New species of Microspio Mesnil, 1896 (Annelida: Spionidae), with additions to the description of M. pigmentata (Reish, 1959) and comparative notes on all members of the genus Free

The spionid polychaete genus MicrospioMesnil 1896 comprises a small group of species, with 18 accepted prior to the addition of the new species in this paper (Table 1)¹. The genus was established by Mesnil (1896) to include two species: Spio mecznikowianusClaparède, 1869 and Spio atlanticusLangerhans, 1880, with the main character separating the two genera being the first occurrence of branchiae on chaetiger 1 in Spio and chaetiger 2 in Microspio. No additional species were described in the genus until Augener described a species from West Africa in 1918 (M. rolasianaAugener, 1918). Gravier (1911) described Mesospio moorei; this genus was later synonymized with Microspio by Foster (1971).

Söderström (1920:247) rejected the idea that the first occurrence of branchiae, the length of the first branchiae, or the fusion or lack of fusion of the branchiae with the dorsal lamellae were relevant systematic characters and synonymized M. mecznikowiana and M. atlantica, making M. mecznikowiana the type species of the genus. He (op. cit.) instead used the number of longitudinal dorsal ciliary bands to distinguish the two genera, with Spio having four such bands (i.e., two pairs) per segment and Microspio having two (i.e., one pair). Bick et al. (2010), however, pointed out the presence of only one pair of these bands in at least one species accepted as Spio (S. goniocephalaThulin, 1957). Although Hannerz (1956) tended to reject the separation of Spio and Microspio based on any of the proposed characters, he observed a few unusual features in the morphology and development of M. atlantica that suggested a separate genus for this species might actually be justified; he resurrected the species from its synonymy with M. mecznikowiana and left the genera as they stood.

Problems with the definition of Microspio and assignment of species to it are apparent in a few of the species assigned to the genus. Developmental studies by Hannerz (1956, for M. atlantica) and Simon (1967, for S. setosa) demonstrated that the first pair of branchiae do not appear in those species until the animal is fully developed, with branchiae first appearing from chaetiger 2 in S. setosa and chaetiger 3 in M. atlantica, whereas the mature adults have branchiae from chaetigers 1 and 2, respectively. When Claparède described M. mecznikowiana, he mentioned the presence of rudimentary, nipple-like gills on chaetiger 1, contradicting his own statement that gills begin on chaetiger 2 (Claparède 1869:64–65). Cazaux (1971) followed the development of M. mecznikowiana through the 23-chaetiger stage; he documented branchiae first appearing as small buds on chaetigers 2, 3, and 4 when the worm was at the 17-chaetiger benthic stage and on chaetigers 2–8 in the 23-chaetiger juvenile. Thus, either chaetiger 2 is the final as well as first occurrence of the first pair of branchiae in this species or, if M. mecznikowiana follows the same pattern as M. atlantica and S. setosa, branchiae may later appear on chaetiger 1. Microspio mecznikowiana has been reported in many ecological studies (e.g., Çinar et al. 2014, Mikac 2015) but has not been redescribed in recent times, so this issue is unresolved. Microspio rolasianaAugener, 1918 was described from newly settled individuals, some of which Augener decided were adults but may not have developed a full complement of branchiae; this species has not been reported since the original description. Using SEM, Meißner & Götting (2015: Fig. 10B, C) were able to see an extra lobe associated with chaetiger 1 in Microspio granulataBlake & Kudenov, 1978; they speculated that one interpretation of this lobe is that it could be a branchial remnant.

Based on the confusion surrounding the first appearance and size of the anterior branchiae, Foster (1971) regarded Microspio as a subgenus of Spio, saying further that they should perhaps be synonymized. However, misunderstanding does not preclude validity and is not a sound basis for synonymy (Blake & Kudenov 1978). Recent authors treating Microspio as a separate genus include Blake & Kudenov (1978), Blake (1983, 1984, 1996), Maciolek (1990), Bick & Meißner (2011), and Meißner & Götting (2015). Given the lack of any phylogenetic investigations, morphological or molecular, into the relationship of these genera, the separation of genera is followed here.

The majority of Microspio species have been described from intertidal or shallow subtidal depths (Table 1); only three species (M. profundaMaciolek, 1990, M. spinosaBlake, 1996, and M. tetrabranchiaMaciolek, 1990) have been described from locations deeper than 100 m; those were from 584–807 m, 90–150 m, and 1760–3600 m, respectively. The three new species found in the present collections come from a range of depths, including shallow water in Bermuda, the continental slope (150 m) off Massachusetts, USA, and deep water (1150 m) in the South China Sea off Brunei.

Collections of polychaetes from offshore the U.S.A. Atlantic coast were made in the 1980s during the Georges Bank Benthic Infauna Monitoring Program (GBMP, aka BIMP) conducted for the U.S. Department of the Interior, Bureau of Land Management (BLM), now the Bureau of Ocean Energy Management (BOEM) and the deep-water U.S. Atlantic Continental Slope & Rise Program (ACSAR, aka ASLAR) also conducted for BOEM (at the time called the Minerals Management Service or MMS). Specimens from off Brunei in the South China Sea were collected as part of deep-water baseline studies conducted for Total E&P Deep Offshore Borneo B.V. in 2011. Collection of the material from Bermuda was made by hand in shallow water near the Bermuda Biological Station (see Fischer & Fischer 1995 for details). Specimens of M. pigmentata (Reish, 1959) were borrowed from the Los Angeles County Museum, Allan Hancock Foundation collections.

