Karen J. Osborn

Diversification of acorn worms (Hemichordata, Enteropneusta) revealed in the deep sea

Enteropneusts (phylum Hemichordata), although studied extensively because of their close relationship to chordates, have long been considered shallow-water, burrowing animals. The present paper more than doubles the number of enteropneust species recorded in the deep sea based on high-resolution imaging and sampling with remotely operated vehicles. We provide direct evidence that some enteropneusts are highly mobile—using changes in posture and currents to drift between feeding sites—and are prominent members of deep, epibenthic communities. In addition, we provide ecological information for each species. We also show that despite their great morphological diversity, most deep-living enteropneusts form a single clade (the rediagnosed family Torquaratoridae) on the basis of rDNA sequences and morphology of the proboscis skeleton and stomochord. The phylogenetic position of the torquaratorids indicates that the group, after evolving from near-shore ancestors, radiated extensively in the deep sea.

Description and Relationships of Chaetopterus pugaporcinus, an Unusual Pelagic Polychaete (Annelida, Chaetopteridae)

An extraordinary new species, Chaetopterus pugaporcinus, is described from eight specimens collected from deep mesopelagic waters off Monterey Bay, California, by remotely operated vehicles. All specimens exhibit a consistent combination of both adult and larval characteristics, leaving in question the maturity of the specimens. All specimens lack ciliated larval bands and the stout, modified chaetae (cutting spines) typically found in segment A4 of chaetopterids. If the specimens described here are larvae, they are remarkable for their size, which ranged from 10 to 21 mm total length, nearly twice the length of the largest polychaete larvae previously reported and 5 to 10 times larger than known chaetopterid larvae. Then too, their lack of segment addition prior to settlement would be atypical. If adult, they are particularly unusual in their habitat choice and body form. Morphology of the uncini and comparison to larval morphology indicated a close relationship to either Chaetopterus or Mesochaetopterus. However, the lack of cutting spines and typical adult morphology made it impossible to determine to what genus this species should be allied. Thus, we carried out the first molecular phylogenetic analysis of the Chaetopteridae in order to appropriately place and name the new species. Three partial genes were sequenced for 21 annelid species. The sequencing also provides the first molecular evidence that Chaetopterus variopedatus sensu Hartman (1959) is not a single cosmopolitan species. The question of C. pugaporcinus being a delayed larva or a genuine holopelagic chaetopterid is discussed.

Deep-Sea, Swimming Worms with Luminescent “Bombs”

Several species of deep-sea polychaete worms have been discovered that have a bizarre predator distraction mechanism. By using remotely operated vehicles, we found seven previously unknown species of swimming annelid worms below 1800 meters. Specimens were large and bore a variety of elaborate head appendages. In addition, five species have pairs of ellipsoidal organs homologous to branchiae that produce brilliant green bioluminescence when autotomized. Five genes were used to determine the evolutionary relationships of these worms within Cirratuliformia. These species form a clade within Acrocirridae and were not closely related to either of the two known pelagic cirratuliforms. Thus, this clade represents a third invasion of the pelagic realm from Cirratuliformia. This finding emphasizes the wealth of discoveries to be made in pelagic and deep demersal habitats.

Relationships within the Munnopsidae (Crustacea, Isopoda, Asellota) based on three genes

The Munnopsidae are a diverse group of asellote isopods that are an important component of deep‐sea fauna. Morphologically‐based phylogenetic inference attempts have proven to be of limited use due to the ecological and morphological diversity within the clade. Monophyly of the family is well‐established but relationships within the group remain unresolved. This project is the first molecularly‐based effort focused specifically on resolving phylogenetic relationships within the Munnopsidae. Partial 28S and COI and complete 18S genes were sequenced for 28 asellotes, 15 additional taxa were included from which only one or two of the three target sequences could be obtained, and 18S sequences for five additional taxa were available from GenBank. Sequences were analysed both as individual genes and in combination using Bayesian and maximum parsimony approaches. Each gene provided a phylogenetic signal that could be identified in the combined analyses, with 18S analyses providing the most resolution of phylogenetic relationships. The available representatives of subfamilies Munnopsinae and Ilyarachninae were monophyletic, as was the genus Munneurycope. Relationships within the subfamily Munnopsinae were well‐resolved by thorough taxon sampling, several new species were placed, and the need for taxonomic revision of Munnopsis/Munnopsoides was supported. These analyses supported putative Eurycope paraphyly and emphasized the need for careful revision of this highly variable genus. Tytthocope was sister to Munnopsurus. Syneurycope was suggested as the sister group to the ilyarachnines. Combined analyses provided increased support for clades suggested in at least two individual gene analyses and for clades not strongly contradicted by individual analyses. Further work is required to fully resolve the munnopsid phylogeny and should consist of increased taxon sampling for the complete 18S sequence and possibly identification of at least one slowly evolving, nuclear protein‐coding gene to resolve the basal polytomy and enable placement of the root.

