Phylum Nemertea

Chapter 7 Phylum Nemertea Jon L. Norenburg and Stephen A. Strieker INTRODUCTION it appears to be at least paraphyletic, with one or more of its included taxa comprising the most basal clades in Although most zoologists have had little direct experi- a nemertean phylogeny (JLN, unpublished observa- ence with the phylum Nemertea, many are acquainted tions). Thus, the tetm 'palaeonemerteans', from here with the striking image of a fully formed nemertean onward, refers to a presumed paraphyletic assemblage, pilidium larva. Many embryologists know about the rather than a monophyletic taxon. Hoplo- and pilidium larva, thanks to the works of Metschnikoff palaeonemerteans traditionally are regarded as direct {1869), Salensky (1886) and Wilson (1900). However, developers, whereas all heteronemerteans whose life the other planktonic larvae of nemerteans, the so-called cycles have been studied produce a pilidium larva or a direct developers, are very poorly known, although larva that appears to be derived from a pilidium. Jagersten (1972) gave them prominent attention in his Consequently, based on phylogenetic evidence to date, widely cited monograph. the pilidium is most likely to be an apomorphic larval During the last 150 years, various observations about form unique to the Nemertea. Although non-pilidial nemertean planktonic larvae have been made; many of larvae of nemerteans are not known to undergo a radi- these have been compiled in Ftiedrich's (1979) mono- cal metamorphosis, scattered observations (Maslakova graph on nemertean morphogenesis, and they have also and Malakhov, 1999) provide cause to question the been summarized in a review by Cantell (1989). More assertion that all n on-hetero nemerteans are direct recently, the use of modern experimental embryological developers. techniques has resulted in significant advances in our understanding of aspects of larval morphogenesis, espe- REPRODUCTIVE BIOLOGY cially with regard to the early development (Henry and Martindale, 1997a, and references therein). However, Most nemerteans are dioecious, and almost all of the knowledge of nemertean larvae remains relatively rudi- hermaphroditic species occur within the suborder mentary when compared with what is known about Monostilifera of the Hoplonemertea (Friedrich, 1979). larvae in many other groups. Spermatogenesis and oogenesis in nemerteans have been A comprehensive and widely accepted phylogeny addressed recently by Strieker et al. (unpublished obser- of nemerteans is not currently available. However, vations) and Strieker and Folsom (1998), respectively. strong evidence is emerging that the two most spe- Mature oocytes range from 50 pm to 2.5 mm in diame- ciose groups of nemerteans, the orders Hoplonemertea ter (Friedrich, 1979), with approximately commensurate and Heteronemertea, are monophyletic (Sundberg and differences in yolk content (Strieker et al., unpublished Saur, 1998; JLN, unpublished observations). A smaller, observations). Ovaries may possess from one to more third order, the Palaeonemertea (including the than too mature oocytes, which are usually arrested at Cephalothricidae), is traditionally recognized. However, prophase I of meiosis; the number of oocytes varies ATLAS OF MARINE INVERTEBRATE LARVAE Copyright © ZDOZ Academic Press ISBN 0-11-77 3141-j AJ1 rights of reproduction in any form reserved. «>4 Atlas of Marine Invertebrate Larvae within a species-specific range (Friedrich, 1979; Strieker described, although it is thought to close permanendy in et al., unpublished observations). Yolk production hoplonemerteans, and it usually moves inward with for- appears to be mostly by an 'autosynthetic' mode, but mation of the stomodeum in palaeo- and several exceptions are suspected, for example, heteronemerteans (Iwata, 1960a; Friedrich, 1979). The Carcinonemertes epialti {Strieker and Reed, 1981), stomodeum becomes a more anteriorly located imagi- Tubutanus polymorphus (Strieker et al., unpublished nation on the ventral surface of the larva, posterior to observations), and most pelagic nemerteans (Norenburg the brain (Friedrich, 1979; Iwata, 1985). In most and Roc, 1998a) exhibit some exogenous contribution to hoplonemerteans, the stomodeum fuses with the rhyn- yolk synthesis. Both elongate and compact-headed chodeum (proboscis aperture) and comes to lie in front sperm are produced in the phylum, but fertilization of the brain (Friedrich, 1979). The origin of mesoderm mode is not clearly correlated with sperm type {Strieker in nemerteans and whether this varies by species has and Folsom, 1998). been in dispute (Henry and Martindale, 1997a). Most species of nemerteans are oviparous. The mode However, Henry and Martindale (1996) demonstrated of spawning is known for relatively few nemerteans, that larval mesoderm in the pilidium