In the field, samples were sieved on either a 300-μm-mesh or a 500-μm-mesh sieve, preserved in 10% formalin, and later transferred to 70% ethyl alcohol (EtOH). Specimens were examined with light microscopy using a high-quality Wild M-5 stereomicroscope and a Zeiss research compound microscope equipped with phase contrast optics. Measurements were made using an ocular micrometer. Photographs were taken with a Nikon D7100 camera mounted on the stereo- and compound microscopes. Some specimens were stained with Shirlastain A to highlight surficial morphology; other specimens were stained with a saturated solution of Methyl Green (MG) in 70% EtOH to elucidate staining patterns, which are usually associated with glandular structures that preferentially retain this stain. The MG stain dissipates completely in fresh EtOH, although some morphological features may retain the stain for several days or even weeks. Line drawings were made in pencil using a drawing tube (camera lucida) on the Zeiss or sometimes by tracing photographs. Sketches were scanned and imported into Adobe Illustrator where vector line drawings were made. Plates were prepared using Adobe Power Point and Adobe Photoshop software.

This work has been registered in ZooBank with the registration number urn:lsid:zoobank.org:pub:D24F8834-3230-469D-A2CD-759B018EF8AB.

Abbreviations of sampling programs and institutions referred to in this paper:

ACSAR

Atlantic Continental Slope & Rise (aka ASLAR)

AHF

Allan Hancock Foundation

ASLAR

Atlantic Slope and Rise (aka ACSAR)

BOEM

Bureau of Ocean Energy Management

BLM

Bureau of Land Management

BIMP

Benthic Infauna Monitoring Program (aka GBMP)

CAMP

California Monitoring Program

GBMP

Georges Bank Monitoring Program (aka BIMP)

LACM

Los Angeles County Museum

MCZ

Museum of Comparative Zoology, Harvard University

MMS

Minerals Management Service

USNM

Smithsonian Institution, National Museum of Natural History

MicrospioMesnil, 1896 

• MicrospioMesnil, 1896; type-species: Spio mecznikowianusClaparède, 1869 (type by subsequent designation [Söderström 1920]).

• MesospioGravier, 1911; type-species: Mesospio mooreiGravier, 1911, by monotypy. Fide Foster 1971.

Prostomium anteriorly rounded to deeply incised, frontal or lateral horns always absent; eyespots present or absent; occipital antenna present or absent. Nuchal organ with median and lateral ciliary bands extending to chaetiger 2 or 3, sometimes an oval or U-shaped ciliated groove. Longitudinal metameric dorsal ciliated organs present or absent. Transverse ciliary bands connecting bases of branchiae on some segments. Branchiae present from chaetiger 2, restricted to anterior region or continuing to posterior end of body; completely free or partly fused with bases of notopodial postchaetal lamellae. Ventral epidermal glands present or absent. Notochaetae capillaries of various types; notopodial spines present or absent; neurochaetae include capillaries and hooded hooks, hooks bi-, tri-, or multidentate; ventral sabre chaetae present or absent. Pygidium with 2–4 anal cirri.

Bick & Meißner (2011) discussed characters important in the description of Spio and Microspio species; they emphasized the need to include new characters such as the shape of the nuchal organs and dorsal ciliary bands in any revision. Meißner et al. (2011, 2015) refined the diagnosis of Microspio to include characterization of the nuchal organs and metameric dorsal bands; the wording of the present diagnosis differs slightly from that given in Blake et al. (2020), primarily with reference to these ciliary patterns. It also includes the potential for inferior sabre chaetae being absent, as well as the branchiae being completely free from the notopodial postchaetal lamellae as described by early authors (Mesnil 1896) and as seen, for example, in the middle and posterior chaetigers of Microspio elegantulaBlake, 1984 and M. granulataBlake & Kudenov, 1978 as figured in Meißner et al. (2015). This feature is difficult to see in the anterior region of very small specimens; it is usually clearer in middle and posterior regions; sometimes the branchiae may be (partly) fused in anterior chaetigers and free in posterior chaetigers, as in M. lydonia, new species, described below. Table 1 includes a summary of described characters for currently accepted Microspio species.

Microspio fischeri, new species Figs. 1–3

urn:lsid:zoobank.org:act:4CE1500E-17D7-4069-A1C5-2B2BF7A34C76

North Atlantic Ocean, Bermuda, SW of St. George's, near Ferry Point, coll. A. Fischer, 16 Jun 1994, 21.746′N, 64°42.827′W, intertidal, associated with Ircinia sp. (sponges), holotype (MCZ 162298); 6 paratypes (MCZ 162299).

