Jaw growth and replacement in Ophryotrocha labronica (Polychaeta, Dorvilleidae)
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- Paxton, H. Zoomorphology (2004) 123: 147. doi:10.1007/s00435-004-0097-4
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Ophryotrocha labronica, as typical for Eunicida, has a complex jaw apparatus consisting of ventral mandibles and dorsal maxillae. Mandibles are not replaced but are retained throughout life. Larval mandibles have adult-sized cutting plates but their proximal shafts lengthen and enlarge as the worm grows. The maxillary apparatus of O. labronica undergoes three moults or replacements. The initial, or larval maxillae, consisting of two paired basal plates and two paired free denticles, develop in the unreleased larvae. They are replaced in the 5-setiger juvenile by the P1-maxillae consisting of falcate forceps and six denticles. The second moult occurs in the 8- to 9-setiger juveniles and results in the P2-maxillae with bidentate forceps and seven denticles, and the third and final moult results in the K-maxillae and seven denticles. The K-maxillae develop in 9- to 12-setiger males and 13- to 15-setiger females and are not replaced but enlarge proximally. Thus the K-forceps can be traced back through the P2-forceps, P1-forceps, to the larval basal plates, indicating the apomorphic state of the K-forceps. Three pulp cavities, separated by darker fusion lines are visible in weakly sclerotised young K-forceps suggesting the fusion of three separate elements. It is concluded that the Ophryotrocha forceps are homologous to the superior and probably inferior basal plates of other dorvilleids. The internal structure of the Ophryotrocha forceps demonstrates that they are not homologous to the labidognath maxilla I as has been suggested.
KeywordsEunicidaCtenognathLarval jawsMandiblesMoulting maxillae
As members of the Eunicida, dorvilleids are characterised by having a complex jaw apparatus consisting of ventral mandibles and dorsal maxillae. The jaws of Dorvilleidae are made up of mineralised sclerotised proteins, with the maxillae of the ctenognath type. While the Ctenognatha were diverse during the Palaeozoic and Mesozoic, their only Recent representatives are the Dorvilleidae. Among the eunicidan types of maxillae, it is only in the dorvilleid ctenognath type that jaw replacement can clearly be observed, and has been demonstrated for a number of genera. All Eunicida mandibles, on the other hand, are not replaced but grow during the lifetime of the animal (Paxton 1980, 2000).
The earliest descriptive studies of jaw development of Ophryotrocha species were undertaken more than a century ago. Korschelt (1894) gave well illustrated descriptions of different stages of jaws of Ophryotrocha puerilis Claparède and Mecznikow, 1869. However, it was Bonnier (1893) who recognised that the maxillary apparatus does not grow but undergoes a series of moults and interpreted the occasional presence of a second set of maxillae as the replacement set. Kegel and Pfannenstiel (1983) demonstrated with histological studies that the replacement maxillary elements are formed in epithelial sac-like structures situated ventrolateral to the existing maxillae. The ultrastructure and composition of the jaws of O. puerilis was examined by Damas (1987), and Purschke (1987) studied the dorvilleid pharynx, the growth of the mandibles, and growth and replacement of the maxillary apparatus at the ultrastructural level. He showed that the shape of the maxillary elements is preformed by microvilli carrying cell processes. Although the new maxillary elements start to develop individually, they become connected by thin ligaments to form an interconnected structure. The old maxillae remain functional until the replacement maxillae are fully formed, and are then shed through the mouth or gut.
