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VERMETID GASTROPODS FROM SAO MIGUEL, AZORES: COMPARATIVE ANATOMY, SYSTEMATIC POSITION AND BIOGEOGRAPHIC AFFILIATION

Rildiger Bieler

Center for Evolutionary and Environmental Biology, Field Museum of Natural History, Chicago, Illinois 60605, U.S.A.

ABSTRACT Two vermetid species inhabit the intertidill and upper subtidal rocky

shores of Sao Miguel, Azores. The larger-shelled species, identified as Vermetus cf. triquetrus Bivona-Bernardi, 1832, has highly variable shell characters, spanning previously assumed diagnostic features of several nominal genera. The smaller form is recognized as Thylaeodus cf. rugu­losus Monterosato, 1878, a species previously deemed restricted to the Mediterranean. Females of both species brood their eggs in stalked capsules attached to the interior shell wall. After feeding on nurse eggs, juveniles are released at the crawling stage and attach to suitable sub­stratum. Neither form is known to date from the western Atlantic, and colonization of the mid-Atlantic Azores by these vermetids is hypothe­sized as passive long-distance dispersal by "rafting" from an eastern Atlantic/Mediterranean source. A lectotype is selected for nominal spe­cies Vermetus rugulosus Monterosato, 1878 (Museo Civico di Zoologia, Rome). The commonly used name "Vermetus triqueter" is dismissed as an incorrect subsequent spelling of Vermetus triquetrus Bivona-Bernar­di, 1832.

RESUMO Duas especies de vermetfdeos habitam o intertidal e subtidal superior

das costas rochosas de Sao Miguel, Ayores. A especie de concha maior, identificada como Vermetus cf. triquetrus Bivona-Bernardi, 1832 possui caracteres conquiliol6gicos altamente variaveis, abrangendo varios gene­ros nominais caracterfsticas antes tidas como diagnosticantes. A forma menor e reconhecida como Thylaeodus cf. rugulosus Monterosato, 1878, especie previamente tida como restricta ao Mediterraneo. As femeas de ambas as especies incubam os ovos em capsulas pedunculadas fixas a pa­rede interior da concha. Depois de se alimentarem de ovos de criayao, os juvenis sao largados na fase rastejante e fixam-se a um substrato adequa­do. Ate a data nenhuma das formas e conhecida do Atlantico oeste, e avanr;a-se a hip6tese que a colonizayao dos Ar;ores no meio do Atlantico por estes vermetfdeos fez-se por dispersao passiva a longa distancia por meio de "jangada" a partir de uma origem do Atlantico leste/Mediterra­neo. E seleccionado um lectotipo para a especie nominal Vermetus rugu­losus Monterosato, 1878 (Museo Civico di Zoologia, Rome). 0 nome co­mummente utilizado "Vermetus triqueter" e abandonado por ser uma soletrar;ao incorrecta subsequente de Vermetus triquetrus Bivona­Bernardi, 1832.

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INTRODUCTION

Vermetidae (Caenogastropoda: Vermetoidea incertae sedis) is a gastropod family whose members are highly modified snails, adapted to a sessile life mode. Their irregularly coiled and frequently corroded shells, which in the postlarval stage are firmly cemented to rock or other hard substrate, resemble those of serpulid polychaete worm tubes. The animals collect food from the surrounding seawater by ciliary action or by producing particle­trapping mucus strands which are then ingested (e.g., Boettger, 1930). Generic or specific identification from empty shell tube fragments (which is the usual condition of his­toric vermetid collection material) is often impossible. Although it con­tains common members of many tem­perate to tropical rocky shore com­munities, the group has remained poorly studied. The high variability of shell features defeats attempts to apply "standard" gastropod shell characters for descriptive and iden­tification purposes. This, and the difficulty in collecting (preferably by hammer and chisel; often from the under-sides of rocks and boulders in the surf zone and in deeper water) have excluded them from many stu­dies of molluscan communities.

Field work for the present study concentrated on the intertidal and upper subtidal (SCUBA depth) rocky shore of Sao Miguel, mostly in the vicinity of Vila Franca do Campo and on Ilh6u de Vila Franca, a small

island formed by a drowned volcanic crater (B. Morton, 1990).

Although now known to be com­mon, the vermetids of Sao Miguel are relatively small and inconspicuous, and were not mentioned in the more general descriptions of local inter­tidal habitats and ecology (Arruda & Gordo·, 1984; B. Morton, 1990; Hawkins et al., 1990).

Several morphotypes ultimately determined to represent two verme­tid species were found in the study area. Comparative sampling of the rocky shore at the far north-eastern end of Sao Miguel, near Mosteiros, resulted in the collection of the same two species. The larger-shelled one is the form previously referred in the Azorean literature to Vermetus t riq u e te r (V. cf. t riq ue t rus in this work). The smaller one is a new record for the Azores, and here is called Thylaeodus cf. rugulosus Monterosato, 1878. Morphological and anatomical characters of the two species, as well as aspects of their reproductive biology will be com­pared.

