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Boba PE ee OTT oe ee ee ET ere Ee NE aS array cae thee af he ITI <9 Bae oF wha aS F I RROD ore lp re ; ~ sae iu aoe: i < 2g Sh S STs Me ST ETAT ORNL eet eam aguemeonsn natn Se aie tamee : 2 xe mee ste tateoe a a a 56 ek ow ; ; aaa a eran apes oe A tet ; 7 . a : ; ? ‘ Reman per a) nese ai pemea e ir . ay he 3 > “ore 4 iy be ers Be eee ee < prise : : : POSTILLA PEABODY MUSEUM YALE UNIVERSITY NUMBER 144 27 APRIL 1970 - THE TAXONOMIC STATUS OF QUILL WORMS, GENUS HYALI- NOECIA (POLYCHAETA: ONU- PHIDAE), FROM THE NORTH AMERICAN ATLANTIC CONTINENTAL SLOPE CHARLOTTE P. MANGUM WILLIAM R. RHODES POSTILLA Published by the Peabody Museum of Natural History, Yale University Postilla includes results of original research on systematic, evolution- ary, morphological, and ecological biology, including paleontology. Syntheses and other theoretical papers based on research are also welcomed. Postilla is intended primarily for papers by the staff of the Peabody Museum or on research using material in this Museum. Editors: Nancy A. Ahlstrom, Elizabeth G. Weinman, Elise K. Kenney. Postilla is published at frequent but irregular intervals. Manuscripts, orders for publications, and all correspondence concerning publications should be directed to: Publications Office Peabody Museum of Natural History New Haven, Conn., 06520, U.S.A. Lists of the publications of the Museum are available from the above office. These include Postilla, Bulletin, Discovery, special publications, and available back numbers of the discontinued journal, Bulletin of the Bingham Oceanographic Collection. All except Discovery are available in exchange for relevant publications of other scientific institutions anywhere in the world. THE TAXONOMIC STATUS OF QUILL WORMS, GENUS HYALINOECIA (POLYCHAETA: ONUPHI- DAE), FROM THE NORTH AMERICAN ATLANTIC CONTINENTAL SLOPE CHARLOTTE P. MANGUM WILLIAM R. RHODES Department of Biology College of William and Mary ABSTRACT Morphological characters of quill worms from the North American continental slope have been compared with those of Hyalinoecia tubicola (O. F. Miller) from the English Channel. The results in- dicate consistent and exclusive differences in worms of the same size. We suggest that Hyalinoecia artifex Verrill be reinstated for North American quill worms, as originally intended. POSTILLA 144: 13 p. 27 APRIL 1970. 2 POSTILLA INTRODUCTION Quill worms of the onuphid genus Hyalinoecia are often dredged in great numbers from 400-1500 meters depth on the continental slope of the northwestern Atlantic Ocean. These worms were orig- inally described as H. artifex by Verrill (1880, 1885a, 1885b), who remarked upon the close relationship with the European H. tubicola (O. F. Muller). The primary difference clearly stated by Verrill (1880) is larger size, although his full description (Verrill, 1885b) includes a number of morphological characters that do not agree with those of H. tubicola. Probably unaware of Verrill’s findings, Ehlers (1887) described a North American collection of extremely small (less than 21.5 mm long) worms as Onuphis gracilis, explicitly noting the resemblance to both H. tubicola and the West Indian H. varians Baird. Quite a few characters, notably the condition of the occipital antennae, the anterior setae and the absence of so-called “Augenflecke” on the largest specimen, do not agree with H. tubicola. Augener (1906) noted the existence of differences between European and American worms, particularly the absence of “eyes” and the location of gills, but nevertheless synonomized both H. artifex Verrill and O. gracilis Ehlers with H. tubicola (O. F. Miller). He believed that the differences could be attributed to size. Since Verrill’s discovery of a North American quill worm, other animals identified as H. tubicola have been dredged from all of the world’s major seas except the Antarctic Ocean. The species is often cited as an example of the cosmopolitan fauna of the deep sea (Ekman, 1953). The concept of a single faunal assemblage com- prised largely of cosmopolitan species inhabiting the depths of oceans throughout the world is currently being