A very small species, complete specimens measuring 0.3 mm wide and 2.0 mm long for 22–24 chaetigers. Color in alcohol: chalk white. Body slightly tapered in far posterior region; regenerating specimen with posterior segments much smaller than preceding chaetigers. Prostomium deeply incised anteriorly, forming rounded anterior lobes (Figs. 1A, B, D, 2A), medial portion with straight sides, posterior portion narrow elevated caruncle extending to middle of chaetiger 2; occipital tentacle absent; eyespots absent. Palps with groove, without sheath or papillae, with rounded tip, extending for roughly one-half the body length. Nuchal organs oval or U-shaped, from posterior margin of caruncle to middle of chaetiger 2, indistinct, seen only after staining, surrounded by curved row of ciliated cells extending between branchial bases (Fig. 2A). Transverse dorsal ciliated bands present between bases of branchiae from chaetiger 3, particularly visible on median chaetigers, continuing throughout posterior segments. Longitudinal dorsal metameric ciliary bands or patches not observed. Venter without epidermal glands. Internal gut narrow and straight to chaetiger 7; then separated from wider intestine with two glandular structures on either side that retain Shirlastain A (Figs. 1A, B, 2A); wider intestine narrowing toward end of body. Peristomium surrounding prostomium dorsally, fused with chaetiger 1 ventrally but not dorsally (Figs. 1B, D, 2A, B, D).

Chaetiger 1 weakly distinguished from chaetiger 2 on venter (Figs. 1D, 2D), segments distinct thereafter (Fig. 1B). Chaetiger 1 reduced, lacking notopodium, neuropodium small, with a few short, fine capillary chaetae (Figs. 1A, C, 2A, B). Notopodial postchaetal lamellae from chaetiger 2 small at first, oval, rounded on distal margin (Fig. 2B); lamellae gradually becoming larger along anterior and middle chaetigers and noticeably large and club-shaped in far posterior chaetigers (Figs. 1A, E, 2E); all notopodial postchaetal lobes glandular, especially in posterior chaetigers. Notopodial prechaetal lobes inconspicuous bump in anterior chaetigers, absent in middle and posterior chaetigers. Neuropodial postchaetal lamellae small, oval on first two chaetigers, becoming larger, square-shaped through middle region (Fig. 2B), glandular in posterior chaetigers; no neuropodial prechaetal lobes. Neuropodia appearing increasingly swollen posteriorly, most obvious in ventral view starting around chaetiger 6–9 (Fig. 1B); swollen area anterior to chaetae, which are positioned in posterior portion of podium in these segments (Figs. 1G, 2C). Branchiae from chaetiger 2; first pair small, triangular, upright, well separated medially from notopodial lobe (Figs. 1A, C, 2A, B); from chaetiger 3, branchiae at base of notopodial lamellae, short, rounded at first, rapidly becoming larger, straplike, through chaetigers 14–18, then becoming smaller or absent in far posterior chaetigers (Figs. 1A, 2A, B). Branchiae close to but do not appear fused with notopodial postchaetal lamellae.

Anterior notopodial chaetae all capillaries, arranged in two rows; anterior row of chaetiger 2 with three chaetae, these shorter, curved, limbate, moderately granulated; posterior row with three chaetae, these longer, straight, alimbate. Chaetiger 3 with one short, granular limbate chaeta and three longer limbate chaetae. Notochaetae of chaetigers 4–8 include 5–10 capillaries, each broadly limbate with long, fine aristate tips, limbation of these chaetae long, thickened and undulating, with a few small protruding fibrils below the arista (Figs. 1H, 3A); these chaetae in two rows with 2–3 shorter aristate capillaries in first row and with up to seven long chaetae in second row. Posterior notochaetae long thin capillaries with only narrow limbation. Anterior neuropodial chaetae include ca. five short, thin capillaries on chaetiger 1; from chaetiger 2, capillaries in two rows, anterior row shorter, with broad limbation and fine aristate tips. Neurochaetae of chaetigers 4–6 arranged in ventral group of three in slightly curved row, separate from additional dorsal group of 3–4 broad, thickened chaetae with narrow tapered tip (Figs. 2B, 3B). Chaetigers 7–8 also with broad, limbate capillaries but these smaller than in preceding chaetigers. Neuropodial hooded hooks from chaetiger 9, usually 2 per fascicle, sometimes 1 or 3, absent from last 1–3 chaetigers; hooks bidentate, with small pointed apical tooth surmounting main fang (Figs. 1F, 3D); hood bulbous, entirely surrounding apex, with opening from which fang emerges; shaft straight, then curving at point of emergence from neuropodium. Hooks accompanied by 0–2 fine straight capillaries. Ventral sabre chaetae present from chaetiger 9–10, golden in transmitted light, curved, usually single but may be two per podium.

Pygidium with four anal cirri; oval to paddle-like, highly glandular, dorsal cirri larger than ventral cirri (Figs. 1E, 2E).

Body destains fairly rapidly; stain is retained briefly on anterior-most ends of peristomium. Posterior parapodial lamellae and anal cirri initially stain deeply but rapidly lose the stain. Venter picks up stain on chaetigers 4–5 but this is also rapidly lost. No indication of ventral epidermal glands.

Microspio fischeri has three morphological characters that make it unique among Microspio species: 1) the almost medial location of the first pair of branchiae, which are well separated from the notopodial lamellae; 2) the enlarged, glandular, and club-shaped notopodial postchaetal lamellae of posterior chaetigers; and 3) the unusual aristate capillary chaetae of some anterior notopodia, some of which have thickened undulating limbations.