The known range of reproductive strategies in the family Vermetidae includes brooding of very small clutches resulting in crawl-away larvae as well as brooding of egg masses releasing numerous plankto­trophic larvae that facilitate wide geographic dispersal (Hadfield et al .• 1972). The isolated position of the mid-Atlantic Azores poses interest­ing questions of the geographic ori­gin of its fauna and flora (see, e.g., Gofas, 1990; Prud'homme van Reine,

BIELER: VERMETIDAE OF THE AZORES 175

1988). For the Vermetidae, the question is here whether the local species can be recognized as part of the eastern Atlantic/Mediterranean fauna, whether they are part of the western Atlantic vermetid fauna (currently under rev1s1on by the present author). or whether they re­present endemic forms of the Azores.

MATERIALS AND METHODS

During two weeks in July and Au­gust of 1991, living specimens were collected on Sao Miguel by wading, snorkling and SCUBA diving. The snails were removed from overturned rocks and boulders in 0.1-10 m depth of water, using a knife blade or hammer and chisel. Some speci­mens were collected with shell hash in 20 m depth, employing a suction device attached to a SCUBA air tank. Animals were transferred to the workshop laboratory in Vila Franca do Campo on Sao Miguel, where they were measured, observed and sketch­ed under a dissecting microscope and prepared for further study. Measurements were taken with cali­pers or by using calibrated eye­pieces on the dissecting microscope. Photographs were taken with stan­dard 35 mm equipment and macro­lenses. For selected listings of ma­terial examined, see individual spe­cies descriptions, below.

Animals were anestethized by placing menthol crystals on the water surface of finger bowls hou­sing the specimens. Soft-bodies and brooded egg masses were removed

from the shell after cracking with a small vice. Soft-parts were measured in the "relaxed" state and their gross anatomy studied using a dissecting microscope. For histolo­gical studies, specimens were rela­xed in MgCl2 solution isotonic with seawater and chemically fixed in either 5% buffered formalin or Bouin's solution. On return to the home laboratory at FMNH, specimens were embedded in paraplast, sec­tioned at 7-8 µ m and stained with Alcian B 1 ue/Periodic-Acid-Schiff (PAS) and/or Hematoxylin/Eosin. Radular ribbons and jaws were ex­tracted by dissolving the surround­ing tissue in 10% KOH solution at room temperature for 24 hours, with subsequent washing in distilled wa­ter. Air-dried shells, radulae, jaws, and opercula were coated with gold, and observed and photographed using an AMRA Y 1810 scanning e­lectron microscope at Field Museum. Nomenclature for radular characters follows the outline given by Bandel (1984: Figs. 1-3).

Preserved Azorean specimens were compared with freshly collect­ed western Atlantic vermetids at the Smithsonian Marine Station at Link Port, Ft. Pierce, Florida, U.S.A., in March of 1992. For comparison with Mediterranean material, specimens in the Monterosato Collection, Museo Civico di Zoologia, Rome, Italy, were studied in August of 1992. Pre­viously reported Azorean vermetid specimens (Dautzenberg, 1889; 'Hi­rondelle' cruise of 1887; Mu see Oceanographique de Monaco) were

176 A<;OREANA SUPPLEMENT 1995: 173-192

examined on loan. Abbreviations used in text ('*'

denotes institutions where voucher material was deposited):

*FMNH Field Museun of Natural Histo­ry, Chicago, Illinois, U.S.A.

*HBOM Harbor Branch Oceanographic Museum, Ft. Pierce, Florida, U.S.A.

*MCZ Museum of Comparative Zoology, Harvard University, Cam-bridge, Massachusetts, U.S.A.

MC7R. Museo Civico. di Zoologia, Rome, Italy.

*MNHNP Museum National d'Histoire Na­turelle, Paris, France.

Additional voucher material will be deposited with the Museu Carlos Machado, Ponta Delgada, Sao Miguel, Azores (awaiting upgrade of museum facilities; Frias Martins, pers. comm.).

DESCRIPTIONS

Ve rm e tu s cf. tr i q u et r us Bivona-Bernardi, 1832

Figs. 1-14

?Vermetus triquetrus Bivona-Ber­nardi, 1832: 6 (Palermo, Italy; Recent)

Material studied (selected listing; all Sao Miguel, Azores; collected during 2nd International Workshop, 21 VII - 3 VIII 1991): Ponta da Piramide (37°42.?'N, 25°28.0'W), 0.5-1 m, in strong currents on sides and under-surfaces of rocks and boulders (FMNH 224921-23, 224927, 224933-37. 224939-41, 224944, 224946 [incl. sectioned specimen], 224925-26, 224930-31, 224945; MCZ 302758; MNHNP unnumbered); off Ponta da Piramide (37°42'N, 25°28'W), 5-13 m (SCUBA), on rocks (FMNH 224924, 224943, 224947); 300 m off Ponta da Piramide, 20 m (SCUBA suction device), in shell hash with red algae Antitham­nion cruciatum (C. Agardh) Nligeli (FMNH 224928; HBOM 065:03700); W of Rosto do Cao, Sao Roque, E of Ponta Delgada (FMNH 224932); Ilheu de Vila Franca (37°42.3'N, 25°26.6'W), eastern part of inside lagoon, intertidal, among coralline algal turf (FMNH 224929, 224942); Mos­teiros (37°54.0'N, 25°49.1 'W), intertidal, on sides and under-surface of rocks and boulders (FMNH 224938).