questioned due to the elucidation of distinct faunas in different regions (Sanders, Hessler and Hampson, 1965). Nonetheless, there remains a sizable group of species such as H. tubicola that have been so widely re- ported that they are considered cosmopolitan. We have investigated American and European representatives of this species in hopes of clarifying the basis of morphological differences noted by earlier workers. Diagnoses of morphological, physiological and molecular characters will be presented in evidence. This paper is restricted to a morphological comparison of three populations, one European and two North American. All animals in our own collections were removed from their TAXONOMIC STATUS OF HYALINOECIA 3 tubes prior to preservation in 70% ethyl alcohol. This precaution not only facilitates preservation but also prevents autotomy of the tail region and distortion of the body. We made no special effort to insure against bias for size; the measurements given are intended to portray the samples on which our results are based, not the natural populations. The error is probably not large, but small worms are easily overlooked in shipboard sorting, and a few of the largest were discarded from the European sample because they did not fit the mailing containers. RESULTS European worms Hyalinoecia tubicola (O. F. Miller, 1776) Ayalinoecia tubicola Quatrefages, 1865; Grube, 1878; Langerhans, 1880; Fauvel, 1923; Stép-Bowitz, 1948. More than 300 specimens were collected by R/V Sula of the Marine Biological Association of the United Kingdom in the sum- mer of 1967. The worms originated from depths of 44 to 55 meters in the English Channel (50° 15-17’ N, 4° 20-30’ W). Excluding tentacles and terminal cirri, the size range of the animals was 35— 130 mm (Fig. 1A). The quill-like tubes of the species, a few cm longer than their inhabitants, were described by Watson (1903). DESCRIPTION OF MATERIAL COLLECTED. Prostomium bulbous, bearing five occipital antennae with annulate (3—4 rings) cerato- phores, and two stout, short frontal antennae without ceratophores. Three dorsomedial occipital antennae of equal length, twice as long as more lateral pair (Fig. 166i in Fauvel, 1923), and extending posteriorly as far as setigerous segment XVI. Two dark pigment spots (often designated “eyes” in the literature) occurring lateral to the bases of the dorsomedial paired occipital antennae. Ventrally two large globose palps forming the upper border of the mouth. Buccal segment dorsally forming an achaetous ring at the base of the prostomium. Mouth located ventrally, with reniform lower lip and two protruding wing-shaped mandibles. Four pairs and one unpaired dark maxillae (Fig. 88 in McIntosh, 1885). Maxillae I hooked forceps. Right maxilla II typically with 13-14 teeth (range 4 POSTILLA A HYALINOECIA TUBICOLA JUNE 1967 H. ARTIFEX APRIL 5,1967 FREQUENCY (%) fo) H. ARTIFEX MARCH 4, 1967 10 5 0 PERSPRSRSESSESTHSL ZPAaSLSRBSRBRS 644464486 SS ee eos LENGTH (MM.) FIG. 1. Size distribution in sample of quill worms. A. English Channel. B. and C. North American continental slope (420—480 m). TAXONOMIC STATUS OF HYALINOECIA 5 10-15); left maxilla If with 12 (11-14) teeth. Right maxilla III absent; left maxilla II] with 13 (12-14). Right maxilla IV with 10 (10-11); left with 13 (12-14). Each right and left maxilla V with | tooth only. Setigerous segment I smooth dorsally, longer than succeeding segment. Parapodia enlarged, directed anteroventrally. Dorsal para- podial cirri about same size as on segment II; ventral cirri slightly larger than on II. Presetal lobe somewhat fan-shaped (enlarged distally) covering the bases of typically 3 (2—6) stout tridentate acicula (Fig. 2A). Postsetal lobe cirriform, about one-half as large as on setiger II. Setigerous segment II shorter than I. Parapodia smaller, more conical and directed ventrally. Presetal lobe spatulate, covering bases of 2—4 bilimbate capillary setae (Fig. 2D in Claparede, 1868) which are noticeably stouter than in succeeding segments, 2—4 stout tridentate acicula and a small clump of pectinate setae. Postsetal lobe more closely applied to fascicle, less conical, and more lobulate than on I. Setigerous segment III closely resembling II though slightly smaller. Dorsal and ventral parapodial cirri slightly smaller than on II, beginning posterior gradation in size. Limbate capillary setae A SSS 0o.1 mm . eae a + 0.1 mm FIG. 2. Hyalinoecia tubicola (O. F. Miller). English Channel. A. Tridentate aciculum from setiger I. B. Hooded bidentate aciculum from bran- chial region. 