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The World of Protozoa, Rotifera, Nematoda and Oligochaeta

[ref. ID; 6565 (Melone, Ricci & Segers, 1998)]

General description of bdelloid trophi

The trophi of Bdelloidea consist of three paired structures. The rami are situated medially and caudally. Because a fulcrum is absent in all Bdelloidea, the incus consists only of the rami. The unci consist of two rows of transversely oriented teeth and are located frontal and lateral to the rami. Lateral to the unci are the manubria. Unci and manubria together from the malleus. The trophi of Philodinida and Adinetida are similar in structure, but those of Philodinavida are different and will be treated separately. The mastax in most Bdelloidea (Philodinida and Adinetida) is located deep inside the body. The orientation of the trophi is oblique, with the unci situated anterodorsally to the rami, which articulate ventrally. When the rotifer body is compressed (e.g., on a microscope slide), the trophi tilt and the articulation between the rami becomes cephalic. The trophi lie perpendicular to the main body axis in Phiodinavida and Flosculariacea, the latter having malleo-ramate trophi. For convenience the trophi of bdelloids are illustrated with the articulation between the rami ventral, in analogy with the trophi of other rotifers. The parts of the trophi will be described with reference to the medial symmetry plane and to the ventral articulatin of the two halves of the trophi, and "proximal" and "distal" refer to the position of the parts relative to the articulation.

Rami

Typically, the rami of Bdelloidea are symmetrical, paired structures oriented along the dorsoventral plane. Both rami are curved, are most strongly reinforced medially, and have convex external margins. All along the inner margin of the rami there is a fringe of minute projections consisting of several superimposed rows of denticules. Each ramus bears a ventrocaudal projection that points medially, here termed the ramus apohysis. This apophysis is separated from, or variably connected to, the ventral end of the ramus. Movement of the rami and the associated unci is obtained by rotation around an axis formed by the ventral points of contact between the rami and their apophyses.

Unci

The unci consist of sheetlike arrangements of a large number of transversely oriented teeth (27-46 in Philodinida and 23-29 in Adinetida). Each tooth consists of a rod-shaped, elongated shaft bearing a lanceolate head pointing medially. The uncus teeth are connected to the rami by ligamentous connections between the distal part of the tooth shaft and the ramus. They are also connected to each other by a variably developed membrane, and, more firmly, to the manubrium. The uncus teeth are differentiated into a proximal group of minor teeth, a median group of major teeth, and a distal group of minor teeth. The number of teeth is generally higher in the distal group than in the proximal group, with the exception of some Habrotrocha species. The number of teeth in the proximal group ranges from 10 to 20 in Philodinida and from 10 to 12 in Adinetida, and in the distal group from 10 to 26 in Philodinida and from 11 to 15 in Adinetida. There is a noticeable difference in the number of teeth in the distal group between the trophi of embryonic (17 teeth) and adult (25-26 teeth) R. rotatoria. The teeth, especially the major ones, are in alternating positions in the left and right uncus plates. All of the minor teeth are more or less straight in frontal view, gradually decreasing in length from medially to both proximally and distally. In frontal view the shaft appears curved and the head is separated and club-shaped. A shaft and head can be recognized in the major teeth as well, and a pore is present at the connection between shaft and head. Occasionally the major teeth can be seen to consist of two fused elements. This is most obvious in embryonic specimens of R. rotatoria. The major teeth are accompanied by a pair of other teeth that are availably fused to them. Apart from the large major teeth, one or more small major teeth may be present in alternating positions proximally or distally in each uncus. The number of major teeth, i.e., two large and ocassionally a small one, is fairly constant throughout the material we were able to examine, except for some Habrotrocha species and Otostephanos species. In the latter, size differences between the major uncus teeth are slight whereas in the other taxa examined they are marked. Because of the presence of a ligamentous connection between the uncus teeth and the medial edges of the rami, the motion of the teeth against the denticulate projections of the rami is restricted to a grinding movement. The unci can rotate around the axis formed by these ligamentous connections.

Manubria

Bdelloid manubria are ribbon-shaped structures that form a rounded external boundary to the uncus plates. They are oriented perpendicular to the plane of the unci. This is not evident in all cases, as the manubria are relatively soft; hence, these structures are easily distorted, becoming folded and (or) broken during preparation of the trophi. They appear to be made up of minute elongate filaments arranged side by side, giving the manubrium a striated appearance. The manubria form a broad joint with the unci and are connected to the tips of the rami.

Structure of the trophi of Philodinavida

The trophi of the three genera deviate from those of other Bdelloidea to a variable extent, with important intergeneric differences. Apart from being situated close to the mouth rather than deep inside the body, the trophi of the different genera present the following peculiarities.