Teleoconch (descriptions based on live-taken material; for measure­ments, n=30): Coiling pattern, shell thickness, sculpture and coloration very variable. Maximum dimensions of individual adult shell mass ran­ging from 10 x 8 mm to 19 x 13 mm; maximum outside whorl diameter

FIGS. 1-7. Vermetus cf. triquetrus (Bivona-Bernardi). Sao Miguel, Azores. l, living animal, with final part of shell removed to expose head-foot area (note long pedal ten­tacles), bar=2 mm, FMNH 224930. 2, strongly-keeled morph, live-collected, greatest dimension 11.4 mm, FMNH 224930. 3, multi-ribbed morph, live-collected, greatest dimension 13.6 mm, FMNH 224932. 4, smooth (corroded) morph, live-collected, early whorls opened to expose transverse septa; greatest dimension 16 mm, FMNH 224935. 5, intertwined cluster, greatest dimension 45 mm, FMNH 224944. 6-7, surface shell sculpture (SEM): 6, early teleoconch whorl (aperture facing toward right), bar=l mm, FMNH 224928; 7, first teleoconch whorl, bar=lOO µm, FMNH 224929.

; BIELER: VERMETIDAE OF THE AZORES 177

F IGS. 1-7. Ve n11e t11 s cf. 1riq11etrus (Bivona-B ernardi ). Sao Miguel, Azores. (Legends on previous page).

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from 3.8 to 5.1 mm (x= 4.7). Coiling rarely deviates from counter-clock­wise direction, but ranges from a re­gular, tight coil (Fig. 2), or a "Tur­ritella-squashed-sideways" growth form (Fig. 3), to very loosely coiled, irregular morphs, the latter espe­cially when gregarious (Fig. 5). Shape of cross sections through whorls variable, ranging from circu­lar to depressed-oval or almost tri­angular, influenced by substrate and shell sculpture. Usually with short erect feeding tube (raising aperture 4-10 mm above surface), narrower than those whorls appressed to the substrate, with inner apertural dia­meter ranging 2.6 to 3.6 mm (x= 3.2). Some specimens with remnants of earlier feeding tubes. Without lon­gitudinal columellar lamellae, but occasionally with one or several in­ternal septa (Fig. 4). Early postlar­val sculpture of axial growth lines (Fig. 7), subsequent sculpture of 8-10 nodose longitudinal (spiral) ribs of varying thickness (Fig. 6), the outermost ones drawn out into flan­ges appressed to substrate. One rib

usually considerably stronger, form­ing an often prominent shell keel on inner "dorsum" of shell. Rib tuber­cles often scaly, coordinated into ir­regular transverse (axial) bulges. In weakly sculptured or somewhat ero­ded shells, these bulges form the on­ly discernible sculpture. Shell wall thickest at dorsal keel and lateral flanges; attached ("bottom") part of tube very thin-walled, especially on smooth surfaces. Inside of tube lined with smooth, glossy layer; brown in the adult. Juvenile shells translucent, off-white, tan or dark brown. Adult coloration also varia­ble, dark brown with dorsal keel lighter, or mottled light-tan/brown with tubercles lighter; occasionally only dorsal keel with discernible co­lor pattern, or all ribs with alterna­ting brown/off-white pattern (Fig. 1). Smooth shells often appearing gray, with inner brown shell layer shining through outer whitish layer. Shells of living snails can be strong­ly eroded, smooth and partly trans-1 ucen t, resulting in a purplish­brown (inner layer) and white (cor-

FIGS. 8-14. Vermetus cf. triquetrus (Bivona-Bernardi). Sao Miguel, Azores; SEM. 8, protoconch (725 µm in length) and early teleoconch whorls (normally attached to rock surface), with first teleoconch whorl partially opened to illustrate tight wrapping of whorls, FMNH 224941. 9, operculum, external side, 870 µm maximum diameter, FMNH 224946. 10, shell of intracapsular juvenile, after metamorphosis; apical aspect (note wavy growth marks on caplike embryonic shell), greatest diameter 640 µm, FMNH 224946. 11, shell of freshly hatched juvenile (note beginning teleoconch growth), ma­ximum dimension 760 µm, FMNH 224946. 12, shell of settling juvenile (note proto­conch umbilicus, fine spiral striation, and part of first teleoconch whorl); protoconch dimensions 815 x 680 µm, FMNH 224946. 13, radula, approximately mid-ribbon; arrow pointing to single inner flanking cusp of outer marginal tooth; bar=lOO µm, FMNH 224938. 14, fine detail of jaw surface; bar=lO µm, FMNH 224943.

; BIELER: VERMETIDAE OF THE AZORES 179

FIGS. 8-1 4. V e n11e111s cf. rr iqu errus (B ivona-Bernardi). Sao Miguel, Azores; SEM (Legends on previous page).

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roded outer layer) shell (Fig. 4). Shells often fouled by numerous or­ganisms, especially coralline algae, sponges and barnacles.

Protoconch: Globular shell, with a little over 1 2/3 whorls; maximum shell length 720-815 µ m, diameter 600-680 µ m; embryonic part cap­shaped, with wavy growth lines (see Fig. 10); larval shell (comprising approximately final full whorl) in­flated, with faint spiral riblets (es­pecially · n~ar protoconch umbilicus). No noticeable growth between hatch­ing of crawl-away larva (see below) and settlement (compare Figs. 8, 10-12). Translucent off-white to light tan, with suture darker.

