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The anatomy, life habits, and later development of a new species of enteropneust, Harrimania planktophilus (hemichordata: Harrimaniidae) from barkley sound.

Introduction

The deuterostome phylum Hemichordata is composed of three extant classes: the Enteropneusta are solitary worms, the Pterobranchia are colonial tube-dwelling suspension feeders, and the Planktosphaeroidea are known only from their larvae. The enteropneusts and pterobranchs differ sufficiently in size and modes of reproduction and feeding that some investigators have considered the phylum Hemichor-data to be polyphyletic (Jeffries, 1986; Nielsen, 1994). A recent molecular study strongly supports hemichordate monophyly and suggests an entirely new hypothesis for the evolution of the hemichordates (Cameron et al., 2000). That study proposes that the pterobranchs are a sister taxon to the enteropneust family Harrimaniidae, and that this clade is a sister taxon to the enteropneust family Ptychoderidae (i.e., enteropneust paraphyly). If this phylogeny is correct, then detailed studies of the morphology and development of the harrimaniid worms should yield important insights into the biology and evolution of the ance stral hemichordate and the colonial pterobranchs.

Thirteen genera are currently recognized from four families of Enteropneusta: the Ptychoderidae, including the familiar Balanoglossus; the monotypic hydrothermal vent Saxipendiidae (Franzen et al., 1985; Woodwick and Sensenbaugh, 1985); the Spengeliidae; and the Harrimaniidae, including the genera Protoglossus, Saccoglossus, Xenopleura, Stereobalanus, and Harrimania. Harrimaniids are the most morphologically simple of the Enteropneusta; they lack hepatic sacs, synapticles joining adjacent gill bars, and nerve roots extending from the collar cord; about 20 species have been described from the family. To date, developmental observations of the family Harrimaniidae have been restricted to Saccoglossus (Davis, 1908; Burdon-Jones, 1952; Colwin and Colwin, 1953). Saccoglossus pusillus (Davis, 1908) is the only harrimaniid from the West Coast of North America for which developmental information exists.

Ricketts et al. (1985; originally published in 1939) remains the most comprehensive review of the Enteropneusta from the Pacific Coast of North America. The present status of the Enteropneusta from this region is briefly summarized here. From the family Harrimaniidae, Saccoglossus (formerly Dolichoglossus) pusillus (Ritter) (in Davis, 1908; Horst, 1930) is described from San Pedro and San Diego, California. In an earlier work, Ritter (1902) indicates that this same animal is abundant in Puget Sound. Recently, the Saccoglossus from Puget Sound was described by King et al. (1994), who found it conspecific with S. bromophenolosus (formerly identified as S. kowalevskii) from the Northeast Coast of the United States. Two other apparently undescribed species of Saccoglossus occur on the Pacific Coast; one is common subtidally in Barkley Sound, British Columbia (Cameron and Mackie, 1996; Cameron et at., 1999), and the other is from the Santa Maria Basin (Woodwick, 1996). Molecular tools should help us to distinguish the morphologically similar species of this North American genus. Stereobalanus sp. has been discovered from the Santa Maria Basin (Woodwick, 1996), and Harrirnania maculosa (Ritter, 1900) is described from Alaska.

Two undescribed species of Schizocardium (family Spengeliidae) have been found on the coast of California: the first is from Mugu Lagoon (Ricketts et al., 1985) (now a military base) and Newport Bay (Ricketts et al., 1985) (which now has a highly modified and heavily populated shoreline), and the second is from the Santa Maria Basin (Woodwick, 1996). From the family Ptychoderidae, Ritter (1902) mentioned, but did not describe, Balanoglossus occidentalis from San Pedro, California. Other species of Balanoglossus have been collected from the Santa Maria Basin (Woodwick, 1996) and from the northeast coastline of the Sea of Cortez (author's collection). Glossobalanus berkeleyi (Willey, 1931), originally described from Nanaimo, British Columbia, is no longer present in Nanaimo Bay, but is found in Puget Sound, Washington (author's records). Ptychoderidae is the morphologically most complex of the enteropneust families, and the life cycle of its species usually includes a tornaria larva. Two species of tornaria lar vae have been described from western North America (see Ritter and Davis, 1904), but the corresponding adult worms are unknown.