6 POSTILLA up to 11; clump of pectinate setae in dorsal portion of fascicle. Emergent acicula lacking. Setigerous segment IV with several pectinate setae (Fig. 166n in Fauvel, 1923) as well as limbate capillaries. Ventral cirrus short, globose, becoming a flattened cushion by setiger V and persisting as such for rest of body length. Presetal lobe diminishing to rudi- mentary lip on branchial segments. Postsetal lobe diminishing to rudimentary lobe, then disappearing by setiger XXXV. Branchiae flattened, beginning typically at setiger XXIV (XXIII to XXV) and subsequently increasing in length up to or more than two-thirds the body width. Dorsal parapodial cirri simultaneously decreasing to a fine filament about one-tenth the length of the branchial filaments. Number of limbate setae increasing to maximum of 14 per fascicle between setigers IX to XXV. Single hooded bidentate aciculum (Fig. 2B) appearing in the middle of the fascicles at about setiger XXV (XX to XXVIII), increasing to typically 2-3 (up to 5) more posteriorly. Hooded bidentate aciculum notched imme- diately proximal to teeth, which are directed at acute angle to main axis of seta (Fig. 2B). Number of limbate capillary setae decreasing to 9 or less per fascicle in the midbranchial region. Pectinate setae present on all but setiger I. Three stout, tapered, hooded acicula present internally in all parapodia but typically not emerging. Posterior region becoming flattened, ending in large pygidium with two fragile terminal cirri. Last few segments without branchiae but with dorsal cirri and all setae types (in reduced numbers). Material deposited in the Peabody Museum, Yale University, YPM No. 2694. North American worms Hyalinoecia artifex Verrill 1880 Hyalinoecia artifex Verrill, 1885a; Verrill, 1885b. Onuphis (Paronuphis) gracilis Ehlers, 1887. Hyalinoecia tubicola Augener, 1906; Hartman, 1944; Pettibone, 1963. We have collected thousands of specimens from the Atlantic continental slope at 420—480 meters depth, 34° 16’ N, 75° 48’ W. The collections were made on cruises on R/V Eastward of the TAXONOMIC STATUS OF HYALINOECIA 7 Duke University Marine Laboratory in the period 1965-68. The description below summarizes our examination of several hundred worms ranging in length from 15 to 180 mm (Figs. 1B and 1C). The morphology is stable after the worms reach a length of approxi- mately 20 mm, but quite plastic in smaller animals. The description pertains to worms exceeding 20 mm; a few notes on juvenile speci- mens follow at the end. DESCRIPTION OF MATERIAL COLLECTED. Prostomium bulbous (Fig. 3A), bearing five occipital antennae with annulate (3—4 rings) ceratophores and two short, stout, frontal antennae without cerato- aan, \ «1 Eps =. S Y); SRI ERC -— 1 mm — 0.1 mm FIG. 3. Hyalinoecia artifex Verrill, continental slope (420-480 m). A. An- terior region, dorsal view. B. Blunt aciculum from setiger I. C. Hooded bidentate aciculum from branchial region. 8 POSTILLA phores. Three dorsomedial antennae of equal length, about 3—4 times the length of the more lateral pair (Fig. 178 in Verrill, 1885b) and extending as far posteriorly as setiger XXX. Prostomium of adult worms invariably without dark pigment spots (see notes on juvenile specimens below). Ventrally two large globose palps form- ing upper border of mouth. Buccal segment dorsally forming achaetous collar at base of the prostomium. Mouth located ventrally, with reniform lower lip and two protruding wing-shaped mandibles. Four pairs and one un- paired maxillae; Maxillae I hooked forceps; right maxilla II with 13 (10-15) teeth; left with 14 (11-16). Right maxilla HI absent and left with 13 (11-15) teeth. Right maxilla IV with 12 (9-14) and left with 10 (8-12). Each maxilla V with 1 tooth only. Setigerous segment I