Operculum: Round, slightly con­cave, 700-870 µ m in adult speci­mens, about 1/5 to 1/3 of relaxed pedal disk diameter; exposed side with edge of earlier whorls rising as free-standing lamella along suture of final 1.5 whorls (edge rolling inward in dry specimens; see Fig. 9); horny, transparent.

Radula (Fig. 13): Regularly tae­nioglossate; transparent, largest specimens with some horn-colored staining; consisting of 25-30 rows of teeth (for counts and dimensions: n= 15, from specimens with maxi­mum shell mass dimensions of 12-19 mm; no difference noted between sexes or between specimens from different localities on Sao Miguel).

Total length of (artificially straightened) radular ribbon 1.8-2.4 mm, width (mid-ribbon, marginal teeth not folded outward) 340-440 µ m. Radular configuration agreeing

with general description of vermetid characters given by Bandel (1984: 44-46) and the sketch for "Bivonia triquetra" (see Bandel, 1984: fig. 51 ). Trapezoidal rachidian tooth with strong main cusp and 4-5 flanking cusps on either side (redu­cing in size outwardly); basal denti­cles strongly developed. Inner mar­gin of lateral tooth fitting into deep marginal depressions of rachidian tooth; cusp arrangement on triangu­lar cutting edge as in central tooth. Marginal teeth long, slender, with long and strong main cusp. Inner marginal with 1 flanking cusp on in­side, 2-3 on outside. Outer margi­nal with single inner flanking cusp, smooth on outside. Indicated varia­tion in numbers of flanking cusps may occur between left and right sides of same radula.

Jaws: Elongate bean-shaped; attached to transparent cuticula; lightly tan-colored cutting area con­sisting of small (5 x 10 µm) oblique­ly quadrangular subunits (Fig. 14); maximum jaw dimensions 800x300 µm

Anatomy: Animal (removed from shell) serpentine, large specimens to 30 mm in (relaxed) length, 3.5 mm in width; long posterior lobe of diges­tive gland and gonad occupying at least half its length. Columellar muscle a long ·narrow strip with a deep insertion in the shell _(animal capable of retreating deeply into shell). Pedal tentacles long, extre­mely slender and tapered (Fig. 1 ), in fully extended position with right tentacle longer than left (e.g., 5.0 vs.

-'

...

BIELER: VERMETIDAE OF THE AZORES 181

4.3 mm); ciliated groove running along mesial side as far as tip, di­verging from the median opening of very large pedal gland. Sole of foot small and ovoid, between and ante­rior to pedal tentacles. Large and bulbous head with short tentacles (ca. 0.80 mm in living adults). Head with no trace of deepened or flatten­ed food tract. Pallial skirt of brood­ing females deeply incised in the dorsal midline. Gill extending full length of mantle cavity, approxima­tely 14 fifaments per mm in large specimens; anteriormost filaments very short, quickly increasing to average adult length of 800 µ m ; filaments forming small triangles, somewhat taller than wide. Extensi­ve area of hypobranchial gland left entirely uncovered by small gill. Osphradium vermiform (about 2.4x0.24 mm in large specimens), beginning somewhat anterior to gill filaments. Nervous and alimentary systems not studied in detail; fecal pellets ovoid, about 900x320 µ m . Female capsule gland not running the length of mantle cavity, but forming ovoid, ventrally slit pouch (as described by J.E. Morton, 1965: 609-611).

Soft-body coloration: Adult colo­ration: head-foot including pedal disk usually appearing brown-black; darker-shelled animals also with darker body pigmentation; pedal disk yellowish, mottled orange, black and white, with some orange granules more deeply embedded in tissue; upper rim (toward snout) of pedal disk with four evenly spaced

black dots; forehead with fine black and orange coloration, appearing brown; forehead and lightly-orange lateral concave regions of head with white "tiger-stripe" pattern; snout with orange, black and white pig­ment; cephalic tentacles whitish, with some fine black surface pigment and orange granules embedded with­in; rims of cephalic tentacles and sole of foot white; pedal tentacles translucent, with embedded yellow­white and/or orange bodies and with yellow tips, in some specimens also with sparse black pigment; lower part of foot orange-yellow to bright orange with greenish iridescence, and some black pigment; outside of mantle appearing brightly orange, pigments consisting of yellow, gra­nular orange, and white; mantle edge with alternating pattern of black and whitish-orange; inside of mantle yellow and orange. Young post-larva without dark body pigment, only some white at mantle margin and on anterior foot; after reaching about 1/2 teleoconch "whorl," with fine black pigment on head-foot and sparse orange spots on mantle.

Eggs and development: 5-9 egg capsules brooded in mantle cavity, arranged in single, occasionally dou­ble, row (second row started after completion of first); capsules attach­ed by stalks passing through mantle slit to interior lining of shell; ter­minal capsule stalk 400-500 µ m in length, attaching at one smaller end of oval egg capsule; capsule dimen­sion approximately 11OOx1600 µ m to 1500x1600 µm; in early develop-

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mental stages often more rounded. Egg capsules apparently deposited over a period of time, oldest (most developed) closest to shell aperture [a single clutch contained· 5 capsules with early cleavage stages, 2 with developing embryos, and with veligers and crawling stages]. Yolk yellowish-white; developing em­bryos/larvae feeding on nurse eggs, with 5-14 developing larvae per capsule; velar lobes resorbed during intracapsular metamorphosis to crawling stage; crawling stage with 2 black eye spots, long cephalic ten­tacles, agile foot (anterior foot and cephalic tentacles · heavily . ciliated); anterior part and sole of foot of pre­hatching animal with fine black pig­ment; shell transparent, light-tan, with suture and columella somewhat darker brown.