The purpose of the study reported here was to describe Harrimania planktophilus, a newly discovered member of the Harrimaniidae from the West Coast of North America. The description includes--in addition to details of habitat and morphology--observations on the mode of development of H. planktophilus. Features of this development support the recent hypothesis (Cameron et al., 2000) that the Harrimaniid worms are sister taxa to the colonial class Pterobranchia; the evidence also suggests that these taxa evolved from a worm-like ancestor with indirect development. See the appendix for a key to the families and genera of the Enteropneusta and the species of the genus Harrimania.

Materials and Methods

Harrimania planktophilus (Figs. 1 through 5) was collected from the intertidal sand flat at Cape Beale (48[degrees] 47' 30" N, 125[degrees] 12' 56" W) in Barkley Sound, Vancouver Island, Canada. Six worms were collected during February 1997, and another twenty-one were collected over the summer of 1999. All worms were transported to the Bamfield Marine Station, where they were kept in specimen bowls containing their natural sediment under a flow of fresh seawater. One or two worms at a time were removed from their bowls for histology. These animals were allowed to defecate their gut contents, and the external surface was cleaned of sediment. The cleaned worms were relaxed in 7% Mg[Cl.sub.2], then fixed in Bouin's solution, and dehydrated in a graded series of ethanol, Once in 100% ethanol, the animals were dissected into small pieces, transferred to xylene, and infiltrated with paraffin wax. Sections were cut on an American Optical Corporation 820 Spencer microtome, stained with either Delafield's hematoxylin or eriochrome-cyanin, and viewed and photographed with an Olympus OM-4T 35-mm camera mounted on an Olympus BH2 compound microscope.

I was unable to study unfertilized eggs, fertilization, and early cleavage stages preceding the late blastula stage. Blastulae were obtained on 19 February 1997 from a single egg mass maintained in an aquarium; about 70 embryos were in this tubular mass. Twenty of these embryos were removed and reared in finger bowls containing fresh seawater that was changed daily, but mortality was high. Consequently, the remaining 50 embryos were allowed to develop in the jelly mass, in the sediment, but an individual was removed periodically to document development. The temperature of the seawater during the observation period varied between 10 [degrees]C and 11 [degrees]C The various stages were measured, photographed, described, and drawn.

Taxonomic Treatment

Harrimania Ritter 1900

Harrimania Ritter 1900: 112.

TYPE SPECIES: Harrimania maculosa Ritter 1900: 112-115.

Harrimania planktophilus new species

Figs. 1, 2, 3, 4.

Description

External

Harrimania planktophilus is, in general, muscular and active. It is robust and can be collected intact, unlike many other species of enteropneust, which are fragile and easily broken. H. planktophilus (Fig. 1) is small compared with other enteropneusts. The longest individual was 6 cm in length when extended in the bottom of a specimen bowl, and the average specimen was approximately 3.5 cm. The proboscis is conical, is longer than broad, and about twice as long as the collar (Fig. 1, 2). It bears a middorsal groove that extends two-thirds the length of the proboscis from the posterior margin. In some animals, the proboscis skeleton is pigmented black and can easily be seen through the proboscis epithelium. The collar is shorter than it is wide, with a distinctive circumbuccal groove about halfway between anterior lip and posterior marginal ridge. The posterior marginal ridge of the collar is accompanied by a fine crease. Anteriorly the collar lip (see fig. 4, in Cameron, 2002) is muscular and contractile, al tering the circumference and shape of the mouth. An epidermal pit is always present at the dorsal midline where the collar meets the trunk, and its perimeter is rust colored. The trunk can be separated into four regions: a long anterior branchial region; an esophageal region with a reddish esophageal organ; a short transparent region, followed by a darkly pigmented hepatic region (there are no liver sacs); and an intestinal region that has a terminal anus with a sphincter muscle. In gravid males and females the gonads are a pair of large, irregular masses, located dorsolaterally and extending from the posterior pharyngeal region to the anus. The pharyngeal region has many (36.2 [+ or -] SD 9.7; n = 6) pairs of large, muscular gill pores (Figs. 1, 5) that open to the outside in paired dorsolateral grooves. A strong exhalent water current was observed in animals acclimated to cold (5-7 [degrees]C) seawater. Under these conditions, the pores are expanded, and through the pores can be seen the tongue bars in the wall of the pharynx. In about 1 of 10 animals, the skeletal bars are black, rather than the more common collagenous opaque white. The pharyngeal region is 5 times the length of the extended proboscis. The esophageal region has a large bilobed muscular organ that is pigmented dark red, and posterior to this is a darkly stained hepatic region, and then a meandering gut that can be seen through the translucent body wall. The following measurements are from an average adult living specimen: length of proboscis, 2 mm; length of collar, 1 mm; length of pharynx, 9 mm; length of esophagus to anus, 20 mm; total, 32 mm.