Abrochtha and Philodinavus

The uncus of genera Abrochtha and Philodinavus differs from the semicircular form common to other Bdelloidea. Here, the proximal group of minor uncus teeth is reduced, and the major teeth are situated more ventrally. The reduction is strongest in Philodinavus: its major uncus teeth are the proximal ones and their shafts are bent. The proximal part of the manubrium is reduced to a small projection and, in conjunction with this, the proximal connection between manubrium and ramus is absent. The ramus apophysis is elongate and has an additional articulation point. As a result, the rotation of the rami is no longer around an axis formed by the ventrocaudal projection and the ventral end of the rami, but around an axis formed by the ventral and dorsal processes of the ramus apophysis. Elongation of the ramus apophysis is most pronounced in Abrochtha; the ramus apophysis of Philodinavus is medially concave.

Henoceros

As in the genera Abrochtha and Philodinavus, the uncus of Henoceros deviates from the semicircular form and its ventral part is the most specialized. In addition to the above-mentioned differences, the trophi of Henoceros exhibit further peculiarities: (i) the proximal tip of each ramus bears two recurved, triangular projections. Between these lies the head of the single large major tooth (a single small major tooth is present in either the left or the right uncus). This tooth is provided with a variable number of infra-uncinal teeth; (ii) an articulation is present between the basal part of the major tooth and the anterior part of the manubrium. Here, the manubrium is not ribbon-shaped but rod-shaped. The anterior part of the manubrium is as in Philodinavus; (iii) the ligamentous connection between the distal ends of the manubria and rami is absent. These differences seem to indicate that the manubrium of Henoceros not only provides support for the unci, as in the other bdelloids, but also enhances the movement of the major uncus tooth. Probably the manubrium and the major tooth function like a hammer and chisel, respectively, and produce a stronger force as a result. The development of bifid projections on the ramus near the head of the major uncus tooth, and the absence of the distal connection between the manubria and rami, facilitate movement and thus allow more strength to be exerted.

Morphological variation in bdelloid trophi

Our results confirm that the trophi are fairly homogeneous in structure within the class Bdelloidea (Donner 1965; Markevich 1985). This holds especially for Philodinida and Adinetida, and is surprising considering the differences in corona shape and feeding mode between the two taxa (Melone & Ricci 1995). The trophi of Philodinavida differ noticeably from those of the other Bdelloidea in position, orientation, and structure. In Philodinavida, they are protrusible and situated superficially near the mouth, whereas they are close to the stomach in Philodinida and Adinetida. As for their orientation within the body, the unci are frontal to the rami in Philodinavida but dorsofrontal to the rami in Philodinida and Adinetida. The trophi differ in structure between two groups, and the differences are variably pronounced within Philodinavida. The trophi of Abrochtha most resemble typical ramate trophi, while those of Henoceros are different. In general, the dorsoventral asymmetry of the trophi is more distinct in Philodinavida than in the other Bdelloidea. In the former, the major teeth are ventral, and this accomplished through reduction of the number of minor uncus teeth in the proximal group. In addition, the elongation of the ramus apophyses in Philodinavida enables the rami and unci to be opened wider than in the other Bdelloidea. The presence of protrusible trophi may be connected to a grasping function of the trophi in Philodinavida. This is certainly the case in Abrochtha (Pourriot 1974), but may also apply to Philodinavus. The cooperation between manubrium and major uncus tooth in Henoceros is probably a further specialization for this feeding mode, and appears to be functionally similar to that which occurs in the virgate and forcipate trophi of some evolved Ploimida (Monogononta). Analogous to this, the development of the malleus of Henoceros may be connected to more specialized selection of food items. It is noteworthy that in Adinetida, another group of Bdelloidea that does not filter-feed, the trophi are located deep in the pharynx and are used to masticate the ingested food particles, while a different structure is used of detaching the food particles from the substratum. This structure is called the rake and is specialization of the integument (Donner 1965; Melone & Ricci 1995). The total number of uncus teeth is relatively low in the Adineta species we examined, and this may be a consequence of the small size of their trophi. Among the specimens we observed, strong intraspecific variability in the number of major uncus teeth in present only in Habrotrochidae, although intra- and inter-specific variability is reported for other Philodinida as well (see Donner 1965).