Habits/habitat: Attaching to more-or-less smooth patches of volcanic rock; usually singly or in pairs, occasionally in clusters at­taching to each other. Juveniles often settling on mother shell. Not actively corroding into substratum. Feeding by mucus-net trapping.

Specific identity: The name "Vermetus triqueter" has been used for Azorean records (Dautzenberg, 1889; .Drouet, 1858: 26, who erro­neously credited it to Linne). Bivo­na-Bernardi (1832: , 6) introduced the name as Vermetus triquetrus, using the correctly formed Latin suffix -q u et r us meaning angled, cornered, or sided. Philippi ( 1836: 170) changed this name to Vermetus triq ue te r, an incorrect subsequent

spelling without nomenclatural status (ICZN Art. 33[c]) in use ever since.

Vermetus triquetrus Bivona-Bernardi, 1832, was originally de­scribed from Palermo in the Medi­terranean, and has subsequently been cited for the Atlantic and Me­diterranean coasts of the Portuguese mainland (e.g., Nobre, 1936; Sal­danha, 1979). The taxonomy of Me­diterranean Vermetidae is still in a state of confusion, and the systema­tics of the Mediterranean members of the triquetrus-complex poses ques­tions beyond the scope of the present study. The last monograph on the subject was published by Monterosa­to ( 1892) who expanded on the earlier works of Bivona-Bernardi ( 1832) and Morch (papers spanning 1859-1871), but like most of his predecessors, Monterosato concen­trated on naming numerous nominal species and "varieties" based on teleoconch characters alone. Some authors (e.g., Morch, 1871) suggested conspecificity of the nominal species Vermetus triquetrus and V. semisur­rectus Bivona-Bernardi, 1832, while Keen (1961) placed them in separate subgenera of Vermetus. The best work available on members of the triquetrus-complex is that by Laca­ze-Duthiers ( 1860), who documented the anatomy and embryology of spe­cimens identified as Vermetus .tri­quete r and V. semisurrectus "Phi­lippi" (err. pro Bivona-Bernardi, 1832). The very detailed, study has an unfortunate flaw. Vermetus tri­quetrus was said (1860: 210) to have

; BIELER: VERMETIDAE OF THE AZORES 183

been used mainly for dissections and observations, but shells and anato­mical material had become separated during the course of that study. Lacaze-Outhier, who studied these nominal species first on Corsica and then continued his work on the Spa­nish island of Menorca, was uncer­tain about the species identity for some of his data. In addition to striking similarities of the anatomi­cal descriptions and illustrations, the developmental data for the Mediterranean forms are close to those reported here for the Azorean "cf. triquetrus." Mediterranean Vermetus triquetrus was described as having a series of 4-6 (sometimes more) egg capsules, containing 10-30 eggs each (Lacaze-Duthiers, 1860: 266; see also partial anatomical re­description by J. E. Morton [1965: 608-611] based on material from Mo­naco, and Bandel's [1984: fig. 51] sketch of radula). The Azorean spe­cies has 5-9 capsules containing 5-14 eggs each.

Previous Azorean records: Seve­ral previously published records mention the occurrence of vermetids in the Azores. Martens in Simroth (1888: 214) reported a "Vermetus sp." on the shell of a Patella species in the current study area ("Villa­franca"). In his contribution on the molluscan fauna of the Azores, Dautzenberg (1889: 43) listed two species. One, cited as Ver met us triqueter Bivona- Bernardi, 1832, is based on Drouet's ( 1858) record from Sao Miguel. Drouet (1858: 26-27) described two forms, "1 'une d'un

jaune rose, tres c6telee; 1 'autre blanchatre, moins rugueuse (peut­etre une autre espece?)," but it re­mains unclear whether he referred to two of many morphs of cf. triquetrus, or to the two species recognized in the present study.

The second Azorean vermetid spe­cies mentioned by Dautzenberg (1889: 43; from Sao Miguel and from shallow water off the island of Pico ("Lagens de Pico" [Lages do Pico], 'Hirondelle' station 108) is given as Vermetus cristatus Biondi, 1859. This nominal species was also originally described from Lhe Medi­terranean. It was subsequently (e.g., Monterosato, 1892) interpreted as a species of "Spiroglyphus" [ Dendro­poma Morch, 1861], a group not en­countered during the present study. The original material on which Daut­zenberg's (1889) "cristatus" record was based (Collections du Musee Oceanographique de Monaco, unnum­bered; vidi) consist of somewhat cor­roded shells that are here identi­fied as V. cf. triquetrus ('Hirondelle' material: 16.9 x 7.9 mm and 15.5 x }.5 mm greatest shell dimensions).

Thy la e o du s cf. rug u lo s u s (Monterosato, 1878)

Figs. 15-20

?Vermetus rugulosus Monterosato, 1878: 29 (Palermo, Italy).

? Vermetus ( Petaloconchus?) rugulo­sus, Monterosato, 1892: 2, pl. I, fig. 8.