Color (Ridgway, 1912): cream-colored proboscis (p1 XVI, f-19); capucine orange collar p1 III, d-13); pale yellow-orange trunk (p1 III, f-15), except for the esophageal organ, which is brick red (p1 XIII, k-5), and the hepatic region, which is brownish olive (p1 XXX, m-19). The eggs are amber yellow (p1 XVI, b-21), and the male gonads are slightly paler.

Anatomical and histological characters

Proboscis. The epithelium of the proboscis is simple and columnar, with multiciliated cells and with glandular cells having basal nuclei. The nervous layer of the ectoderm is about equal in thickness to the underlying circular muscle layer, and thickening slightly under the dorsal proboscis groove. The longitudinal muscle fibers, in transverse section, are arranged in radiating plates, as in Ptychodera and Stereobalanus (Woodwick, 1996); there are fewer than 50 plates, with spaces between them, and they narrow near the center of the proboscis where the coelom is small or absent (Fig. 3A). There is no ventral proboscis mesentery; instead, a plate of connective tissue underlies the ventral stomochord and extends ventrally, nearly halfway to the epidermis, wedging itself between two radial muscle plates. This connective tissue is contiguous with the posterior portion of the proboscis stomochord (Fig. 3G) and becomes continuous with the proboscis skeleton posteriorly. The stomochord, which lacks the vermiform pro cess of Schizocardium (Horst, 1939), is composed of columnar cells arranged radially around a central ciliated lumen, each cell with a large vacuole distally and a proximal nucleus. The ciliated lumen opens into the dorsal midline of the buccal collar, just posterior to the position where the two proboscis skeleton crura bifurcate from the skeletal body. An extensive U-shaped glomerulus is situated on the wall of the heart and at the anterior tip of the stomochord. The pericardium, in transverse section, is a small wedge-shaped sac that extends dorsally from the heart, nearly halfway to the epidermis, between two longitudinal muscle plates (Fig. 3G).

The proboscis coelom is small to absent, is never divided completely, and extends posteriorly on the ventral and dorsal sides of the stomochord. Ventrally the coelom ends in a blind sac; dorsally it extends extremely posteriorly into the stalk and opens to the outside through a single proboscis pore just left of the dorsal midline of the proboscis stalk and almost into the anterior neuropore.

Collar. In some specimens, an anterior neuropore is located at the midline of the proboscis stalk where it meets the collar. A posterior neuropore is always present at the dorsal midline where the collar meets the trunk. Over the length of the collar nerve cord, one or two small lacunae may reside lateral to the midline. Giant nerve cells are absent. A dorsal mesentery is present throughout the length of the collar cord (Fig. 3C). Ventral to the collar cord, the perihaemal coelomic diverticula are well developed and extend from the trunk coelom for two-thirds the length of the collar; the mesentery between the diverticula is well defined. Anteriorly the diverticula become confluent, reduced in size, and enveloped in collagenous tissue that is continuous with the proboscis skeleton. In the collar, the dorsal blood vessel lies in the mesentery formed by the adjacent medial walls of the perihaemal diverticula (Fig. 3C). The collar coelom extends far anteriorly into the proboscis neck (Fig. 3B). Peribuccal spaces are apparently absent. The body of the proboscis skeleton (Fig. 3B) reaches beyond the middle of the collar before bifurcating into two crura that extend into the pharyngeal region. The stomochord consists of two distinct parts. The anterior pouch-shaped part has a central ciliated lumen that opens into the buccal cavity (Fig. 3G), as it does in all Hemichordata. The anterior part is continuous with a posterior gutter-shaped part, which projects posteriorly from the pore of the stomochord lumen, farther along the roof of the buccal cavity, before ending as two open troughs. The stomochord of H. planktophilus is thus similar in design to that of Harrimania maculosa (Ritter, 1900), but not as extensive.

