl. 1, figs. 8-12; Fig. lA, B). The size relationship between the two openings (and their attendant opercula) is extremely variable. When the depth of pericoel development is limited, and the outer and inner bodies are similar in surface area (as in D . pachyderma), the two operculate openings are similar in size. When the surface area of the outer body is significantly greater than the inner body, then the operculate periarchaeopyle is noticeably larger, as in Chatangiella coronata (McIntyre) in McIntyre (1975, pl. 3, figs. 1-4).
One other significant aspect of this archaeopyle type concerns the planes of the two apertures. In the majority of cases, where the two opercula are separate, the two apertural planes are either parallel, or convergent to beyond the posterior archaeopyle margin. When the two opercula are partially united, as in Deflandrea antarctica Wilson (Wilson, 1967, figs. 23, 24, 26, 27), the two apertural planes converge towards the posterior margin of the archaeopyle.
The development of two operculate openings to form a simple archaeopyle further emphasises the structural independence of the outer and inner cyst walls in these peridiniod cavate cysts.

Gonyaulacoid cysts.
In elongate gonyaulacoid genera such as Gonyaulacysta (Deflandre) and Tubotuberella Vozzhennikova, the archaeopyle is simple, mid-dorsal, and involves the displacement of precingular paraplate 3". Epicystal periocoel development in these genera frequently extends onto the area of 3"; in this case the archaeopyle has a double aperture.
This double aperture is clearly displayed by the specimen of Gonyaulacysta jurmsica in PI. 2, figs. 1-3 and in Fig. 2C. This specimen is exceptional in that the extent of the outer periarchaeopyle can be fully appreciated: it is larger than the inner endoarchaeopyle and its limits are defined by the proximal margin of the parasutural ornament around 3". Also, the two apertural planes are not convergent over the area of 3". This relationship is simply a function of the degree of separation of the outer and inner body in this particular specimen. Separation occurs throughout the area of paraplate 3", and extends posteriorly over and beyond the paracingular zone.
In more typical specimens of G . jurmsica (Pl. 2, figs. 7, 8; Fig. 2B) showing more limited epicystal pericoel development, the two apertural planes converge in the anterior portion of the archaeopyle. Here, only the anterior area of the periarchaeopyle is separated and therefore distinguishable. This more typical relationship between the two openings is often difficult to interpret, and probably for this reason this archaeopyle type has received little attention. In the recent review of Gonyaulucysta and its allies (Sarjeant, 1982), for instance, the archaeopyle in Gonyaulacysta (and Tubotuberella) is described simply as having a "reduced operculum".

Eaton
Turning now to opercular style, it is interesting that G . jurussica does not show evidence of an opercular covering for its periarchaeopyle. This absence has also been reported for Hystrichosphaeropsis quasicribrutu (Wetzel) by Gocht (1976, p. 325) in a paper which also beautifully illustrates the typical archaeopyle style of the elongate gonyaulacoid cyst type (Gocht, 1976, figs. 14a, d). Despite the presence of two archaeopyle apertures, and in contrast to the peridinioid opercular style discussed earlier, there appears to be only a single opercular piece in G. jurassica. In the specimen shown in PI. 2, figs. 7, 8 and Fig. 2B, the single opercular piece has been displaced but is retained within the cyst. It clearly only covers the inner opening. If the absence of an outer operculum is genuine, rather than a function of preservation, then the specimen of G . jurussica in PI. 2, figs. 4, 5 and Fig. 2A is complete. This is despite the presence of a large opening into the pericoel, anterior to the in-place operculum.
Tubotuberella Vozzhennikova, (Pl. 2, figs. 6,9; Fig. 3) has the same archaeopyle and opercular style as G . jurassica, but displays considerably less parasutural ornament. In T . upatela (Cookson & Eisenack) (Fig. 3A) there is no parasutural ornament to define the posterolateral and posterior margins of the periarchaeopyle. In T . rhombiformis Vozzhennikova (Fig. 3B) parasutural crests fully define the lateral margins of the periarchaeopyle, but again there is no definition of its posterior margin. In Tubotuberella then, the periarchaeopyle is not a fully defined opening, and therefore it cannot be covered by a definable operculum.
These observations indicate that no periphragm is developed over the area of paraplate 3" in these particular gonyaulacoid cysts. Summary. The structural relationships around the dorsal archaeopyle in the cyst types discussed above, are summarised in Fig. 4.
In the peridinioid archaeopyle (Fig. 4A), both the peri-and endoarchaeopyle are operculate, with separate or partially united opercula. This emphasises the structural independence of the two cyst walls. The ready separation of the outer and inner body indicates that, in areas away from pericoel development, e.g. posterior to the archaeopyle, the two walls retain their structural independence even where they are in contact with each other.
In Gonyuulacysta jurassica (Fig. 4B), only the endoarchaeopyle is operculate, with the periarchaeopyle developed as a primary, non-operculate opening defined by the proximal margin of the parasutural crests. The lack of evidence for the separability of the outer and inner body in G. jurassica suggests a more complex wall structure than in the peridinioid cyst type. This complexity is perhaps best explained by treating periphragm and endophragm in G. jurussica as differentiated layers of a single cyst wall, rather than different walls. Away from the area of pericoel development the periphragm only expresses its presence through the development of parasutural ornament, and the two wall layers remain partially undifferentiated. This would maintain a more intimate structural relationship between the outer and inner body.

Explanation of Plate 2
All photomicrographs are x 600; the 'England Finder' co-ordinates follow the slide number.    In Tubotuberella (Fig. 4C) the structural relationship is identical to G. jurassica, but there is n o parasutural crest to define the posterior margin of the periarchaeopyle. Consequently, the narrow strip of endophragm immediately posterior to the endoarchaeopyle cannot be distinguished from the combined periphragm and endophragm of the more posterior paracingular zone and beyond.

