Larval Development and Metamorphosis in Pleurobranchaea maculata, With a Review of Development in the Notaspidea (Opisthobranchia)
GLENYS D. GIBSON Department of Biology, Acadia University, Wolfville, Nova Scotia, Canada B4P 2R6
Abstract. Pleurobranchaea maculata is a carnivorous notaspidean that iscommon in New Zealand. This species produces small eggs (diameter 100 m) and planktotrophic veligers that hatch in 8 d and are planktonic for 3 weeks before settling on bioﬁlmed surfaces (14 °C). Larval development is known in detail for only two other notaspidean species, P. japonica and Berthellina citrina. In all three species of pleurobranchids, mantle and shell growth show striking differencesfrom veligers of other opisthobranch taxa. In young veligers of pleurobranchids, the shell is overgrown by the mantle, new shell is added by cells other than those of the mantle fold, and an operculum does not form. Thus some “adult” traits (e.g., notum differentiation, mechanism of shell growth, lack of operculum) are expressed early in larval development. This suggests that apomorphiescharacteristic of adult pleurobranchids evolved through heterochrony, with expression in larvae of traits typical of adults of other clades. The protoconch is dissolved post-settlement and not cast off as occurs in other opisthobranch orders, indicating that shell loss is apomorphic. P. maculata veligers are atypical of opisthobranchs in having a ﬁeld of highly folded cells on the lower velar surface, amouth that is posterior to the metatroch, and a richly glandular, possibly chemodefensive mantle. These data indicate that notaspidean larvae are highly derived in terms of the novel traits and the timing of morphogenic events. Phylogenetic analysis must consider embryological origins before assuming homology, as morphological similarities (e.g., shell loss) may have developed through distinctmechanisms.
Introduction The Notaspidea is a small, specialized order of opisthobranchs that are considered to be phylogenetically intermediate between the highly derived Nudibranchia and the more basal Cephalaspidea (Schmekel, 1985; Willan, 1987; Mikkelsen, 1998) or monophyletic with the Nudibranchia to form the Nudipleura (Wagele and Willan, 2000). Compar¨ ative embryological studies of theNotaspidea are therefore signiﬁcant for phylogenetic analyses but also for understanding morphological evolution in the Opisthobranchia, a clade rich in homoplastic similarities (Gosliner, 1991, 1994; Mikkelsen, 1998). Unfortunately, little is known about notaspidean development. My goal is to describe larval development in Pleurobranchaea maculata (Quoy and Gaimard, 1832) and to provide a preliminaryanalysis of development in Notaspidea. Adult notaspideans are carnivores and opportunistic scavengers. They are characterized by a single, external ctenidium on the right side, rolled rhinophores, and a ﬂattened shell (Willan, 1983; Schmekel, 1985; Willan, 1987). The order traditionally includes the Umbraculomorpha (families Tylodinidae and Umbraculidae) with large limpetlike external shells and asmall mantle, and the Pleurobranchomorpha (Pleurobranchidae) with a prominent mantle and shells that are internal and reduced or lost in adults (Thompson, 1976; Willan, 1983, 1987). Mantle secretions provide chemical defense in many species, both shelled and shell-less, through the release of acid (Thompson and Slinn, 1959; Thompson, 1988), secondary metabolites (Ciavatta et al., 1993, 1995;Spinella et al., 1997), or dietary alkaloids (Ebel et al., 1999). On the basis of adult anatomy, some investigators suggest that the Notaspidea are polyphyletic (Schmekel, 1985), while others argue that they are
Received 27 August 2002; accepted 23 June 2003. E-mail: firstname.lastname@example.org
G. D. GIBSON
paraphyletic and require inclusion of the Nudibranchia (Wagele and Willan,...