Trunk. Poorly developed parabranchial ridges (Fig. 3D), formed by the ventral edge of the gill bars projecting into the pharynx (see fig. 2 in Cameron, 2002), separate the dorsal branchial pharynx from the ventral digestive pharynx (Fig. 3D). The gill slit skeletal bars are commonly opaque, but in 1 of every 10 animals, they are pigmented black. Peripharyngeal diverticula extend into the tongue bars only. No synapticles join the gill bars with the tongue bars (see figs. 1, 2 in Cameron, 2002). The atrial canal (branchial sac) (Fig. 3D, and see fig. 2 in Cameron, 2002) is U-shaped, heavily ciliated, and leads from the pharyngeal gill slits to the outside via the ciliated gill pore. An epibranchial ridge is absent. Harrimania planktophilus is dioecious. Gonads, which are restricted to the posterior two-thirds of the trunk perivisceral coelom, begin in the pharyngeal region and extend into the intestinal region (Figs. 2, 3D). Gonadal pores occur dorsolaterally. Immediately behind the pharynx, the esophogeal epit helium thickens laterally (Fig. 3E) and forms two opposing lobes, called here the esophageal organ; the lumen is correspondingly reduced in size, as compared with that of the intestine. The intestine meanders en route to the anus; it is lined with a simple epithelium, and hepatic sacs are absent. Two longitudinal muscles are broad and well-developed ventrolaterally, and narrow dorsally (Fig. 3E). Circular muscle is absent in this part of the body. The subepidermal nerve layer is thickened on the dorsal midline and even more so on the ventral midline (Fig. 3F). Thus, the midventral cord may be the main conductive channel in the trunk, as it is in a sympatrically occurring and apparently undescribed Saccoglossus sp. (Cameron and Mackie, 1996).

Diagnosis

The adult animal is distinguished by having a single proboscis pore, a glomerulus that extends frontally over the stomochord (Fig. 3G), and a proboscis skeleton that extends into the pharyngeal trunk. The stomochord begins in the buccal collar as a middorsal ridge; the ridge is maintained on the lateral sides by the proboscis skeletal crura. The opening of the stomochord canal is positioned just posterior to where the two crura meet to form the skeletal body. The collar has a complete dorsal mesentery (Fig. 3C). Animals may have as many as 54 pairs of gill pores. Gonads overlap with only a few of the most posterior gill pores, and the eggs are pigmented yellow.

Development

Embryos were found in aquaria at early blastula to midblastula stage and, therefore, information about gamete structure, egg maturation, events of fertilization, early cleavage stages, and blastulation is lacking. The coeloblastula (Fig. 4A) is 75 [micro]m in diameter and heavily pigmented lemon yellow. It develops in a fertilization membrane 83 [micro]m across that has a thin (1.5 [micro]m) sticky jelly layer, thus development of the animal was often obscured by debris and sand adhering to the jelly coat. Gastrulation appears to proceed by invagination of the posterior (vegetal) pole, resulting in a hemispherical shape that persists for about 12 h (Fig. 4B). The wide archenteron greatly reduces the blastocoel. The blastopore begins to constrict, changing the shape of the gastrula, once again into a sphere (Fig. 4C). Over a period of 24 h the blastopore shrinks, finally persisting as a teardrop shape. There are no external cilia.