Microspio fischeri shows some similarity to M. paradoxaBlake, 1983, described from 17–18 m water depth in the Galápagos Islands, in that both species have modified capillaries in several anterior chaetigers. In M. fischeri, the notochaetae of chaetigers 4–8 include broadly limbate capillaries with long, fine aristate tips; the limbation is long, thickened, and undulating. In M. paradoxa, the posterior row of notochaetae in chaetigers 7–10 includes capillaries with a wide limbation that is notched or open, which is unique in Spionidae (Blake 1983); M. paradoxa differs further from other Microspio species by having the notochaetae of chaetigers 4–6 in a U-shaped arrangement. In M. paradoxa, the neurochaetae of chaetigers 4–6 are thicker than those of chaetigers 3 and 7, whereas in M. fischeri, the neurochaetae of chaetigers 4–6 are arranged in a ventral group of three in a slightly curved row, separate from an additional dorsal group of 3–4 broad, thickened chaetae with a narrow tapered tip; chaetigers 7–8 also have broad, limbate capillaries but these are smaller overall than in preceding chaetigers.

Several species, including M. granulata, M. microcera, and M. minuta, have a bilobed prostomium, lack notochaetae on chaetiger one, and have hooks starting on chaetiger 9, but differ from M. fischeri in other characters such as the number of teeth on the hooks, as well as the placement of the first pair of branchiae (see Table 1).

The discovery of a new Microspio species in Bermuda was part of a research project on the biology of the bioluminescent syllid Odontosyllis enopla Verrill, 1900 conducted by Albrecht and Ursula Fischer in 1994. Apart from the spectacular bioluminescence associated with the syllid, nothing was known about the biology of the species, including their fate after swarming and spawning until the results by Fischer & Fischer (1995). The authors were able to study the diet of post-swarming adults in the laboratory, including specimens transported to Germany from the collection site in Bermuda. Fischer & Fischer (1995:242) state: “We offered a variety of potential diets to post-swarming worms: artificial fish food; the sponges Ircinia, Chondrilla, and Tedania and the excavating sponge, Cliona sp.; hydrozoans (e.g., Myrionema amboinense Pictet); colonies of encrusting bryozoans; the ascidian Botrylloides; and a number of polychaetes (cirratulids, terebellids, spionids, and decapitated nereids). Of all of these food items only spionids and, in a few cases, small terebellid polychaetes were accepted as food.” The preferred prey was a spionid, later identified as a new species of Microspio, which was found in large numbers inhabiting sponges of the genus Ircinia in Bermuda.

In a communication to one of us (JAB) in November 1994, Dr. A. Fischer described the Microspio collecting site as shallow sublittoral with moderate current, and a rough coral gravel substrate at the fringe of a Thalassia sea grass bed. The brown sponges (Ircinia sp.) were growing upright between gravel and sea grass. Dr. Fischer described the Microspio specimens as very numerous in these sponges; they were residing in sediment-covered mucoid tubes oriented perpendicular to the surface of the sponge. When the sponges collected were removed from seawater and became stressed and fouling, the worms left the sponges in great numbers, probably due to oxygen stress. After collection, the worms proved to be hardy, and Dr. Fischer was able to transport them to his laboratory in Germany where further feeding experiments were performed with the syllids.

Associations of spionids and sponges appear to be rare and all reported taxa are genera and species of the Polydora complex (Martin & Britayev 1998, 2018). All five known species of Polydorella live on the surface of sponges where they construct tubes (Williams 2004, Radashevsky 2015). A few polydorid species are known to burrow and build tubes directly into the sponge from which they extend their palps and feed in the overlying water. The best known example is Polydora colonia Moore, 1907, which builds tubes in the sponge Microciona prolifera and other species. First described from near Woods Hole, Massachusetts, the species has since been widely collected globally, apparently because the host sponges colonize the hulls of ships, which transport the worms to distant ports (Blake 1971, David & Williams 2012, Blake et al. 2020). Polydora spongicolaBerkeley & Berkeley, 1950 has been collected from several different sponge species and is known from Canada to southern California (Woodwick 1963) and the north-western Pacific (Radashevsky 1993). Carazziella spongillaSato-Okoshi, 1998 constructs tubes within the sponge Spongilla alba, in a brackish water lake in Japan. Microspio fischeri is thus the first non-polydorid species of Spionidae to be reported as an inhabitant of sponges.

This species is named in honor of Dr. Albrecht Fischer, who collected the organisms and made them available to us for study.

Shallow sublittoral; known only from the type locality in Bermuda, associated with the sponge genus Ircinia.