Material studied (selected listing; all Sao Miguel, Azores; collected during 2nd

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International Workshop. 21 VII - 3 VIII 1991): Ponta da Pirimide (37°42.7'N. 25°28.0'W). 0.5-1 m. in strong currents on sides and under-surface of rocks and boulders (FMNH 224951-53); . 300 m off Ponta da Piramide (37°42'N. 25°28'W). 20 m (SCUBA suction device). in shell hash with red algae Antithamnion cruciatum (C. Agardh) Niigeli (FMNH 224949); Ilheu de Vila Franca (37°42.3'N. 25°26.6'W). eastern part of inside lagoon. intertidal. among coralline algal turf (FMNH 224950); Ilbeu de Vila Franca, inside lagoon. 1.5 m, under-surfaces of rocks (FMNH 224954-57; HBOM 065: 03701; MCZ 302759; MNHNP unnumbered); Mosteiros (37°54.0'N. 25°49. l 'W). intertidal, on sides and under-surface of rocks and boulders (FMNH 224948).

Teleoconch (descriptions based on live-taken material; for measure­ments. n=15): Maximum dimensions of individual adult shell masses ranging from 4.0 x 2.5 mm to 7 .8 x 5.3 mm; maximum outside whorl diameter ranging from 1.2 to 1.9 mm (x= 1.6). Coiling counter-clockwise, usually very irregular, but rarely forming open loops; spreading side­ways (Fig. 15). Shape of cross sections through whorls round to oval, influenced ' by subStrate and development of shell flanges. Usual-

ly with short erect feeding tube (raising aperture 1.5-2.2, rarely to 5 mm above surface), narrower than whorls appressed to the substrate, with adult inner apertural diameter normally ranging 0. 74-1.0 mm (x=0.81 ), sometimes narrowed to as small as 0.40 mm. Remnants of earlier feeding tubes usually pre­sent (Fig. 17). Without longitudinal columellar lamellae, and without longitudinal (spiral) sculpture. With distinctive, Caecum-like, transverse (axial) sculpture, con­sisting of weak axial growth lines at first, later forming smooth, more-or­less regular, closely spaced, some­what wavy axial ribs; the latter strongest in appressed drawn-out lateral shell flanges (Figs. 15, 17). Outer shell layer translucent white, inner layer in most specimens brown (in late whorls especially dark in the unattached, "roof"-forming part of the shell tube); outer layer thin in juveniles, shell thus appearing tan to dark brown, later especially ribs and flanges whitish; apertural rim often darker (showing inner layer). Inner layer in about 40% of the animals not. brown, shells thus overall translucent milk-white; early whorls of these morphs

FIGS. 15-20. Thylaeodus cf. rugulosus (Monterosato), Sao Miguel, Azores; SEM. 15, entire shell. taken from living animal (Q ), bar=l mm, FMNH 224956. 16, operculum. external side. diameter 800 µm. FMNH 224953. 17, early teleoconch whorls, with part of whorl, removed (dashed line) to expose protoconch; arrow pointing to remnant of early feeding tube; same specimen. as in Fig. 15. 18, protoconch (730x390 µm), same

specimen as in Fig. 15. 19, radula (Q ). approximately mid-ribbon; ribbon-width 150 µm, FMNH 224953. 20. as in previous figure.· with outer marginal tooth folded out­ward to expose inner flanking cusps (arrow).

l

~ I

BIELER: YERMETIDAE OF THE AZORES 185

FIGS. 15-20. Thylaeod 11 s cf. ru gulorns (Monterosato), Sao Miguel, Azores; SEM. (Legends on previous page).

186

appearing tan with darker digestive gland shining through. Brooding fe­males : appearing greenish with colo­ration of eggs visible through thin shell. Shells often fouled by several different organisms, especially fora­miniferans and serpulid worm tubes.

Protoconch (Fig. 18): Relatively slender, pupa-shaped, with sinuous outer lip; with 2 1/2 whorls; maxi­mum shell length 700-730 µm, dia­meter 390-420 µ m. Without noti­ceable growth between hatching of crawl-away larva (see below) and settlement. Suture deeply impressed around embryonic apex. Overall tan with lighter central part of body whorl, suture brown.

0 p e r cu l um : As large as pedal disk (in living animal}, 0.74-1.0 mm, filling aperture; exposed side with edge of earlier whorl rising as free­standing lamella along suture of final 1.5 to 2 whorls (see Fig. 16); transparent.

Radula (Figs. 19-20): Regularly taenioglossate; transparent; con­sisting of 28-32 rows of teeth (for counts and dimensions: n=7, from specimens with shell mass dimen­sions of over 5 mm; no difference noted between sexes or between spe­cimens from different localities on Sao Miguel). Total length of (artifi­cially straightened) radular ribbon 660-700 µ m, width (mid-ribbon, marginal teeth not folded outward) 140-150 µm. Radular configuration agreeing with general description of vermetid characters given by Bandel ( 1984: 44-46). Trapezoidal rachi­dian tooth with strong main cusp and

SUPPLEMENT 1995: 173-192

4-5 flanking cusps on either side (decreasing in size ot~!wardly); mar­ginal ridges strongly developed. In­ner margin of lateral tooth fitting into deep marginal depressions of rachidian tooth: cusp arrangement on triangular cutting edge as in central tooth. Marginal teeth long, slender, with long and strong main cusp. Inner marginal with 4-5 flanking cusps on either side. Outer marginal (about 64 µ m in length) with 5-6 flanking cusps on inside (largest toward main cusp}, smooth on outside (Fig. 20).