Ophryotrocha labronica La Greca and Bacci, 1962 is a gonochoristic species. After some courtship, eggs are deposited in a tube-shaped cocoon or egg case, fertilised by pseudocopulation and generally protected by both parents to undergo direct development lasting about a week (Åkesson 1973). The development of the jaw apparatus is precocious, resulting in a fully functional set of jaws even before the larvae are released from the egg case. The complete sequence of jaw development from the larva to the adult has never been clearly documented for this species. The only other description of juvenile jaws of O. labronica was given by Sudzuki and Sekiguchi (1972). The authors reported O. labronica from marine aquaria at Tokyo Kyoiku University where Japanese horse-shoe crabs were cultivated. Although the species is a member of the O. labronica complex, its correct identity cannot be ascertained. Typical Ophryotrocha maxillae consist of eight elements on each side, with seven anterior free denticles, and the two sides of the most posterior element, the ice-tong-shaped forceps, fused caudally in a carrier-like structure. Opinions on the taxonomy of the group are divided, with proponents for two families and several genera (Orensanz 1990) to a single genus (Hilbig and Blake 1991). A recent phylogenetic analysis of all apparently valid genera of Dorvilleidae, Iphitimidae and the jawless Dinophilidae resulted in the single family Dorvilleidae and placed the Ophryotrocha group in a central position in the cladogram with the tetrachotomy Schistomeringos, Dorvillea, Protodorvillea and Meiodorvillea at the ancestral end, and Dinophilus at the derived end (Eibye-Jacobsen and Kristensen 1994).
Opinions on the origin of the forceps have been divided. Jumars (1974) suggested that the forceps are the result of fusion of the carriers and both basal plates. This idea was accepted by Hilbig and Blake (1991), although Eibye-Jacobsen and Kristensen (1994) questioned the involvement of the inferior basal plates, while Orensanz (1990) considered the forceps homologous to the superior basal plates only.
Tzetlin (1980) proposed an evolutionary scheme for the Eunicida maxillary apparatus where the Ophryotrocha P-type, gives rise to two basic lines, one leading to Dorvilleidae (except most Ophryotrocha species) and the other to the Ophryotrocha species with K-type forceps, which leads in turn to the labidognath families. Thus he suggested that the Ophryotrocha forceps are homologous to the forceps-like maxilla I of the Onuphidae, Eunicidae and Lumbrineridae.
The primary aspect of the present study is to document the timing of moulting maxillae from larvae to adults in male and female O. labronica and to provide illustrated descriptions of the various stages of maxillae as well as a growth series of mandibles. Furthermore, it is hoped that the ontogeny of the maxillae will clarify the origin of the Ophryotrocha forceps with respect to their homology to the maxillary elements of other Dorvilleidae and the labidognath Eunicida.
Materials and methods
Specimens of the Naples strain (NI) (Åkesson 1970) of O. labronica were reared in culture. The animals were kept in small glass bowls in local seawater at 21.5°C. Once a week the water was replaced and finely blended spinach was provided as a food source. To examine and draw the jaw apparatus, animals were anaesthetised in 6% magnesium chloride and mounted on a slide with diluted glycerin added to the edge of the coverslip. Drawings of these squash preparations were made with the aid of a camera lucida. The maxillary elements or plates are represented in the drawings in a flattened state as they appeared in squash preparations. They are drawn in a dorsal view, where in a more life-like attitude the serrated cutting edges would be pointed towards the observer. Jaw terminology follows Jumars (1974) and will be discussed below.
Appearance of maxillary apparatus
Type of maxillae
Number and type of paired elements
Stage of worm
Age of worm (at 21.5°C)
1 Superior basal plate
3 days before release
1 Inferior basal plate
2 Finely serrated free denticles
10–12 days after release
3 Coarsely serrated free denticles
3 Finely serrated free denticles
8- to 9-setiger
14–16 days after release
3 Coarsely serrated free denticles
4 Finely serrated free denticles
Forceps (left falcate; right bidentate)
Males 9- to 12-setiger; females 13- to 15-setiger
20–25 days after release
3 Coarsely serrated free denticles
4 Finely serrated free denticles
The maxillary apparatus of O. labronica undergoes three moults or replacements, each resulting in a structurally different set. The initial, or larval maxillae, are replaced by the first postlarval set, here referred to as the P1-maxillae. The second moult results in a second postlarval set, here referred to as the P2-maxillae, which differ in number of elements and shape of the forceps from the P1-type. The third and final moult results in the K-maxillae.