Microspio pigmentata (Reish, 1959)
Fig. 4

Eastern Pacific Ocean, California. Orange County, Lower Newport Bay, Newport Harbor, Sta. NB-14, 33°36′31.17″N, 117°54′11.72″W, 13 ft., gray mud, coll. D. J. Reish, 26 Jan 1951, 11 paratypes, (LACM-AHF Poly 606).—San Diego Bay, id. L. Harris, 14 May 2020, St. NB-DS/R.2, 40 m, 2 specimens (LACM-AHF Poly 12727).—Santa Maria Basin, coll. Battelle: off Purisima Point, CAMP 1-2, Sta. R-5, rep. 2, Jan 1987, 34°42.69′N, 154 m, 1 specimen (LACM-AHF Poly 12724); CAMP 2-5, Sta. R-5, rep. 1, May 1988, 34°42.69′N, 154 m, 1 specimen (LACM-AHF Poly 12725). CAMP 3-4, Sta. R-8, Rep 2, May 1989, 34°55.30′N, 120°45.90′W, 90 m, 1 voucher specimen id. Susan Williams (LACM-AHF Poly 12723). CAMP 1-3, Sta. PJ-7, May 1987, 34°55.79′N, 120°48.60′W, 123 m, 1 specimen (LACM-AHF Poly 12726).

Nuchal organs with medial ciliary bands adjacent to posterior prostomium extending to chaetiger 2, then turning laterally, with small gap between this and second, lateral band (Fig. 4A, B). From chaetiger 3, dorsum with two transverse rows of ciliated patches; one row extending between branchial bases; second row widely separated from first, near segmental groove (Fig. 4C). Single pair of longitudinal dorsal metameric ciliated organs visible after staining on chaetigers 10—end of 27-chaetiger fragment, largest on chaetiger 20–25 (Fig. 4D).

Venter with dark pigment spots on midline of several segments.

Prostomium stains deeply, especially in middle region where pigment is concentrated, posterior tip destains rapidly. Ventral peristomium retains stain evenly on posterior half, speckled on anterior half. Nuchal organs and transverse ciliary rows do not stain. Small glands in branchiae and both notopodial and neuropodial lamellae stain deeply. Dorsum with numerous small, stained spots in most chaetigers, weakly organized into transverse rows; venter also with stained spots concentrated along midline in anterior chaetigers where pigment is densest, become diffuse posteriorly, no indication of ventral epidermal glands.

Neither Reish (1959) nor Maciolek (1990) mentioned nuchal organs, transverse dorsal ciliated bands, or metameric longitudinal bands in their descriptions; examination of the paratypes and additional fresh material allowed these characters to be described. The nuchal organs are for the most part typical for the genus, although the medial band is alongside the prostomial caruncle rather than posterior to it. The double, widely separated, transverse ciliary bands are unusual in that they appear as isolated patches rather than a continuous row, and other Microspio species have a single rather than double row (see Table 1).

Microspio lydonia, new species Figs. 5, 6

urn:lsid:zoobank.org:act:C3624AEA-DB0C-45DE-8133-B1A229529C81

Not Reish (1959).

Western North Atlantic, off Massachusetts, Georges Bank, head of Lydonia Canyon, Sta. 7, 40°28.7′N, 67°42.7′W, Cruise M2, coll. M. Rawson, Lamont-Doherty, Chief Scientist, R/V Oceanus, 11 Nov 1981, ca. 150 m, rep. 3, Holotype (USNM 1655928) and 4 paratypes (USNM 1655929); rep. 5, 1 paratype (USNM 1655930). coll. G. Hampson, WHOI, Chief Scientist. Cruise M3, R/V Endeavor, 17 Feb 1982, 152 m, rep. 1, 2 paratypes plus posterior fragment from a 3^rd specimen (USNM 1655931); rep. 3, 7 specimens (6 lost) (USNM 1655932); rep. 5, 4 paratypes (USNM 1655933). Cruise M4, R/V Cape Henlopen, 13 May 1982, 40°28.8′N, 67°43.2′W, 130 m, rep. 3, 1 specimen (USNM 1655934). Sta. 7A, Cruise M12, R/V Gyre, 5 Jun 1984, 40°32.2′N, 67°44.2′W, 167 m, rep 4, 1 specimen (USNM 1655935). Sta. 8, Cruise M12, R/V Gyre, 5 Jun 1984, 40°27.1′N, 67°37.4′W, 152 m, rep 4, 1 specimen (USNM 1655936).—Georges Bank, head of Oceanographer Canyon, Sta. 9, 40°26.7′N, 68°09.8′W, Cruise M1, R/V Eastward, Jul 1981, ca. 145 m, rep. 3, 1 specimen (USNM 1655937); Cruise M3, R/V Endeavor, 13 Feb 1982, 145 m, rep. 4, 2 specimens (partly dried out) (USNM 1655938); Cruise M4, R/V Cape Henlopen, 16 May 1982, 144 m, rep. 6, 3 specimens (USNM 1655939); Cruise M8, R/V Gyre, 19 May 1983, 143 m, rep. 1, 2 specimens (USNM 1655940); Cruise M9, R/V Gyre, 19 Jul 1983, 144 m, rep. 3, 1 specimen (USNM 1655941); Cruise M12, R/V Gyre, 8 Jun 1984, 144 m, rep. 1, 2 specimens (USNM 1655942), rep. 4, 1 specimen (USNM 1655943), rep. 6, 1 specimen (USNM 1655944).—Georges Bank, Sta. 12, 40°22.2′N, 68°30.2′W, ca. 105 m, Cruise M1, R/V Eastward, Jul 1981, rep. 2, 2 specimens (USNM 1655945); Cruise M2, R/V Oceanus, 12 Nov 1981, rep. 3, 1 specimen (USNM 1655946); Cruise M3, R/V Endeavor, 12–13 Feb 1982, 105 m, rep. 2, 1 specimen (USNM 1655947). Sta 17, 40°34.9′N, 67°11.1′W, Cruise M3, R/V Endeavor, 18 Feb 1982, 145 m, rep. 6, 1 specimen (USNM 1655948). Sta. 18, 40°33.5′N, 67°13.7′W, Cruise M3, R/V Endeavor, 17–18 Feb 1982, 145 m, rep. 1, 2 specimens (USNM 1655949); rep. 6, 3 specimens (USNM 1655950); Cruise M4, R/V Cape Henlopen, 13 May 1982, 150 m, rep. 2, 3 specimens (USNM 1655951); rep 3, 1 specimen (USNM 1655952).—US North Atlantic ACSAR Program, Sta. 11, 40°01.3′N, 70°55.1′W, coll. R. Petrecca, WHOI, Chief Scientist, Cruise North-1, Leg 2, R/V Cape Hatteras, 8 Dec 1984, rep. 1, 253 m, 3 specimens (USNM 1655953); rep. 2255 m, 6 specimens (USNM 1655954). Cruise North-2, coll. G. Hampson, WHOI, Chief Scientist, R/V Oceanus, 4 May 1985, rep. 3250 m, 5 specimens (one with posterior) (USNM 1655955).