Jaws: Crescent-shaped opaque cutting area; maximum length 280 µ m, attached to transparent cuticle.

Anatomy: Animal (removed from shell) long and very narrow, coiled into several loops; large specimens to 14 mm in (relaxed) length, 0.8 mm in width; long posterior lobe of di­gestive gland and gonad occupying about 2/3 of its length. Columellar muscle a very long narrow strip with deep insertion in shell (animal capable of retreating very deeply into shell). Pedal tentacles short, even when in extended position rare­ly exceeding 400 µm. Sole of foot a small and bulging protrusion be­tween and anterior to pedal tenta­cles. Pallial skirt of brooding fema­les with deep incision, running obli­quely over dorsum to back of mantle cavity. Gill extending full length of mantle cavity, approximately 20 filaments per mm in large speci­mens; anteriormost filaments very short, quickly increasing to average adult length of 260 µm; filaments

II 'c

BIELER: VERMETIDAE OF THE AZORES 187

forming small triangles, taller than wide. Osphradium vermiform, arched with back to gill (about 800 x 160 µm in large specimens), begin­ning at level of anteriormost gill filaments.

Soft-body coloration: Overall whitish or yellowish; sparse pink granules embedded in outer mantle area, in the 4 tentacles and around snout; fine white granules in head­foot, coarser in outer mantle; remainder of body translucent with more deeply embedded white pig­ment in tissue of foot and head; co­loration of the dark-shelled morph additionally with purplish-pink granules embedded in head-foot, tentacles and mantle.

Egg and larval development: 4-8 egg capsules brooded in mantle cavity, arranged in single row); capsules attached by stalks passing through deep mantle slit to interior lining of shell; capsule stalk 200 µ m in length, subterminal, never centered at pole; egg capsule dimen­sions approximately 750 x 950 µm to 800 x 1200 µm. Capsules apparently deposited over a period of time, old­est (most developed) closest to shell aperture. Egg diameter 100 µm, yolk light-green [green color lost upon preservation in alcohol]; capsules filled with dozens of light-green eggs, only 3-5 of which developing into embryos, the rest being con­sumed as nurse yolk; larval shell pupa-shaped, transparent, with brown suture; larval digestive gland filled with light green yolk; no velar lobes observed; crawl-away larvae

(approximately 700 x 400 µm shell size) developing in capsule, with tentacles and black eyes; at hatch­ing, shell with columella (shining through), suture, and lower outer shell rib browm.

Habits/habitat: Found attached to the under-surfaces of loose lava rocks and concrete blocks in shallow water, together with coralline algae, sponge, barnacles and tube-building polychaetes; singly or in small clus­ters of 2-5 per rock. Small mucous feeding nets observed. Animals not actively corroding into substratum.

Specific identity: Monterosato did not illustrate his new species "Vermetus rugulosus" in the original description (1878: 29); the diagnosis only read "Specie minuta, spirale, con le rugositA regolari simile a quelle del Caecum trachea." A sub­sequent, more detailed description accompanied by a figure (Montero­sato, 1892: 22, pl. I, fig. 8) suggests identity with this Azorean form. The Monterosato collection in Rome contains a specimen lot of 11 synty­pes (MCZR no. 21280, vidi); the largest and best-preserved . of which is the shell subsequently illustrated by Monterosato as "Forma, typica" (1892: fig. 8). This shell is here selected as lectotype of nominal spe­cies Vermetus rugulosus (greatest overall length 4.5, apertural height above attachment plane 3.5, apertu­ral diameter 0.7 mm). No anatomical or biological data from Mediterra­nean specimens were available for comparison, hence the tentativeness of the assignment to this nominal

188 A~OREANA SUPPLEMENT 1995: 173-192

species. DISCUSSION

Generic placement The present study confirms the

presence of enormous morphological variability within a single vermetid species.

Azorean Vermetus cf. triquetrus was found to have smooth, multi­ribbed or sharply keeled shells, and growth forms ranging from tight and regular coils to elo~gated and irregularly· twisted individual shell masses. Shell , coloration of this species is similarly variable, and animals occur singly; in small aggre­gations, or in intertwined clusters. Figures 1-5 illustrate the range of encountered morphs, compnsmg coiling patterns·· .previously regarded as · diagriost:ic of several nominal genus-group taxa ·(e.g., Cladopa, Pe­talocorichus, Novastoq,). Taxonomic decisions based on such teleoconch characters· alone obviously lead to a.rtificial groupings. · · ' ,J ,

As is· the case with species ' defi:.. nitions,' ~our understanding : of mono­phyletic' groups within the Verme­tidae is·: still . p:oor. The . excellent monographs by Keen ( 1961) and J.E. Morton (1965) cleared up much of the historic confusion. However, most of the genus-level assignments remain based on features of relative shell coiling patterns, relative size of operculum, and presence or ab­sence of internal shell lamellae, and not on well-defined suites of syn­apomorphies.