Phylogenetics of Acrocirridae and Flabelligeridae (Cirratuliformia, Annelida)

Osborn, K. J. & Rouse, G. W. (2010). Phylogenetics of Acrocirridae and Flabelligeridae (Cirratuliformia, Annelida). —Zoologica Scripta, 40, 204–219.

Solution to the phylogenetic enigma of Tetraplatia, a worm-shaped cnidarian

Tetraplatia is a genus containing two species of pelagic cnidarians of curious morphology. Their vermiform shape and four swimming flaps are difficult to relate to the features of other cnidarians, thus obscuring their phylogenetic affinities. Since their discovery in the mid-1800s, a number of prominent cnidarian workers have weighed in on this conundrum, some arguing that they are aberrant hydrozoans and others concluding that they are unusual scyphozoans. Current taxonomic practice conforms to the latter view. However, data presented here from the large and small subunits of the nuclear ribosome leave little doubt that Tetraplatia is in fact a hydrozoan genus. Indeed, its precise phylogenetic position is within Narcomedusae, as some authors had previously deduced based on structural characters. The distinctive body plan of Tetraplatia is remarkable because it appears to have a recent origin, in contrast to the prevailing pattern of metazoan history.

Multiple origins of pelagicism within Flabelligeridae (Annelida)

Most pelagic clades are believed to have originated from benthic ancestors and open water habitat is thought to have remained open to invasion throughout evolutionary history (Rigby and Milsom, 1996). Many metazoan lineages contain at least one pelagic example, possibly due to the relative openness of the pelagic habitat. In most cases, the transition from benthic to pelagic habit is assumed to be accompanied by dramatic changes in the morphology and ecology of the animal as seen in the highly modified forms of pelagic species (e.g. Phylliroe, a nudibranch, Tomopteris, a polychaete, Carolinites, a trilobite) and in the varied pelagic larval forms of benthic animals. Broad scope analyses of pelagic invasion and radiation have been made for groups such as Foraminifera (e.g. Darling et al., 1997) and cladoceran (e.g. Sacherová and Hebert, 2003) and copepod (Bradford-Grieve, 2002) crustaceans, but there are few single-lineage examples using extant species. By examining individual invasion events and comparing the changes that occur in those lineages, we can learn about the ‘‘toolbox” they are working with, or the variability possible, and about the evolutionary constraints within the lineage. More importantly, these findings allow us to understand the selective pressures and evolutionary processes at work in the pelagic realm. The majority of polychaetes are thought of as benthic, however, there are many polychaetes that swim periodically, larval and reproductive stages that utilize the water column for a portion of their life history, and several lineages that are holopelagic, or spend their entire lives in the water column (Rouse and Pleijel, 2001). Most holopelagic polychaete taxa belong within Phyllodocida and by the fact of the multiplicity of divergent clades, can be assumed to represent multiple transitions from benthic to pelagic habit (Rouse and Pleijel, 2003; Halanych et al., 2007). Possibly, the highly

Morphology of a new deep‐sea acorn worm (class Enteropneusta, phylum Hemichordata): A part‐time demersal drifter with externalized ovaries