The development of cilia initiated rotation within the embryonic chorion 42 h after the embryos were discovered (Fig. 4D). In addition to rotating, the "larvae" propel themselves in the apical direction. A dimple is all that remains of the closed blastopore. The spherical larvae are 72 [micro]m in diameter. A wide telotrochal band forms on the otherwise uniformly ciliated ball; there is no ciliated apical tuft. Elongation by the constriction of a midventral groove is followed by the hatching of a 9O-[micro]m-long, benthic pre-juvenile stage (Fig. 4E). As with the rest of the development, hatching is asynchronous. Of 20 individuals that were extracted from the burrow egg mass and reared in culture, only a single animal hatched. Of about 50 embryos left in the burrow, 14 survived development into juveniles. The fate of the remaining eggs is uncertain, but predation cannot be ruled out because sympatrically occurring species were present in the sediment. Often the jelly layer is shed shortly before the embryo ha tches from the transparent chorion.

Elongation and differentiation of the body into a distinct proboscis, collar, and trunk was complete by day 8 for the remaining few animals in culture (Fig. 4F). The lengths of these body regions were 55.0 [micro]m, 18.5 [micro]m, and 75.0 [micro]m, respectively. The animal could locomote on a plastic dish one body length every 2 s. Forward locomotion is guided by a ciliated muscular proboscis. Posterior locomotion is equally efficient and accomplished by a reversal in ciliary beat. Ciliation is most apparent on the proboscis tip, the collar, and the end of the tail. The pre-oral ciliary organ developed later, after about 12 days. The posterior ventral tail becomes post-anal with the completion of the alimentary canal. The tail extends from the ventral trunk and is heavily ciliated and glandular. The tail can adhere to sediments, plastic, and glass. Like the adults, the juveniles move away from light.

The first pair of gill clefts (perforating the pharyngeal epithelium) and gill pores (perforating the ectoderm) are large and appeared on day 15 (Fig. 4G). The circular clefts are lined with long cilia and lack any sign of a skeleton. When the juvenile is viewed perpendicular to its body axis, ciliary waves are seen to pass in a clockwise direction on the left side of the body and counterclockwise on the right side of the body. In other words, the metachronal ciliary beat, around the rim of each pair of clefts, is in a bilaterally symmetrical pattern. At day 17, the juveniles had a second pair of gill pores and a ventral post-anal tail (Fig. 4I). Eventually a gill skeleton develops around the perimeter of the gill cleft, elongating it into a dorsoventrally elongated gill slit (data not shown).

Biology

Harrimania planktophilus is an active infaunal burrower. Individuals were found in two locations in Barkley Sound, subtidally in the Ross Islets (49[degrees] 52'N, 125[degrees] 10'W) and in the low intertidal of a protected beach adjacent to the eastern slope of Cape Beale (48[degrees] 47' 30" N, 125[degrees] 12' 56" W). At Cape Beale, H. planktophilus was collected at the extreme low tides that occur during the morning hours in spring and summer, and during the evening in fall and winter (Canadian Tidal Tables). H. planktophilus was typically found in a mixture of biogenic calcium carbonate debris and sorted sands with a low concentration of organics. The carbonate fraction of the Cape Beale deposits in the lower tidal range typically contains more than 30% barnacle plates together with fragments of gastropods and, in lower abundance, echinoids, bryozoa, and foraminifera.

H. planktophilus creates sinuous interconnected tunnel systems that do not seem to approach the epibenthos. They are strongly photonegative and lack the odor of bromophenols. In aquaria, more than one animal would frequent a single burrow system. Embryos are deposited in the burrow; the egg mass is cylindrical and has a hollow center, through which adult worms and water currents may pass (Fig. 5). Embryos stick to each other with a thin, sticky jelly coat. The face of the embryonic chorion directed towards the lumen of the burrow is clean, whereas the face directed towards the burrow wall is coated with sediment and detritus.

H. planktophilus ingests sediments that it traps in mucus on its proboscis (Fig. 5) and transports back to the mouth with cilia. It also feeds on organic matter in interstitial pore water, employing its pharyngeal cilia to propel water into its mouth and out of its gill pores (Cameron, 2002). Although debris acquired from pore water may constitute a small amount of the total gut content, it may have a significant nutritional role.