of the heterone- mostly those from littoral habitats. Among littoral mertean C. lacteus is generated both as ectomesoderm forms, spawning ranges from broadcast release of from the 3a and 3b micromeres, and as endomesoderm gametes into the surrounding sea, to pseudocopulation derived from the 4d micro mere. Henry and Martindale with eggs attached in a gelatinous matrix to a benthic (1997a) speculated that adult mesoderm might arise substratum (Riser, 1974; Strieker, 1987). Hetero- from dormant endomesodermal cells. nemerteans known to have planktonic pilidium larvae are broadcast spawners. Conversely, the heterone- LARVAL DEVELOPMENT merteans Lineus ruber and L. viridis pseudocopulate while depositing their eggs in a gelatinous cocoon Nemertean larval development is usually characterized (Riser, 1974), producing pilidium-like encapsulated as direct or indirect, with the latter being synonymized larvae, known as Schmidt's and Desor's larvae, respec- with a pilidium-forming life cycle (cf. Friedrich, 1979). tively (Friedrich, 1979}. A few nemerteans bear living Direct development in nemerteans has been defined as young, and some of these can be considered to obtain "a path of development that leads to the establishment extraembryonic nutrition by viviparity (Norenburg, of the adult body plan (bauplan) without the formation 1986). In contrast to popular belief, vegetative repro- of an intermediate feeding larval stage that possesses a duction by fission is a significant mechanism of distinct body plan" (Henry and Martindale, 1997a). propagation for only a few species in the genus With the exception of the two presumably derived Myoisophagos (including the former Lineus sanguineus, L. forms, noted earlier for L. ruber and L. viridis, all known socialts, and L. vegetus) (Riser, 1974,1994). species with pilidia hatch at, or shortly after, the gastrula stage. Depending on the species, direct developing nemerteans may hatch from the egg capsule beginning EMBRYOGENESIS at the gastrula stage or at stages up to a fully functional, Early embryogenesis and recent experimental studies non-sexual juvenile (Iwata, 1960a; Riser, 1974; Friedrich, are reviewed by Henry and Martindale (1997a). 1979; unpublished observations). Among those hatching Cleavage is spiral, as in other protostomes. However, as pre-crawling juvenile forms, some remain within a the blasromeres of the 4-ceU stage are of equal size and cocoon, as in some supralittoral hoplonemerteans (e.g., lie in a single plane. Thus, a well-defined cross-furrow Pantinonemertes, cf. Norenburg, 1986). The planktonic does not separate opposite blastomeres of the animal larval phase of palaeonemerteans appears to be limited and vegetal poles as in annelids and mollusks (Henry by both yolk reserves and capacity for planktotrophic and Martindale, 1997a). Apparently unique to feeding, whereas planktonic hoplonemertean larvae nemerteans, 4-celI embryos of Cerebratuius lacteus that appear not to feed and are limited by yolk reserves are bisected along the second cleavage plane, thereby (JLN, unpublished observations). At the risk of intro- disrupting established animal-vegetal and dorsoventral ducing new confusion, the elongate planktonic axes, erect novel sets of axial relationships that can, bur pre-adult phase of such 'direct-developing' palaeo- and do not always, generate normal-appearing pilidia hoplonemerteans will herein be referred to as a 'planuli- (Henry and Martindale, 1997b). The blastula is usually form' larva. Dieck (1874) also referred to a a hollow coeloblastula, but may be a solid stereoblastula cephalothricid' larva of this type as a planula. (Friedrich, 1979). During gastrulation, the archenteron If one expands the view of indirect development to is established by invaginarion or polar ingression of cells include non-pilidial forms, there have been several at the vegetal pole. The fate of the blastopore is seldom reports, starting with Dieck (1874), of'direct developers' Phylum Ntmertea 165 that appear to shed or resorb their larval ectoderm. begin feeding until the proboscis is functional, as was Maslakova and Malakhov {1999) describe this phenom- noted by Iwata (1960b), and they may never be enon as development of a 'hidden' larva. These hidden planktotrophic. larvae, as well as pilidia, may in turn correspond with the concept of maximal indirect development proposed LARVAL ANATOMY by Davidson et al. (1995). A fact that is clearly under appreciated in the sec- By about the time of gastrulation, most nemertean ondary literature is that planuliform larvae are actually larvae are fully ciliated. Each cell generally possesses quite common among palaeonemerteans (Figures multiple cilia, but the cilia may be sparsely distributed, 7.1A-C), an observation

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