Ten individuals of an enteropneust in the family Torquaratoridae were videotaped between 2,900 and 3,500 m in the Eastern Pacific—one drifting a few centimeters above the bottom, two exposed on the substrate, and seven partly burrowed, reflecting a bentho‐pelagic life style. Here, we describe a captured specimen (26 cm living length) as the holotype of Allapasus aurantiacus n. gen., n. sp. The small proboscis is dome‐shaped, and the collar is only slightly wider than deep; both of these body regions are more muscular than in other torquaratorids, which presumably facilitates burrowing. The proboscis complex, in contrast to that of shallow‐living enteropneusts, lacks a pericardial sac and is located relatively posteriorly in the proboscis stalk. The stomochord is separated from the main course of the gut by the intervention of a small, plate‐like proboscis skeleton lacking posterior horns. The most anterior region of the trunk houses the pharynx, in which the pharyngeal skeletal bars are not connected by synapticles. The postpharyngeal trunk comprises three intestinal regions: prehepatic, hepatic (with conspicuous sacculations), and posthepatic. On either side of the worm, a flap of body wall (lateral wing) runs the entire length of the trunk. The two lateral wings can wrap the body so their edges meet in the dorsal midline, although they often gape open along the pharyngeal region. The holotype is a female (presumably the species is gonochoric) with numerous ovaries located in the lateral wings along the pharyngeal region. Each larger ovary contains a single primary oocyte (up to 1,500 μm in diameter) and bulges outwards in an epidermal pouch attached to the rest of the body by a slender stalk. Such externalized ovaries are unprecedented in any animal, and nothing is yet known of their role in the reproductive biology of A. aurantiacus. J. Morphol. 2012.

A Unique Apposition Compound Eye in the Mesopelagic Hyperiid Amphipod Paraphronima gracilis

The mesopelagic habitat is a vast space that lacks physical landmarks and is structured by depth, light penetration, and horizontal currents. Solar illumination is visible in the upper 1,000 m of the ocean, becoming dimmer and spectrally filtered with depth-generating a nearly monochromatic blue light field. The struggle to perceive dim downwelling light and bioluminescent sources and the need to remain unseen generate contrasting selective pressures on the eyes of mesopelagic inhabitants. Hyperiid amphipods are cosmopolitan members of the mesopelagic fauna with at least ten different eye configurations across the family-ranging from absent eyes in deep-living species to four enlarged eyes in mesopelagic individuals. The hyperiid amphipod Paraphronima gracilis has a pair of bi-lobed apposition compound eyes, each with a large upward-looking portion and a small lateral-looking portion. The most unusual feature of the P. gracilis eye is that its upward-looking portion is resolved into a discontinuous retina with 12 distinct groups, each serving one transverse row of continuously spaced facets. On the basis of eye morphology, we estimated spatial acuity (2.5° ± 0.11°, SEM; n = 25) and optical sensitivity (30 ± 3.4 μm(2) ⋅ sr, SEM; n = 25). Microspectrophotometry showed that spectral sensitivity of the eye peaked at 516 nm (±3.9 nm, SEM; n = 6), significantly offset from the peak of downwelling irradiance in the mesopelagic realm (480 nm). Modeling of spatial summation within the linear retinal groups showed that it boosts sensitivity with less cost to spatial acuity than more typical configurations.

A new deep-sea species of harrimaniid enteropneust (Hemichordata)

Abstract Ninety-two individuals of a deep-sea harrimaniid enteropneust were imaged between 1675 m and 3225 m off the California coast. Of these, about three-fourths were positioned with their posterior regions buried in sediment or hidden by rocks, and the rest were completely exposed on the substratum. When visible, the posterior end of each worm was typically associated with a dense tangle of fecal strands. One specimen was captured and is described here as the holotype of Saxipendium implicatum. In life, it was 22 cm long, and the color of its dome-shaped proboscis, narrow collar, and anterior trunk was medium orange. No wing-like folds of the body wall protruded anywhere along the length of the worm. The proboscis complex included a stomochord and glomeruli, but neither a heart nor a pericardial cavity could be detected. Most of the dorsal collar nerve runs along an open invagination in the dorsal midline of the collar and is only roofed over very briefly at the posterior extremity of the collar. Another unusual feature is the exaggerated posterior extension of the horns of the proboscis skeleton, which projected into the anterior extremity of the trunk. The trunk commenced anteriorly with a pharyngeal/esophageal region that included a tract of ovaries on either side of the dorsal midline. The ripest ovaries contained a single oocyte approximately 700 μm in diameter (presumably this species is gonochoric, although no males have yet been collected). The gill skeleton lacked synapticles. More posteriorly, the trunk housed a long, darkly pigmented hepatic intestine without sacculations and a short, lightly pigmented post-hepatic intestine. The geographic range of S. implicatum appears to be restricted to the Davidson, Guide, and Taney Seamounts region in the eastern Pacific offshore of Central California.