Etymology

The species name is Latin and means "plankton loving," reflecting the animal's ability to suspension feed on plankton in interstitial pore water.

Holotype

Adult female: British Columbia, Vancouver Island, Barkley Sound, Cape Beale protected beach, north side adjacent to the "gap," 48[degrees] 47' 30" N, 125[degrees] 12' 56" W, 20 September 1999, C. B. Cameron.

Sectioned specimen deposited at the Royal British Columbia Museum (RBCM); holotype number 001-00109-001.

Paratypes

Two specimens of undetermined sex deposited at the RBCM; paratype number 001-00109-002.

Evidence the Genus Harrimania is Monophyletic

There are three families of Enteropneusta--four if Saxipendium coronatum, the deep-sea hydrothermal vent enteropneust (Woodwick and Sensenbaugh, 1985), constitutes a family of its own. Harrimania planktophilus belongs to the family Harrimaniidae, of which there are about 20 described species from the genera Saccoglossus, Protoglossus, Stereobalanus, Xenopleura, and Harrimania. Harrimaniids have no liver sacs, no synapticles joining the primary and secondary gill bars, and no nerve roots in the collar cord mesentery. Harrimania is distinguished from Saccoglossus by having a short proboscis (Figs. 1, 2), and from Xenopleura by having large pharyngeal pores (Fig. 1). Harrimania is distinguished from Protoglossus by having a more developed gill skeleton. Harrimania is distinguished from Stereobalanus by lacking a pair of genital wings and gill pores fused to a common dorsal slit (Ritter, 1900).

Two other species of Harrimania are known: H. maculosa (Ritter, 1900) and H. kupfferi (Spengel, 1901, in Horst, 1939); both have, like Stereobalanus, paired proboscis pores. H. maculosa is commonly found intertidally in Alaska at Kodiak, Prince William Sound, Orca, and Valdez. This thick, dark brown acorn worm is about 12 cm long and emits a strong bromophenol odor (Ritter, 1900). It does not burrow as do most enteropneusts, but lies under stones after the fashion of some holothurians. In all of these respects H. maculosa is unlike the species described here, H. planktophilus. Perhaps the most distinctive feature of H. maculosa is its two-part stomochord. H. maculosa always has two proboscis pores, and has an epibranchial ridge (Ritter, 1900).

H. kupfferi is from Scandinavia (Oresund near Hellebaek, Kattegatt, east of Laesso Island) and Greenland (Horst, 1939). H. kupfferi is 8-9 cm long, with a pale-colored proboscis and collar, reddish gonads, and a brown trunk. It differs from H. planktophilus in that its glomerulus halves do not connect frontally. The crura of the proboscis skeleton are not as extensive, extending to the posterior end of the collar, whereas in H. maculosa and H. planktophilus they extend into the trunk. H. kupfferi has no mesentery separating the dorsal and ventral collar coelomic cavities, and the dorsal pharynx, with up to 40 gill pores, is smaller than the ventral pharynx (Horst, 1939). In contrast, the dorsal pharynx of H. planktophilus is larger than the ventral pharynx (Fig. 3D) and has as many as 54 pairs of gill pores.

Phylogenetic Relationships

The presence of a telotrochal swimming band (Fig. 4D) during the development of Harrimania planktophilus suggests that the harrimaniids had an ancestor that developed indirectly. Within the family Harrimaniidae, Harrimania is a sister taxon to Stereobalanus (Reinhard, 1942) a conclusion based on the shared presence of paired protocoel ducts and pores. Molecular sequence data suggest that the harrimaniid worms are more closely related to the colonial class Pterobranchia (including the genera Rhabdopleura and Cephalodiscus), which also have paired protocoel ducts and pores, than they are to the ptychoderid worms (Balanoglossus and Ptychodera) (Cameron et al., 2000). The evolution of the pterobranchs from a harrimaniid ancestor may have involved a reduction in body size and a switch to coloniality. Harrimaniids and pterobranchs, when compared to ptychoderid enteropneusts, show a reduction and disappearance of coelomic diverticula, gonads, and gill slits. The pterobranchs show the most extreme reduction in the si ze and complexity of these structures. The ventral post-anal tail of juvenile H. planktophilus (Fig. 4G-I) may be homologous to the stalk that joins pterobranch zooids. The phylogenetic position (Cameron et al., 2000) and ontogeny of H. planktophilus support the idea that the harrimaniid worms are intermediate in form between a complex and indirectly developing worm-like ancestral body plan, and the simple and directly developing body plan of the colonial class Pterobranchia. See the appendix for a key to the families and genera of the Enteropneusta and the species of the genus Harrimania.
Appendix