smooth dorsally, longer than succeeding segment. Parapodia enlarged, directed anteroventrally: Dorsal and ventral parapodial cirri smaller than on setiger II. Presetal lobe somewhat fan-shaped (enlarged distally) covering bases of 3-4 stout, smooth-tipped acicula (Fig. 3B). Postsetal lobe cirriform, about one-half as large as on setiger II. Setigerous segment II slightly shorter than I. Parapodia smaller and more conical than on IJ, directed ventrally. Dorsal and ventral cirri larger than on I. Presetal lobe spatulate, covering bases of 3—4 stout acicula, 3—4 stout mono- and bilimbate capillary and small clump of pectinate setae. Postsetal lobe closely applied to fascicle. Setigerous segment III slightly smaller than II. Dorsal cirri longer than on IJ; ventral parapodial cirri smaller than on I, be- ginning to diminish and becoming very small in mid-branchial region (see below). Presetal lobe a small tongue, beginning to diminish. Postsetal lobe similar to that on IJ, but beginning to diminish. Limbate capillary setae up to 10; clump of pectinate setae in dorsal portion of fascicle. Emergent acicula lacking. Setigerous segment IV with slightly smaller parapodia than III; parapodia diminishing to roughly constant size by VII. Pectinate setae present, as well as limbate capillaries. Ventral cirrus short, globose, becoming a flattened cushion by VII. Presetal lobe grading to rudimentary lip by setiger X and persisting as such posteriorly. Postsetal lobe beginning gradation to rudimentary lobe by setiger L. Branchiae simple, flattened, beginning typically at setiger XXIX (XXVI to XXXIII); length up to but not exceeding two-thirds of TAXONOMIC STATUS OF HYALINOECIA 9 body width. Dorsal parapodial cirrus decreasing to fine filament at base of branchiae and about one-eighth the length of the branchial filament; dorsal cirrus becoming somewhat larger again in post- branchial region. Maximum number of limbate setae about 16, occurring between setigers XV and XL. Single hooded bidentate aciculum appearing in center of fascicle between setigers XXIV and XLV, increasing to 2 (uncommonly 3) in more posterior segments; hooded acicula not notched, with teeth directed parallel to main axis (Fig. 3C). Number of limbate capillary setae decreasing to maximum of 12 in mid- branchial region. Pectinate setae present on all but setiger I. Three stout, tapered, hooded acicula present internally on all parapodia but typically not emerging. Posterior region becoming flattened, ending in small pygidium with two fragile terminal cirri. Last few setigerous segments with- out branchiae but with dorsal cirri and setae (reduced numbers). Maximum segment number about 200. Material deposited in the Peabody Museum, Yale University, YPM No. 2695. We have also examined forty individuals from the same popula- tion between 12 and 25 mm in length. The two smallest specimens (12 mm) show striking morphological deviations from larger mem- bers of the species (greater than 20-25 mm). Most striking is the enlarged condition of dorsolateral antennae (Fig. 4) and the very short condition of other occipital antennae. Many of the remaining small worms (12—25 mm) show a transitional condition for this character. Another interesting deviation found in the smallest worms is the absence of demarcation between the buccal segment and the first setiger. Two somewhat larger specimens of the forty examined had distinct prostomial pigment spots very much like those found on all specimens of H. tubicola. Comparing the mor- phological characters of these very small worms with those at- tributed by Ehlers (1887; see Fig. 6) to North American worms, we believe that he described as Onuphis gracilis an intermediate condition between juvenile and adult forms of H. artifex Verrill. Hyalinoecia sp. Finally, we have examined 50 specimens obtained by Dr. Gilbert Rowe at 33° 59’ N, 75° 46’ W. This station is very close to the 10 POSTILLA FIG. 4. Hyalinoecia artifex Verrill, continental slope (420—480 m). Anterior region of a worm 12 mm in total length, dorsal view. previous one on the Atlantic continental slope, but at the consid- erably greater depth of 1125-1350 meters. The