Holotype incomplete, 1 mm wide, 4 mm long for 16 chaetigers; other specimens 0.8–1 mm wide, 2.5–3.0 mm long for 11–16 chaetigers. Color in alcohol white, one specimen with very faint circular pigment mid-prostomium, two specimens with faint brownish pigment spots mid-venter on six to eight anterior chaetigers.

Prostomium rectangular, slightly flared anteriorly (Figs. 5A, 6A); no occipital tentacle; eyespots 0–4, if present, brown spots in trapezoid arrangement. Palps present on one small specimen, extending lengthwise through widest anterior region, other palps lost. Peristomium forming low collar on dorsal side, inflated, puckered on ventral side (Fig. 5A, B, 6A, B). Nuchal organ with medial bands from posterior margin of prostomium extending longitudinally to middle of chaetiger 2, then turning laterally, small gap between medial and lateral band, which also extends to middle of chaetiger 2, may turn slightly laterally at the end (Figs. 5A, 6A). Chaetiger 1 with cilia obscuring posterior margin of prostomium, visible with MG staining (Figs. 5A, 6A); from chaetiger 2, dorsum with transverse ciliary bands extending between branchial bases (Fig. 6A). Longitudinal dorsal metameric ciliary bands or patches not observed.

Chaetiger 1 with both notopodial and neuropodial postchaetal lamellae and chaetae: notopodium with small, rounded, slightly oval, glandular lamella and about 15–20 capillary chaetae; neuropodial lamellae broader than notopodial lamellae, with about 20 capillary chaetae. From chaetiger 2, notopodial lamellae broad, glandular, largest in anterior and mid-body chaetigers (Figs. 5C, 6A, B), then becoming smaller, oval, in posterior segments, very small in far posterior chaetigers (Figs. 5D, 6E); no prechaetal notopodial lamellae. Neuropodial lamellae glandular, rectangular with broad, rounded distal edge through midbody, then becoming smaller through posterior chaetigers (Figs. 5D, 6B, D). Branchiae from chaetiger 2, first pair about same size or slightly smaller than those following (Figs. 5A, 6A), continuing throughout posterior segments, except for last 2–3 chaetigers; basally fused to notopodial lamellae (Figs. 5C, 6A), longest through mid-body region, then becoming very small, short posteriorly, increasingly separate from lamellae.

Anterior notopodial and neuropodial chaetae capillaries in two rows, anterior row shorter than posterior row, 20–30 chaetae per fascicle. Neuropodial hooded hooks from chaetiger 10, initially 5–6 per fascicle, increasing up to 26 in posterior chaetigers, then abruptly decreasing to 2–5 in last few chaetigers; with anterior row of curved capillary chaetae up to twice the length of hooks and 2–3 thin, inconspicuous chaetae in inferiormost position of fascicle; hooks multidentate, with main fang surmounted by usually 3 (sometimes 2) large single teeth and by 2 (sometimes 3) pairs of smaller apical teeth (Figs. 5F, G, 6C); shaft of hooks slightly curved, appearing striated. Posterior notopodial chaetae long, fine, stiff capillaries numerous in last 10–12 chaetigers (Figs. 5D, 6D).

Pygidium on smallest specimens with rounded dorsal lobe (Fig. 6E), larger specimen with two tiny dorsal lobes (Figs. 5D, 6D).

Dorsal prostomium stains deeply in middle region with a dense speckled pattern; posterior prostomium usually clear but often with a few small spots medial and posterior to eyes, cilia across base visible with staining (Fig. 5A). Anterior prostomium mostly clear of stain on dorsal surface; lateral tips stain on ventral surface as a continuation of stain along the lateral edge of prostomium (Fig. 5E). Dorsal and lateral peristomium stain in dense pattern, similar to prostomium (Fig. 5B). Ventral peristomium stains in stripes along posterior half, with lateral stripes going over top and down into the gullet (Fig. 5E). Ventral portion of chaetiger 1 stains, paralleling ventral peristomial stained pattern. Small glands in palps, branchiae, and both notopodial and neuropodial lamellae stain deeply. Dorsum and venter both with transverse rows of small stained spots along length of body, these stain more deeply in anterior (especially just posterior to nuchal organs) and mid-body.

