Abstract
BackgroundThe nemertean pilidium is one of the most notable planktotrophic larval types among marine invertebrates. The juvenile forms inside the larva from a series of isolated rudiments, called the imaginal discs. The development culminates in catastrophic metamorphosis, in which the larval body is consumed by the juvenile worm. Although the pilidium was first described in 1847, and is commonly found among marine plankton, there is not a single complete description of its development. The few published studies of pilidial development are based on observations of typically unidentified larvae opportunistically collected from plankton at various developmental stages.ResultsThe development of Micrura alaskensis, a common Northwest Pacific coast intertidal nemertean, is described from fertilization to metamorphosis. A staging scheme is proposed based on characteristic developmental milestones. Three pairs of imaginal discs develop as invaginations of larval epidermis. The cephalic discs invaginate from the larval epidermis above the ciliated band, while the cerebral organ discs and the trunk discs invaginate below the ciliated band. All paired imaginal disc invaginations are closely associated with different portions of the larval ciliated band. In addition, two unpaired rudiments contribute to the juvenile - the proboscis rudiment and the dorsal rudiment, which do not develop as invaginations. A pair of thick-walled esophageal pouches previously thought to represent nephridial rudiments give rise to the juvenile foregut. Branched rudiments of protonephridia, and their efferent ducts are also described. Larval and juvenile serotonergic nervous systems are briefly described. Development of the juvenile is completed by 5-8 weeks at 11-15 degrees C. During the rapid metamorphosis the juvenile emerges from and devours the larva.ConclusionsThis study is the first description of pilidial development from fertilization to metamorphosis in a single species. It is illustrated with photomicrographs of live larvae, diagrams, confocal images, and videos. The findings are discussed in the context of previously published accounts of pilidial development, with which they disagree on several accounts. The results described here indicate a different number, origin and fate of various juvenile rudiments. The proposed staging scheme will be useful in subsequent studies of pilidial development.
Highlights
The nemertean pilidium is one of the most notable planktotrophic larval types among marine invertebrates
This paper describes the development of a typical pilidium larva in M. alaskensis from fertilization to metamorphosis, focussing on the relative timing of developmental events, and the number and origin of the various juvenile rudiments
The present study shows that in M. alaskensis, the appearance of the paired imaginal discs follows the same order: the cephalic discs appear after about one week of development, followed by the trunk discs at two weeks, and the cerebral organ discs at about three weeks of development at ambient sea temperature
Summary
The nemertean pilidium is one of the most notable planktotrophic larval types among marine invertebrates. The development culminates in catastrophic metamorphosis, in which the larval body is consumed by the juvenile worm. The ciliated planktotrophic pilidium larva of nemertean worms (phylum Nemertea) is one of the most characteristic and unmistakable representatives of marine plankton. It is shaped like a helmet and equipped with an apical tuft of long cilia, and, typically, four lobes, spanned by the larval ciliated band [1]. The pilidium larva, first described by Müller in 1847 [2], looks nothing like the juvenile nemertean worm, which Metschnikoff discovered in 1869 [3] develops inside the larva from a series of isolated rudiments called the imaginal discs. The term “metamorphosis” has been applied, in the older literature, to the entire process of development of the juvenile worm inside the pilidium larva, I am using it in a more restrictive sense, referring to the end-point of pilidial development - i.e. the rapid transition between the pilidium and the juvenile
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