taxonomic status is particularly interesting because horizontal belts of quill worms are found at the two depths but not in between (Rowe, 1968). DESCRIPTION OF MATERIAL COLLECTED. Prostomium bulbous, bearing five occipital antennae with annulate (3—4 rings) cerato- phores, and two stout, short, frontal antennae without ceratophores. Three dorsomedial occipital antennae 3—4 times the length of the lateral pair. Unpaired median antenna extending as far as setiger XXVI; paired dorsomedial antennae extending as far as segment XIX. Single median antenna consistently longer. Prostomium with- out dark pigment spots. Ventrally two large globose palps forming the upper border of mouth. Buccal segment dorsally forming an achaetous ring around base of prostomium. Mouth located ventrally with reniform lower lip and two protruding wing-shaped mandibles. Four pairs and one unpaired dark maxillae. Maxillae I hooked forceps. Right and left maxillae If with 12 (10-14) teeth. Right maxilla HI absent; left with 8 (6—10) teeth. Right maxilla 1V with 8 (6-13) teeth; left with 8 (6-11). Both right and left maxillae V without teeth, rudimentary. Setigerous segment I very large, longer than succeeding segment. Parapodia enlarged, directed anteroventrally. Dorsal and ventral TAXONOMIC STATUS OF HYALINOECIA 11 cirri about same as on segment II. Presetal lobe fan-shaped (en- larged distally), covering bases of 2—4 stout, tapering acicula. Postsetal lobe small (one-half the size as on II), cirriform. Setigerous segment II about two-thirds the length of I; parapodia smaller, more conical and directed ventrally. Dorsal and ventral cirri about the same size as on I. Presetal lobe somewhat spatulate covering bases of about 8 stout limbate and several pectinate setae. Postsetal lobe considerably larger than on I, more conical. Setiger III about three-fourths the length of II. Setiger IV about three- fourths the length of III, slightly larger than other body segments of the anterior and mid-regions. Branchiae simple, flattened, beginning typically on setiger XX (XIX to XXII). Branchiae less than two-thirds width of body. Limbate setae increasing to about 24 per fascicle in prebranchial segments. Emergent bidentate acicula appearing about setiger XXVIII, and increasing to two in posterior segments. Hooded acicula resembling those of H. artifex. Three stout, tapered, hooded acicula present internally on all parapodia but typically not emerg- ing. Posterior region missing. Pectinate setae present in all but setiger I. Material deposited in the Peabody Museum, Yale University, YPM No. 2696. DISCUSSION Shallow-water North American quill worms differ from their European relatives by the following morphological characters: 1) allometry of dorsomedial occipital antennae relative to lateral occipital antennae as well as to body segments; 2) allometry of median occipital antenna relative to paired dorsomedial antennae; 3) virtually complete absence of prostomial pigment spots; 4) aden- tate condition of acicula on anterior setigers; 5) morphology and smaller number of hooded bidentate acicula in branchial and mid- regions; 6) more posterior position of branchiae; 7) larger numbers of capillary and pectinate setae; 8) allometry of pygidium relative to body; 9) allometry of dorsal cirri relative to branchial filaments in mid-region. North American worms differ from their European relatives by a number of other characters, the importance of which is difficult to assess. Some of these differences may arise from handling or 12 POSTILLA method of preservation; others, although undoubtedly natural, are of minor significance. The differences include: 1) allometry of frontal antennae; 2) disappearance of postsetal lobe on different setigers; 3) number of teeth on maxillae; 4) allometry of dorsal and ventral parapodial cirri on first and second setigerous seg- ments; 5) larger mean size and segment number. It should be em- phasized that these differences occur in worms of the same overall Size: The two North American populations also consistently differ from one another in: 1) number of limbate setae per fascicle; 2) allometry of occipital antennae relative