ENCYSTMENT
On the evidence presented in this paper, particular peridinioid and gonyaulacoid cavate cysts can be divided into a different number of physically separable component parts. These are illustrated in Fig. 5, which also serves to summarise the structural findings of this paper. This difference in structural style must also reflect a difference in encystment style between particular peridinioid and gonyaulacoid dinoflagellates.
The encystment style which produced the peridinioid cavate cyst of Fig. 5 would have been very similar to that described for Recent Peridinium limbatum by Evitt & Wall (1968). After initial contraction of the encysting protoplast away from its thecal covering, the outer body is formed by the secretion of the outer wall. Following further contraction of the protoplast, the inner body is formed by the secretion of the inner wall. Failure to develop the inner body apparently does not affect the outer body, and a non-viable acapsulate cyst is produced. Secondary damage to the outer body of normal cysts can lead to the occurrence of displaced isolated inner bodies.
This encystment style coupled with eventual excystment through a simple dorsal, double aperture, double opercular archaeopyle has a long geological history, ranging through much of the Late Cretaceous and the Palaeogene. It is certainly expressed by fossil peridinioid deflandreacean cysts of the subfamily Wetzelielloideae Vozzhennikova, and the Tribes Deflandreae Bujak & Davies and Chatangielleae Vozzhennikova of the subfamily Deflandreoideae Bujak & Davies (see Bujak & Davies, 1983). With different archaeopyle types, this encystment style has an even longer history, extending to the present day in taxa such as Peridinium limbatum.
The encystment style which produced the gonyaulacoid cavate cyst of Fig. 5 has not been described in Recent dinoflagellates, so the following comments are speculative. Initial contraction of the protoplast is accompanied by the development of the outer body through the secretion of the outer wall layer. This development is selective, and the mid-dorsal precingular area of 3" is not physically expressed leaving a primary opening in the outer body. With further contraction, the areas of the outer wall layer which are not in contact with the protoplast become structurally stable. However, the areas which do retain contact, (essentially equatorial), remain structurally unstable until secretion of the inner wall layer ultimately defines the inner body. Failure to develop the inner body layer prevents the outer body layer from becoming entirely structurally stable, and it eventually disintegrates. This explains the absence of acapsulate outer bodies of gonyaulacoid cavate cysts in the fossil record. The extent of the area of potential instability must show some variation for a given cyst species, and is presumably genetically controlled. If encystment is successfully completed, the outer and Fi inner wall layers co-exist in their areas of contact in a stable intimately related form. The strength of this structural relationship is such that secondary damage does not lead to the occurrence of displaced, isolated inner bodies.
This encystment style coupled with eventual excystment through a simple dorsal, double aperture, single opercular archaeopyle is well represented in the Late Jurassic and Early Cretaceous and can certainly be recognised in the Late Cretaceous and Tertiary. It is best expressed by genera such as Gonyaulacysta, Tubo-4 Structural relationships around the simple dorsal archaeopyle (diagrammatic, not to scale). A. Peridinioid type. B. Gonyaulacysta jurussica. C . Tubotuberella, the dotted line indicates the inferred posterior limit of the narrow strip of discrete endophragm, posterior to the endo-archaeopyle. In the interpretation of wall structure, "p" represents periphragm, and "e" endophragm.

DISCUSSION
Although it would be unrealistic to apply these interpretations of wall structure to all fossil peridinioid and gonyaulacoid cysts, there seems little doubt that they are at least widely applicable. The formal taxonomic groups mentioned in connection with peridinioid encystment style in the previous section of this paper include a large proportion of known fossil peridinioid species. Also, my observations on gonyaulacoid wall structure complement the detailed ultra-thin section studies of Jux (e.g. 1968a, b;1971) on a range of non-cavate gonyaulacoid cyst types: Jux showed that although two layers can be recognised, it is difficult to separate them optically where they are in contact. Again, there is the possibility of a broad taxonomic distribution of this particular wall structural style.
This being the case, these structural interpretations raise some interesting points concerning dinoflagellate cyst morphology in general. For instance, what is the relationship between the walls of peridinioid cysts and the wall layers of gonyaulacoid cysts? Are the two types of wall simply different expressions of the same "doublephase" structure, or is the relationship more complex? Also, have the two structural styles evolved independently, or is one derived from the other; if the latter, then in which direction has evolution taken place?
Throughout this paper I have applied the terms periphragm and endophragm and their derivatives to both peridinioid and gonyaulacoid cysts, mainly for consistency and ease of description. If, however, the peridinioid walls and gonyaulacoid wall layers are not directly related, then there may be a need for a dual terminology. This would certainly go against the recommendations of Cox (1 971), who discussed at length the problems of cyst body structural nomenclature, and advocated a unified terminology.
Finally, is there a direct relationship between wall structural style and morphological potential in dinoflagellate cysts? There is no doubt that cysts of proven or presumed gonyaulacoid affinity show the greater range of morphological and textural variation. Does the close structural relationship of their wall layers provide the basis for greater morphological expression? Peridinioid cysts tend to be morphologically conservative in comparison; much of their variation involves subtle differences in wall texture and degree of wall separation, with the occasional ability to produce variable, multi-walled cysts. This last feature in particular appears to emphasise the structural independence of peridinioid cyst walls, which may have an inhibiting effect on overall morphological expression.
Until there is more detailed information available on wall structure in a greater range of peridinioid and gonyaulacoid cyst taxa, these questions must remain unanswered.