The posterior elements, or basal plates, are of an oblong shape, denticulated on their median edge. The larger element is overlain by a smaller one. The larger basal plate is coarsely denticulated by alternating large and small teeth while the smaller basal plate is uniformly finely denticulated. Anterior to these basal plates are two delicate rounded free denticles, finely serrated along their cutting edge.
The second maxillary moult starts in 8- to 9-setiger worms (Figs. 3B, 4B). The developing maxillae have eight paired elements, consisting of forceps and seven free denticles (Figs. 3D, 4C). This type is here referred to as the P2-maxillae. The forceps are larger than the P1-forceps and posteriorly they are fused into a carrier-like structure. The anterior tips are bidentate with the right forceps finely serrated between the distal fang and the second tooth (Fig. 3E), while the same area in the left forceps is smooth. The shape of the free denticles is the same as in the P1-maxillae, with free denticles 1–3 with a distal fang and a coarsely serrated cutting edge, and the free denticles 4–7 with a finely serrated cutting edge. The duration of the P2 stage is a sexually dimorphic characteristic, lasting longer in females than in males.
The K-maxillae are not moulted anymore. While the anterior elements do not change, the forceps enlarge with age. Figure 5C and D show the maxillae of a female and male, respectively, at the age of 143 days. The female maxillae are less sclerotised and the two sets of fusion lines are still visible (Figs. 4F, 5C). Although their position appears to have shifted with the growth of the forceps, their relative position remains the same as is evident by the attachment of the ligament sheath to the inner side of the forceps at the lower fusion line. The distal enclosed parts of the forceps are of similar size as in the young forceps, but the proximal laterally open parts have enlarged in width and length to some extent in the female and to a much greater extent in the male.
The ultrastructure of mandibles and their growth has been discussed for Ophryotrocha gracilis Huth, 1934 by Purschke (1987). The mandibles of O. labronica are very similar in form and presumably structure. The cutting plates are formed in the larva and remain in their initial size throughout life. The fine teeth of the anterior cutting edge become somewhat worn but appear unrepaired in older animals. The shafts enlarge in length and increase their apophyses for muscle attachment throughout life.
The terminology of the ctenognath maxillary apparatus is still far from resolved. The terms discussed below are those most commonly applied to Dorvilleidae (see Jumars 1974; Oug 1978, Fig. 1a; Orensanz 1990; Eibye-Jacobsen and Kristensen 1994).
The dorsalmost posterior components are the maxillary carriers and may consist of two individual elements, be fused into a V-structure or be absent. The name is unfortunate since it suggests a homology with labidognath and prionognath carriers which is unlikely (see Wolf 1980). Species of Ophryotrocha do not have carriers as such. In this group the two parts of the posterior maxillary element are medially united by a flattened structure, perpendicular to the maxillae, that has been referred to as pseudocarriers (Orensanz 1990) or a carrier-like structure (Purschke 1987).
The basal plates are the posteriormost plates. The larger outer pair is referred to as the superior basal plate. The basal plates are medially denticulated and are thought to consist of a number of fused denticles. The smaller inner pair is finely denticulated and is termed the inferior basal plate. Both basal plates are continued anteriorly by a row of free denticles, the superior and inferior row of free denticles, respectively. The term ‘free denticles’ was considered misleading since the individual denticles are connected by ligaments (Purschke 1987; Orensanz 1990). However, they can be thought of as ‘free’ since they are individual elements, rather than the fused denticles that make up the basal plates. Most species of Ophryotrocha have seven free denticles on each side that seem to lie in one row. There is disagreement as to whether they represent the superior row only (Purschke 1987; Eibye-Jacobsen and Kristensen 1994) or whether denticles 1–3 represent the superior row and denticles 4–7 the inferior row (Orensanz 1990; Hilbig and Blake 1991). The two types of denticle are morphologically very different from each other, and show great similarity with the superior and inferior denticles, respectively, of other genera of Dorvilleidae.
