Lecithotrophic uniformly ciliated pilidia

Initially believed to be the exception, some pilidiophoran species are known to have lecithotrophic development in which the resemblance to the hat-like pilidium is lost and, instead, larvae more closely resemble the vermiform morphology of palaeo- or hoplonemertean larvae. Despite the superficial resemblance, these larvae are modified pilidia. The juvenile develops inside the larval body via imaginal discs and metamorphosis is catastrophic as is seen in other pilidiophoran larvae. Several pilidiophoran species have been shown to have modified development. The larvae of Lineus viridis and Lineus ruber are encapsulated and called Desor’s and Schmidt’s larvae, respectively (Schmidt 1964; Norenburg and Stricker 2002) and Micrura akkeshiensis produces planuliform modified pilidia called Iwata’s larva (Iwata 1958). Several other pilidiophoran species have recently been shown to possess modified development including Micrura rubramaculosa (Schwartz and Norenburg 2005), Micrura verrilli and two undescribed species in the genus Micrura (Schwartz 2009). In 2012, Maslakova and von Dassow described yet another lecithotrophic pilidium larva which they named pilidium neilsoni. These modified larvae differ in the orientation of the juvenile axis with respect to the larval axis and the presence or absence of transverse ciliated bands. Below are three additional pilidiophoran species that produce modified pilidia, all of which have similar morphology but, together with the aforementioned species, suggest that lecithotrophic development may have evolved many times within the Pilidiophora and are no longer necessarily the developmental exception in this clade (see Maslakova and Hiebert 2014).

Generalized modified pilidium where juvenile anterior is pointed downward.

Generalized modified pilidium where juvenile anterior is pointed downward.

The three species whose modified pilidia we've collected from plankton samples in southern Oregon have an apical tuft marking the larval anterior and the juvenile antero-posterior axis is opposite that of the larva (i.e. juvenile posterior is larval anterior). The larvae are uniformly ciliated and the juvenile is sometimes conspicuous within the larval body. There are two more species which we strongly suspect have lecithotrophic development based on oocyte size, but we have yet to observe their development.  

Larva collected in December 2012 where juvenile posterior (note the dark gut) is immediately below the larval anterior (marked with an apical tuft). The juvenile posterior wraps around toward and ends at 8 o'clock (left). Scale bars 100 µm.

Heteronemertea gen. sp. 1

Sequence Data:  16S, COI

Observed in Coos Bay: Feb, Dec

This modified pilidium was collected in December and possessed a blade-like apical tuft but an inconspicuous posterior cirrus. The juvenile axis is opposite of the larval axis and the posterior curved around and toward the juvenile's anterior right side. The larval epidermis was ciliated and decorated or textured with golden lipid droplets. 

Modified pilidium collected in February 2013 shown, note juvenile posterior which projects from left side (left two images). Metamorphosed juvenile from wild-caught larva at left with coiled proboscis and no caudal cirrus (right two images). Scale bars 100 µm. 

Heteronemertea gen. sp. 2

Sequence Data:  16S, COI

Observed in Coos Bay: Jan-Feb

The second species which we've collected as a modified pilidium was collected in winter months. Although the larva shown (above) has a conspicuous apical tuft, we did collect another larva that lacked an apical tuft, which was presumably lost during collection. Upon metamorphosis, the juvenile nemertean ingested its larval body, as is the case for most pilidiophorans, which is the dark mass within the juvenile gut (above right).

This larva was collected in January 2013 and is shown here at two focal places to emphasize, the juvenile coiled inside the larva (left) and the larval ciliated epidermis and apical tuft (right). Scale bars 100 µm.  

Heteronemertea gen. sp. 3

Sequence Data:  16S, COI

Observed in Coos Bay: Jan

The third species who's modified pilidium we observed was collected in January and is indistinguishable from the others. The larva is uniformly ciliated, has a prominent apical tuft and a curled juvenile inside, which is positioned opposite to the larval axis.