Of the 60+ specimens examined, 6–10 had eyespots, four had brown pigmented spots on the mid-line of the venter, and two had a bit of brown pigment laterally (between the parapodia) on some anterior segments starting with chaetiger 3. Only one specimen had a faint round patch on the middle of the prostomium.

Microspio lydonia is very similar to M. pigmentata (Reish, 1959) and was identified as such in an earlier paper (Maciolek 1990). Characters shared in common include unusual multidentate hooded hooks and a posterior region with extremely long, stiff capillary chaetae. Maciolek (1990) redescribed M. pigmentata (Reish, 1959) based on the holotype from California and additional material from several locations along the east coast of the U.S.A.; her Fig. 8 is based on one of several specimens from Florida, which was considered identical to the holotype. At that time, some differences among the specimens from various locations, especially Georges Bank, were noted but not considered to be of taxonomic importance; these and additional differences are now given more weight, particularly given the geographic separation between the original M. pigmentata and M. lydonia. These differences include size, pigmentation, the structure of the nuchal organs and transverse ciliary bands, the number and arrangement of teeth on the hooks, the number of hooks per chaetiger, and the structure of the pygidium.

Microspio lydonia is a smaller species than M. pigmentata; it measures roughly half the width for the same length/number of chaetigers. Microspio pigmentata is strongly pigmented, with a circular patch of brown pigment in the middle of the prostomium and between the noto- and neuropodia of one to several anterior segments. Reish (1959) also described dorsal pigment medially on chaetigers 2–6 (or up to chaetiger 12), and dark ventral pigment spots were seen on the material examined in this study. Only a few specimens of Microspio lydonia had any pigment on the dorsal surface and that was very faint; a few specimens had light brown spots on the mid-line of the venter.

The nuchal organs of M. lydonia originate at the posterior end of the prostomium and there is one row of transverse cilia per segment, whereas in M. pigmentata the medial ciliary band first runs alongside the prostomium and there are two dorsal ciliary bands per segment. Microspio lydonia exhibits a striped MG staining pattern on the ventral side of the peristomium; in comparison, the ventral peristomium of M. pigmentata retains stain in the posterior portion, but this is solid or speckled, not striped.

The multidentate hooks of M. lydonia usually have three, sometimes only two, single teeth surmounted by one or two pairs of very small apical teeth. The hooded hooks of the M. pigmentata holotype were described by Reish (1959) as having two large single teeth surmounted by a pair of smaller teeth and a third small tooth at the apex; Maciolek (1990) reported hooks with two single and three pairs of teeth as clearly seen on the holotype as well as on the specimens from Florida and North Carolina, thus differing from the three single teeth and apical pairs in M. lydonia. Up to 30 hooks per fascicle are present in the posterior chaetigers of M. pigmentata, whereas M. lydonia has slightly fewer, up to 26 per fascicle. Both M. lydonia and M. pigmentata have extremely long capillary chaetae in the far posterior chaetigers, but these may be more numerous in M. lydonia. With only three posterior ends available, the character of the pygidial lobe in M. lydonia was difficult to confirm, but it appears to have poorly developed cirri, if any, which differs from M. pigmentata, which has four anal cirri.

All of these differences point to the conclusion that the Georges Bank material represents a different species; material from the Gulf of Mexico and southeastern U.S.A. previously reported as M. pigmentata (Johnson 1984, Maciolek 1990) should be reevaluated.

In addition to the current material examined, 71 lots of material from the MMS GBMP and ACSAR programs are accessioned at the USNM (Accessions 359235 and 364005) as Microspio cf. pigmentata, but this material was not available for reexamination for this study. However, the material on hand is from several of the same stations, so it is with some confidence that we suggest that the Microspio in those lots is the same as this newly described species.

The species name refers to Lydonia Canyon, where much of the material was collected. The canyon itself was named for NOAA's Coast and Geodetic Survey vessel, the Lydonia, one of the four ships that conducted surveys of the area between the years 1930 and 1932.

Northwestern North Atlantic, off Massachusetts, 130–255 m.

Microspio ariena, new species Figs. 7–8

urn:lsid:zoobank.org:act:F5C8ACA5-0A33-49AE-B6B9-19F86BEB57C1

South China Sea, off Brunei. coll. J. A. Blake, Chief Scientist. Site CA1, R/V Emma, Sta. 55, 01 Jun 2011, 05°43.652′N, 114°14.768′E, 1150 m, holotype (MCZ 162300).