Larval maxillae (Fig. 2) have been reported for several species of Ophryotrocha. Korschelt (1894) showed larval maxillae for O. puerilis that were similar to those of O. labronica reported here but he figured an additional smaller anterior element. Sudzuki and Sekiguchi (1972) mentioned three pairs of elements for their O. ?labronica, with what appears like one posterior oval element and two small anterior elements. The maxillary development of two more species, probably also members of the O. labronica complex, Ophryotrocha schubravyi Tzetlin, 1980 and Ophryotrocha dimorphica Zavarzina and Tzetlin, 1986, were presented with their original descriptions. The authors stated that the elements in the larval maxillae numbered three to four pairs in the unreleased larvae and six pairs in the free 1-setiger juveniles. Thus the number of observed larval elements ranges from three to six pairs. This difference may reflect the difficulty in observing these tiny structures in squash preparations rather than their variability. Purschke (1987), in his light and TEM histological studies of the development of O. gracilis, found the larval maxillae of O. gracilis to consist of four maxillary elements fused with a carrier-like structure, and like O. labronica in the present study, stated that the animals retain this initial maxillary set until they consist of five setigers when the first replacement set starts to develop. Ophryotrocha gracilis and O. labronica are not closely related species and the fact that their larval maxillae are similar and moult at the same size suggests that it is a basic developmental stage.
Juvenile maxillae are smaller and the forceps are of a different shape than in the adult jaw and are referred to as P-type maxillae while the adult forceps are of the K-type. This term was coined by Hartmann and Huth (1936), coming from the German ‘primitiv’ and ‘kompliziert’ (complicated). Among the known species of Ophryotrocha there are some that have only P-maxillae, some where the females have P-maxillae and only the males attain the K-maxillae, and some species where both males and females moult their P-maxillae to the K-type at a certain age or size. The first situation is found in O. gracilis where the maxillae are replaced from time to time and the newly moulted set is always a copy of the old one, i.e. always P-maxillae (Dohle 1967). The best example of the second case is found in the protandric O. puerilis where juveniles undergo several moults resulting in identical P-maxillae. Müller (1962) has shown that individually kept O. puerilis moulted their P-maxillae eight times, with larger intervals as the animals got older. The K-type is formed only when females switch to males. This sexual change is brought about by the presence of other individuals or environmental influences and has been the focus of many studies. The third case is found in O. labronica where at a certain size both males and females attain the K-jaws.
Ophryotrocha labronica has only two sets of P-maxillae and the two are not identical. The P1-maxillae (Figs. 3B, 4B) are not much larger than the larval maxillae and are present only for a short time before the P2-maxillae start to develop in 8- to 9-setiger worms. The same pattern was shown by Tzetlin (1980) and Zavarzina and Tzetlin (1986) for O. schubravyi and O. dimorphica, respectively. While these authors referred to the first postlarval maxillary set appearing in the 5-setiger juveniles as the P-type, Tzetlin (1980) coined the term T (or transitional) type for the second postlarval set developing in the 7-setiger worms. This is a reasonable proposition to distinguish the two types of maxillae. However, it could lead to misunderstandings since the second postlarval maxillae in O. labronica are widely known as P-type in the literature, while the first postlarval maxillae were previously unknown. Therefore, I consider it more prudent to refer to the postlarval maxillae of this group of species as P1- and P2-maxillae or type.
An intriguing question that cannot be answered at the present time is why the K-maxillae do not moult any more. The forceps enlarge posteriorly and become very large and powerful, especially in males. The anterior enclosed part of the forceps (Fig. 5B) remains about the same, while the laterally open posterior part widens and lengthens (Fig. 5D).