The two shallow-water Azorean

species ar/ here placed tentatively in the nominal genera Ver'metus Dau­din, 1800, and Thylaeodus Morch, 1860, respectively. The placement of tr i q u et r us in Ve rm e tu s agrees with Keen's (1961: 193) classifica.; tion, although that . author considered the general absence of feeding-tube scars a generic character (present in some Azorean specimens). The name Bivonia Gray, 1847, used by some authors for this nominal species (e.g., Bandel, 1984), is not available because preoccupied by Bivonia Coc­co, 1832 (Crustacea). Thylaeodus is here employed at the generic level; it was treated as a subgenus of Vermetus by Keen (1961), based on the shared absence of internal la­mellae~ and as a subgenus of.. Pe talo­oon ch us, by Morton (1965: 600), based on overall anatomical simila­rity. ·. ]ts relationships> to (or possi-: hie synonymy with). nominal .genera Vermetus or Petaloconchits need fur­ther study ..

Origin of 'the Azorean vermetid fauna Despite the ·eastward .direction of

the North Atlantic Drift, the Azorean molluscan fauna is known to have close· affinities to those of the European/North African mainland and the other Macaronesian islands, especially the Canaries and Madeira (for overview of surface current pat­terns around the Azores and some theories on colonization pathways-,. see Gofas, 1990). As was proposed for other marine organisms such as seaweeds (Prud'homme van Reine, 1988), the gastropod fauna of the

BIELER: VERMETIDAE OF THE AZORES 189

Azores seems to consist of chance survivors of chance invasions. "Is­land hopping" by forms with lecitho­trophic development, either via pas­sive larval transport (e.g., Leal & Bouchet, 1991 ), or drifting of post­larval stages (Martel & Chia, 1991 ), appears possible within the archipe­lago. However, for the long-distance dispersal over several thousand ki­lometers to the mid-Atlantic Azores, species with planktotrophic larvae and those adapted to "rafting" are obviously advantaged.

Azorean species with intracapsu­lar development leading to "crawl­away larvae" would have to be des­cendants of such planktotrophic forms, or have arrived by "rafting" or similar means of transport. As obligatorily sessile and (in the broadest sense) filter-feeding or­ganisms, vermetids are especially well-equipped for rafting. Although members of this family do · not normally settle on wood, they attach to organisms that do (such as barna­cles and oysters), and have been found as members of the fouling community on ship hulls (pers. observ.). Passive long-distance dis­persal, and thus specific identity with vermetids previously described from elsewhere in the Atlantic, is thus likely. Neither of the two Azo­rean species is known to date from the western Atlantic vermetid fauna, currently under review by the pre­sent author. Two species originally described from the Mediterranean appear to be very similar, and may prove identical after additional and

much needed study of that fauna.

ACKNOWLEDGMENTS

I thank Ant6nio M. de Frias Martins (Universidade dos A~ores)

for the invitation to participate in the 1991 Workshop, and the logistic support provided by him and the other staff members and research students of the Departamento de Biologia. Special thanks are due to Robert C. Bullock, who shared perso­nal laboratory equipment and his knowledge of the local collecting sites with me. Joao Manuel Brum, Robert C. Bullock, Paula M. Mikkel­sen and Brian Morton helped with the field collecting during the work­shop in the Azores. Italo Nofroni kindly assisted with access to the Monterosato Collection at the Museo Civico di Zoo logia in Rome,, Italy. The staff of the Musee Oceanographi­que de Monaco provided a loan of Dautzenberg's ( 1889) vermetid mate­rial from the Azores. I thank FMNH associate Katherine Wiegmann for producing some of the histological sections, Alan Kabat (USNM) for providing photocopies of publica­tions otherwise inaccessible, and Don Cameron (University of Michi­gan) for answering my etymological questions.

Travel funding to the Portuguese Azores was provided in part by the Foster Fund of the Department of Mollusks, MCZ, and the FMNH Mar­shall Field Fund. Work on western Atlantic Vermetidae was supported, in part, by Smithsonian Marine Sta-

190

tion and NATO postdoctoral research fellowships.

Additional comparative studies in Florida were made possible through the Visiting Scientist Program of the Smithsonian Marine Station at Link Port; the local support by Mary E. Rice and her staff is greatly appre­ciated. This is Smithsonian Marine Station Contribution No. 324.

LITERATURE CITED

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BANDEL, K., 1984. The radulae of Caribbean and other Mesogastro­poda and Neogastropoda. Zoologi­schf! Verhandelingen, 214: 1-188, pis. 1-22.

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BIVONA-BERNARDI, A., 1832. Con­tinuazione dell'articolo sui ver­meti, estratto dalle Collettanee di Storia naturale del barone Bivona. Effemeridi scientifiche e lettera­rie per la Sicilia, 2: 3-13, 1 pl.

BOETTGER, C.R., 1930. Studien zur Physiologie der Nahrungsauf­nahme festgewachsener Schnecken. Die Ernahrung der Wurmschnecke Vermetus. Biologisches Zentral­blatt, 50(10): 581-598.

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DAUTZENBERG, P., 1889. Revision des mollusques marins des A~o­

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HADFIELD, M.G., E.A. KAY, M.U. GILLETTE & M.C. LLOYD, 1972. The Vermetidae (Mollusca: Gas­tropoda) of the Hawaiian Islands. Marine Biology, 12(1): 81-98, 20 figs.

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ment 1990: 21-38. [ICZN] International Commission on

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