to one another and to the body; 3) appearance of gills on different segments; and 4) rudi- mentary condition of maxillae V. While the absence of posterior ends prevents a quantitative size comparison, the lower slope specimens are approximately the same diameter. There are addi- tional differences that we believe attributable to preservation of the lower slope specimens without prior removal from the tube. Because of the poor preservation and the absence of complete specimens from the greater depth, we do not consider our mor- phological comparison adequate. It is included here to call atten- tion to possible morphological divergence correlated with the interesting ecological separation. In conclusion, the differences between North American and European worms that were noted by Augener (1906) do exist; moreover, there are additional morphological differences. Contrary to the conclusion of Augener (1906), the differences are consistently found in worms of the same size. Since the synonomization is not supported by either evidence or well-founded argument, it seems reasonable to recognize Verrill’s (1880) species Hyalinoecia artifex as distinct from the European form H. tubicola (O. F. Miller). ACKNOWLEDGMENTS This work was supported by research grants NSF GB-5563 and GB-6884 from the National Science Foundation. We are grateful to Drs. Meredith L. Jones and J. L. Simon for their criticisms of the manuscript. TAXONOMIC STATUS OF HYALINOECIA 13 LITERATURE CITED Augener, H. 1906. Westindische Polycheten. Bull. Mus. Comp. Zool. 43: 91-196. Claparede, E. 1868. Les annélides chétopodes du Golfe de Naples. Mém. Soc. Phys. 19: 313-584. Ehlers, E. 1887. Report on the annelids of the dredging expedition of the U.S. coast survey steamer Blake. Mem. Mus. Comp. Zool. 15: 1-335. Ekman, S. 1953. Zoogeography of the sea. Sidgwick and Jackson, Ltd. London, 417 p. Fauvel, P. 1923. Faune de France. 5. Polychetes errantes. 488 p. Grube, A. E. 1878. Systematische Untersuchungen Uber die Familie Eunicea. Jahresber. Schles. Gesell. f. Vaterland Kult. 55: 79-104. Hartman, O. 1944. New England Annelida. Part 2. Bull. Amer. Mus. Nat. Hist. 82: 327-344. Langerhans, P. 1880. Die Wurmfauna von Madiera. Zeits. wiss. Zool. 33: 267-316. McIntosh, W. C. 1885. Report on the Annelida, Polychaeta collected by H. M. S. Challenger during the years 1873—76. Challenger Reports 12. 554 p. Miller, O. F. 1776. Zoologiae Danicae prodromus, seu animalium Daniae et Norvegiae. 274 p. Pettibone, M. H. 1963. Marine polychaete worms of the New England region. I. Aphroditidae through Trochochaetidae. U.S. Nat. Mus. Bull. 227. 356 p. Quatrefages, A. de. 1865. Histoire naturelle des annéles marins et d’eau douce. Annélides et géphyriens. Libr. Encycl. de Roret I. 588 p. Rowe, G. T. [MS.] Distribution patterns in populations of large, deep-sea benthic invertebrates off North Carolina. Ph.D. dissertation, unpubl. 1968, Duke University, Durham, North Carolina. 296 p. Sanders, H. L., R. R. Hessler and G. R. Hampson. 1965. An introduction to the study of deep-sea benthic faunal assemblages along the Gay Head Bermuda transect. Deep-Sea Res. 12: 847-867. Stép-Bowitz, C. 1948. Polychaeta from the Michael Sars North Atlantic deep-sea expedition, 1910. Rep. Sci. Results Michael Sars North Atlantic Deep-Sea Exped. 1910.5 (8). 91 p. Verrill, A. E. 1880. Notice of recent additions to the marine Invertebrata, of the northeastern coast of America, with descriptions of new genera and species and critical remarks on others. (Pt. II). Proc. U.S. Nat. Mus. 3: 356-405. 1885a. Results of the explorations made by the steamer A/batross off the northern coast of the United States in 1883. Rep. U.S. Fish Comm. for 1883: 503-699. 1885b. Notice of recent additions to the marine Invertebrata of the northeastern coast of America, with descriptions of new genera and species and critical remarks on others. (Pt. V). Proc. U.S. Nat. Mus. 8: 424-448. Watson, A. T. 1903. Observations on the habits of the Onuphidae (Poly- chaeta), and on the internal structures with which they fortify their homes. Proc. Trans. Liverpool Biol. Soc. 17: 303-318. 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