Origin of K-forceps
The carriers and superior and inferior basal plates typical of the Dorvilleidae maxillary apparatus are not present in juveniles and adults of Ophryotrocha species. Instead they are replaced by the forceps. However, the four elements of the larval maxillae of O. labronica have here been interpreted as the superior and inferior basal plates, connected by a carrier-like structure. The basal plates are strongly reminiscent of other dorvilleid genera. The median edge of the larger basal plate resembles the multidentate state of the superior basal plate and the smaller element resembles the finely denticulated inferior basal plate of Dorvillea species. The two finely serrated anterior free denticles of the larval maxillae of O. labronica are reminiscent of the inferior free denticles of some dorvilleids.
From the moulting sequence of O. labronica maxillae it is evident that the basal plates of the larval maxillae become replaced by the P1-forceps which become replaced by the P2-forceps, which are finally replaced by the definitive K-forceps. Therefore, the K-forceps can be traced back to the larval basal plates. This indicates that the Ophryotrocha forceps are apomorphic structures, while the basal plates represent the plesiomorphic state. This is in agreement with the phylogenetic analysis by Eibye-Jacobsen and Kristensen (1994) which placed Dorvillea in a basal and Ophryotrocha in a central position in the cladogram. This negates the proposal of Tzetlin (1980) that Ophryotrocha with P-type maxillae were the ancestors of other dorvilleids, for example, Dorvillea.
The darkly sclerotised lines dividing the pulp cavities of the forceps have here been interpreted as fusion lines, indicating the fusion of separate elements. Another possible explanation, that they provide mechanical support, has been rejected, since even the much larger, superficially similar maxillae I of other Eunicida families, such as Onuphidae, do not have such support structures. In the P1- and P2-forceps two weak fusion lines are visible but they are much more apparent in recently moulted K-forceps. Two distinct sets of fusion lines and three openings to internal pulp cavities are visible (Figs. 4D, 5A). Each dorvilleid maxillary element has a pulp consisting of a few cells (Purschke 1987) in a pulp cavity. These multiple pulp cavities in Ophryotrocha forceps have been described in the palaeontological literature for living and extinct species (Szaniawski and Wrona 1987; Eriksson and Lindström 2000). The two sets of fusion lines and three pulp cavities indicate that the forceps are the fusion product of three elements. These three elements could be the superior and inferior basal plates and carriers (Jumars 1974), the superior basal plates and carriers (Eibye-Jacobsen and Kristensen 1994) or only denticles of the superior basal plate as suggested by Orensanz (1990). While the present evidence indicates that the Ophryotrocha forceps are homologous to the superior and probably inferior basal plates of other dorvilleids, it remains unclear whether the carriers are involved or not.
The evolutionary scheme of the Eunicida maxillary apparatus by Tzetlin (1980) has been rejected by Orensanz (1990) on a number of points. Orensanz stated that the forceps of Ophryotrocha are believed to have evolved independently of the maxillae I of several labidognath families and that the superficial similarity is believed to be due to convergence. The present study can clearly support this statement on the basis of the structure of the elements in question. While each side of the Ophryotrocha forceps is a fused structure with three separate pulp cavities, each side of the forceps or maxilla I of the Onuphidae, Eunicidae and Lumbrineridae is a single structure with a single pulp cavity and thus the forceps of Ophryotrocha and labidognath Eunicida are clearly not homologous.
I am indebted to Prof. Bertil Åkesson, Department of Zoology, University of Göteborg, for providing the initial culture specimens and Dr. Alexander B. Tzetlin, Biological Faculty, State University of Moscow, for translations and unpublished information. Many thanks go to Mr. Ron Oldfield, Microscopy Unit, for photography and Ms Lesleyanne Kilkeary for technical assistance. I am grateful to the reviewers for their helpful comments. This is publication number 390 of the Commonwealth Key Centre for Biodiversity and Bioresources, Macquarie University.