Keys to the families and genera of the Enteropneusta, and to the species
of the genus Harrimania


A. Stomochord with a vermiform
 process; pericardium and
 glomerulus with paired anterior
 diverticula more or less developed  Spengeliidae
 (a) Liver sacs and synapticles
   present; gill slits almost
   equaling the pharynx in depth,
   so that the ventral,
   non-pharyngeal part of the
   pharynx is reduced to a mere
   groove; nerve roots absent;
   pericardial diverticula long      Schizocardium, Spengel (1893)
 (b) Liver sacs absent; ventral
   part of pharynx well developed;
   pericardial diverticula short
   (i) Synapticles and nerve
    roots absent,
    (a) Peribuccal spaces            Willeyia, Punnett (1903)
    ([beta]) Without peribuccal
      spaces                         Glandiceps, Spengel (1893)
   (ii) Synapticles present;
     nerve roots present or
     absent; genital region with
     dermal pits                     Spengelia, Willey (1898)
B. Stomochord with no vermiform
 process; pericardium simple;
 ventral part of pharynx large, and
 sometimes more or less separated
 from the branchial part
 (a) Liver sacs, synapticles, and
  nerve roots present                Ptychoderidae
  (i) Genital wings well
   developed
   (a) Atrium opening by long
    slits                            Ptychodera, Eschscholtz (1825)
   ([beta]) Atrium opening by
    small pores                      Balanoglossus, Delle Chiaje (1829)
  (ii) Genital wings hardly
   developed                         Glossobalanus, Spengel (1893)
 (b) Liver sacs, synapticles, and
  nerve roots absent                 Harrimaniidae
  (i) With many atria
   (a) Proboscis long; one
    proboscis pore
    (1) burrowing                    Saccoglossus, Schimkewitsch (1892)
    (2) non-burrowing                Saxipendium, Woodwick & Sensenbaugh
                                      (1985)
   ([beta]) Proboscis short
    (1) one proboscis pore;
     viviparous                      Xenopleura, Gilchrist (1925)
    (2) usually two proboscis
     pores
     (a) Two pairs of genital        Stereobalanus, Spengel (1901)
      wings
     (b) No genital wings            Harrimania, Ritter (1900)
      (I) Proboscis skeleton
       extending into trunk,
       with collar mesenteries
       - Extensive branchial         H. maculosa, Ritter (1900)
         ridge and collar
         stomochord
       - Reduced branchial ridge     H. planktophilus, Cameron
         and reduced collar
         stomochord
      (II) Proboscis skeleton        H. kupfferi, Spengel (1901)
        not extending into trunk,
        without collar mesenteries
  (ii) Without atria                 Protoglossus, Caullery & Mesnil
                                      (1904)


Acknowledgments

Dr. A. R. Palmer provided support (NSERC Operating Grant A7245 [A.R.P.]) for this project. I gratefully acknowledge Dr. A. Martel for providing his microscope, Dr. R. Marx for help with translating the taxonomy text for H. kupfferi, and the staff of the Bamfield Marine Station for providing facilities.

Received 9 November 2000; accepted 23 January 2002.

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Current address: Department of Biology, University of Victoria, Victoria, BC V8W 2Y2, Canada. E-mail: jetsam@uvic.ca
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Author:Cameron, Christopher B.
Publication:The Biological Bulletin
Geographic Code:1CANA
Date:Apr 1, 2002
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