A small species, holotype incomplete, 0.4 mm wide, 1.5 mm long for 13 chaetigers. Color in alcohol white, no pigment. Prostomium with anterior edge difficult to discern, may be oriented ventrally, may have medial incision with slightly inflated tips, posterior end extending to posterior of chaetiger 1; no eyespots, no occipital tentacle (Figs. 7A, D, 8A). Peristomium forming low dorsal collar, fused with chaetiger 1 ventrally but not dorsally. Nuchal organs not obvious, even with MG or Shirlastain A. Transverse dorsal ciliated bands short, indistinct on chaetiger 2, obvious from chaetiger 3 through end of fragment; two rows per chaetiger, cilia oriented in opposite directions in fixed specimen (Fig. 8A). Longitudinal dorsal metameric ciliary bands or patches not observed. Dorsum with small tear-shaped glands mid-chaetiger. Venter without epidermal glands. Chaetiger 1 with very small, oval to slightly pointed, notopodial lamella and 4–6 notopodial capillaries (Fig. 8A), neuropodium with slightly larger lamella and 10–12 capillary chaetae (Figs. 7A, D, 8A). Chaetigers 1 and 2 distinct dorsally and ventrally. Notopodial postchaetal lamellae glandular, small rounded rectangles from chaetiger 2, becoming smaller, slightly oval in posterior chaetigers. Neuropodial lamellae small, gently rounded rectangles throughout, slightly glandular. Branchiae from chaetiger 2, large, elliptical, densely packed with large elongate glands, largest on chaetigers 3–6, smaller on 7, missing on chaetigers 8–11, small, digitiform on chaetigers 12–13 (last two of fragment) (Figs. 7A, B, D, 8A, B); fusion of branchiae with base of lamellae not clear, fused at base, if at all.

Capillary chaetae in two rows from chaetiger 2 in both noto- and neuropodia; anterior row slightly curved, shorter than posterior row, capillaries slightly bilimbate, not granulated or striated. Hooded hooks from chaetiger 11, straight, tridentate with two small teeth side-by-side over large tooth, appearing bidentate in profile (Figs. 7E, 8C); hooks numbering four per fascicle, with a few accompanying capillaries that greatly exceed hooks in length. Sabre chaetae absent, 1–3 delicate neuropodial chaetae in inferiormost position from chaetiger 9.

Posterior and pygidium unknown.

Prostomium stains dorsally, darkest in middle area; peristomium stains dorsally and ventrally, becoming irregularly spotted ventrally as destaining occurs. Branchiae and notopodial lamellae stain heavily in anterior chaetigers; in chaetigers 8–13, notopodial lamellae with a few glands that stain lightly. Neuropodial lamellae stain lightly throughout. Dorsal surface with 1–4 small elongate or tear-shaped glands mid-chaetiger. Venter stains lightly in anterior region, with irregular and widely scattered spots. Internal gut stains posteriorly to chaetiger 7 (where anterior branchiae end).

Microspio ariena is most similar to Microspio profundaMaciolek, 1990 from 1760–3600 m off New England, Delaware, and the Bahamas. The two species have a similar prostomial shape, i.e., slightly bilobed, although this feature is more pronounced in M. profunda than in M. ariena; both lack eyes and an occipital tentacle and have notopodia and notopodial capillaries on chaetiger 1. The hooded hooks are slender and similarly tridentate in both species, but number up to eight in M. profunda and only up to four in the anterior fragment of M. ariena. The two species differ in the shape of the branchiae, which are long and straplike along the entire body in M. profunda but are large, elliptical, and heavily glandular in the anterior region and very small in later chaetigers in M. ariena. The branchiae differ considerably in shape among the three deep-water species, being long and tapered in the anterior chaetigers of M. profunda and M. tetrabranchia, but shorter and elliptical as well as heavily glandular in M. ariena. The absence of branchiae from chaetigers 8–11 in M. ariena is unusual for this genus; no branchial scars were noted on those chaetigers but having only one specimen for study precludes understanding whether this is a consistent feature of the species.

Latin ariena, meaning fruit of the plantain or banana; used as a noun in apposition, the specific name refers to the elongate glands in the branchiae that resemble a hand of bananas.

Known only from the type locality in the South China Sea, off Brunei; 1150 m.

We are grateful to Dr. Albrecht Fischer for the opportunity to study and describe the spionid he collected in Bermuda (and fed to the syllids in his lab!). Collection of the GBMP and ACSAR material was made under contract Nos.14-12-0001-29192 and 14-12-0001-30064 from the Department of the Interior, Minerals Management Service, to Battelle Ocean Sciences (1983–1987). Field teams were led by the late Mr. George Hampson (WHOI; Georges Bank and U.S. North Atlantic surveys) and Ms. Rose Petrecca (WHOI, Georges Bank surveys). The field work off Brunei was led by Dr. J. A. Blake as part of a project for Total E&P Deep Offshore Borneo B.V. Many lab technicians carefully sorted the samples for the benthic projects that yielded the polychaete material. Our thanks to everyone who participated in these projects. Ms. Leslie Harris of the LACM-AHF arranged loans of types and additional material. Ms. Katherine Ahlfeld (USNM), Mr. Adam Baldinger (MCZ), and Ms. Harris (LACM) provided museum catalogue numbers for the lots deposited in their respective museums. Special thanks to Drs. Karin Meißner and Robin Wilson, both of whom reviewed the manuscript and offered several thoughtful and useful suggestions for improvement. Finally, we acknowledge and thank the Biological Society of Washington for covering the costs of publication of this paper for inclusion in the capstone edition of their Proceedings.