Comparison of the trophi of Bdelloidea and other Rotifera

The ramate trophi of Bdelloidea most closely resemble the malleoramate trophi of Flosculariacea. There are, however, several differences: (i) a fulcrum is present in malleoramate trophi but absent in ramate trophi; (ii) on the proximal inner margin of the rami the denticles are not discernible in malleoramate trophi, but coalesce into intermediate processes. Ramus apophyses are present in both ramate and malleoramate trophi; (iii) in both ramate and malleoramate trophi, the uncus teeth are differentiated. In malleoramate trophi, however, the large teeth are invariably situated proximally, with no small anterior teeth. There is no pore between head and shaft region, and the large teeth are not accompanied by accessory elements; (iv) in malleoramate trophi, the manubria are elongate with a V-shaped cross section, with one part perpendiclar to and other parallel to the axis of the unci; two transverse ridges connect the two parts. The absence of a fulcrum in all Bdelloidea has long been established (de Beauchamp 1965; Norgady et al. 1993), although this was not originally recognized by early authors (de Beauchamp 1909; Remane 1929-1933). Occasionally, recent authors have insisted on attributing a fulcrum to bdelloid trophi (e.g., Koehler and Hayes 1969). A fulcrum is present in all other Rotifera, including Seisonidea (see Segers & Melone 1998). Markevich (1985) and Markevich & Kutikova (1989) state that the absence of a fulcrum is a pelisomorphic feature in Bdelloidea, and that the fulcrum of other Rotifera would be a derivation of the denticules on the inner margin of the rami (the "scleropili" of Markevich & Kutikova 1989). But the fulcrum is an unpaired structure, whereas the scleropili are present on both rami. In addition, those author's hypothesis implies that the fulcrum was formed twice, once in Monogononta and again in Seisonidea. An alternative hypothesis by Segers & Melone (1998), that the fulcrum is part of the original set of elements in rotifer trophi, is more parsimonious and implies that the fulcrum has been lost in Bdelloidea. According to the latter hypothesis, absence of the fulcrum in Bdelloidea is a synapomorphic feature for the group. Differences in ramus structure between Bdelloidea and Flosculariacea are relatively unimportant and appear to be connected to the presence of a fulcrum and large proximal teeth in malleoramate trophi. Indeed, the formation of inter-mediate processes on the rami near the head of the large uncus teeth is similar in the trophi of Flosculariacea and Henoceros. Differences between the large uncus teeth of Flosculariacea and the major uncus teeth of Bdelloidea may be more meaningful. In malleoramate trophi, differences between large and small teeth are more gradual and no structural differences can be found. This is not the case in ramate trophi, as previously described. Whether large or small, the major uncus teeth of Bdelloidea are characterized by the presence of associated elements, and by the pore at the connection between the head and the shaft of the uncus tooth. The function of this pore is not clear, but can be inferred from the ontogeny of the major teeth, as revealed by the trophi of embryonic specimens of R. rotatoria. In frontal view, the shaft of the major teeth consists of two rod-shaped elements that are partly joined medially. Exceptionally, the same can be observed in adult trophi. The merging of these two elements is complete in adult R. rotatoria and adults of other Bdelloidea. This may indicate that the major teeth originate from the merging of two uncus elements. The pores probably act as channels providing space of some filamentous structures interposed between the uncus elements. This structural specialization of the major uncus teeth is synapomorphic to Bdelloidea. The number of uncus teeth is lower in embryonic than in adult specimens of R. rotatoria. The same had already been observed in Rotatoria tardigrada (Ehrenberg) (Markevich 1985). At present we cannot explain this remarkable inconsistency. However, it indicates that small differences in number of uncus teeth are taxonomically irrelevant, while the opposite is true for some Flosculariacea (genus Filinia; see Sanoamuang 1993). Differences in size and robustness of the major uncus teeth among congeneric species seem to be lacking in Bdelloidea but are present in Flosculariacea (Floscularia: Segers 1997; Sinantherina: compare Figs 34 and 36). Another important difference between the trophi of Bdelloidea and Flosculariacea is in their manubria. Whereas the manubria of most bdelloids (except Henoceros) are ribbon-shaped, those of Flosculariacea are more complex and their structural rigidity appears to be greater. On the other hand, the rigidity of the manubria in Bdelloidea seems to be due to the deposition of calcium, as seen by Koehler and Hayes (1969) in Philodina acuticornis odiosa. The same authors (1969) could not detect any calcium deposit on or around the manubria of a monogonont rotifer species, Asplanchna sieboldi. So the rigidity of the supporting elements of the malleus appears to be achieved in different ways by different Rotifera. Manubria are present in both Bdelloidea and Monogononta but absent in Seisonidea (Segers & Melone 1998). Considering the reduction of the malleus in the latter group, it is likely that the absence of manubria in Seisonidea is a secondary loss, and the presence of structure in Bdelloidea and Monogononta is a plesiomorphic feature for these taxa.