Serpula israelitica Amoureux, 1977

Sanfilippo, Rossana, 2009, Systematics and life habit in Serpula israelitica Amoureux, 1977 (Polychaeta Serpulidae) from the Mediterranean with remarks on other soft-bottom serpulids, Journal of Natural History 43 (33 - 34), pp. 2009-2025 : 2011-2019

Serpula israelitica Amoureux, 1977

Serpula (Paraserpula) israelitica Amoureux, 1977: 1056–1059 , fig. 2a–c.

Serpula israelitica Ben-Eliahu and Fiege 1996: 6–7 .

Serpula israelitica Vinn et al. 2008a: 635 , 640, 644, 645, 649; Vinn et al. 2008c: 80, 87, fig. 7B.

Examined material

Sicily Channel. Graham Banks: sample CR/10, 97 m (1 empty tube); sample CR/ 12, 113.5 m (2 tube distal ends); sample CR/ 15, 201 m (1 tube attached to hardground).

Ionian Sea. Gulf of Noto : sample 10N, 107 m (11 tube distal ends), sample 4G, 130 m (3 tube distal ends); Ciclopi Islands: sample 2G, 87.50 m 4158120 N, 516110 E (1 specimen inside its tube, 10 tube distal ends plus 1 attached tube); sample 18G, 102 m (1 tube distal end); Amendolara Bank: sample AM/91 2D, 50 m (2 tubes attached to calcareous algae); S.M. Leuca Bank: sample AP 7, 525 m (3 tubes attached to corals), sample Coral 13, 670 m (4 attached tubes, on hardground fragments); Gymnasium Cave (Syracuse), 20 m (3 tube distal ends) .

Tyrrhenian Sea. Ficarella Cave ( Palermo ), 30 m (1 tube distal end). Eastern Atlantic. Cape Verde Islands: sample CANCAP 7.031, 75 m 14°57′ N, 24°38′ W (1 specimen from foraminifera sands, courtesy of H. ten Hove) .

Description of the body was based on the unique animal from sample Ciclopi 2G, while observations on the body colour were made from the specimen from the Cape Verde Islands.

Description

Body length, without branchiae, 35.6 mm; branchial crown, about 5 mm in length, bearing 13 radioles on each side, with long pinnule-free tips. Peduncle cylindrical, smooth, seemingly the first (modified) left radiole, but inserted just below and in front of first and second radioles. Operculum a simple shallow funnel of fused radii (n = 45), with a denticulate edge, concave on its upper part and separated from the peduncle by a feeble constriction. Radiole opposite to the operculum short, underdeveloped, bearing a club-shaped, rounded pseudoperculum ( Figure 1A,B ).

Thorax 1.2 mm wide, with 12 thoracic segments ( Figure 1D ), but only the second to fifth segment with uncini. Collar trilobed, short, not covering branchial lobes ventrally. Thoracic membranes extending to end of thorax and forming a free apron, covering the first abdominal segment. Collar chaetae slender, limbate capillaries (n = 11) and twice as thick as geniculate chaetae with a narrow distal tip (n = 6). Subsequent thoracic chaetae limbate capillaries, smaller than previous ones. The last (12th) chaetiger possesses 17 simple capillaries. Thoracic uncini subtriangular with 8–10 pointed teeth in one row, the anterior one larger. Abdominal chaetae flat-trumpet-shaped, denticulate distally and radiating fan-like ( Figure 2A–F ).

Branchiae predominantly red, with up to 10 transparent bands with a small white stripe each ( Figure 1C ). Operculum with white inside, red tips of radii (teeth of funnel), an orange circle proximal to the edge of funnel. Narrower part of operculum purplish red, white constriction between operculum and peduncle. “Interradiolar membrane” white with hint of orange band, basis of crown red to transparent proximally. Thorax orange-ish transparent. Collar transparent, edge of thoracic membrane red.

Tube white, rarely brownish near the lumen. Diameter 1.51 mm (0.9–1.8 mm), relatively constant along its length. Attached part loosely coiled, encrusting the substrate with a peripheral basal flange, (semi-)circular in cross-section with smooth shiny surface ( Figure 3A–C ). Alveoles are present inside the two lateral tube flanges ( Figure 3A,D ), regularly aligned, subquadrangular in horizontal cross-section and with an undulate casting ( Figure 3E,F ). These characters appear to be a constant feature of the tube. The proximal end of the tube is fragile, feebly calcified, 100 µm wide and 700 µm long, representing the first secretion of the larva after settling on the substrate. Like similar young parts observed in other serpulid species, it is circular in cross-section without ornamentation, a distinct rim separating it from the slightly older and more calcified tube ( Figure 3G,H ). For this earliest tube part, the term “prototube” is proposed, in analogy to the “protoconch” of molluscs. Distal part of the tube generally rather straight, raised from the substrate for a great length ( Figure 4A ), often flaking off in old specimens ( Figure 4B ).

Tube surface appears smooth under stereomicroscope, displaying very slight growth lines in well-preserved tubes of young specimens ( Figure 4C ). They are rounded and symmetrical in section, corresponding to single growth increments ( Figures 3C , 4D ), and disappear with further calcification ( Figure 4E ). Tube wall on average 120 µm thick, often irregularly discontinued, suggesting a layering, however, not supported by a different ultrastructure ( Figure 5A,B ). Calcium carbonate crystals prismatic, about 3 µm long ( Figure 5C ), displaying a common orientation within a single growth increment like an ordered chevron-like structure sensu Weedon (1994) or lamellofibrillar structure sensu Carter et al. (1990). Such a structure is masked or partially obliterated by a conspicuous homogeneous organic matrix, which fills the interspaces between crystals, probably together with homogeneous carbonate cement ( Vinn et al. 2008a).

A transverse mineralized tabula may close the posterior end of the broken free distal tube, crossing the tube. Its position inside the tube is very oblique ( Figure 3D,E ). The tabula is a cribrate septum of calcium carbonate, with two lateral rows of 17 holes, each of them being rather irregular in size. The tabula is about 140 µm thick in cross-section and has a sphaerulitic prismatic microstructure (sensu Carter et al. 1990) ( Figure 5G,H ). Its outer surface is covered by abundant organic matrix ( Figure 5I ).

Tube microanalysis

Serpulid tubes are composed of a mixture of calcium carbonate crystals and an organic matrix ( Neff 1971). The mineral part can be magnesium calcite, aragonite or a mixture of both ( Bornhold and Milliman 1973; Vovelle et al. 1991; Vinn et al. 2008a). Bornhold and Milliman (1973) discussed the magnesium carbonate concentration in relation to temperature.

SEM–energy dispersive spectroscopy microanalysis on S. israelitica tubes confirmed calcium as the main constituent (average calcium 20.8 wt%), magnesium being subordinate (average 2.0 wt%) with traces of strontium (average 0.8 wt%). The magnesium content is higher than in Ditrupa arietina tubes analysed by Vinn et al. (2008c): 0.82 wt% for the outer tube layer and 1.25 wt% for the internal tube layer.

Radiographic microanalyses of S. israelitica tubes revealed a relatively high concentration of carbon within the tube wall (average 24.3 wt%). The presence of an abundant organic matrix can be seen in Figure 5 (C), where crystals inside the tube wall are partially obliterated, embedded within the organic matrix.

The organic content of the tabula was higher than elsewhere in the tube. Microanalysis gave a mean percentage weight for carbon of 32.0 wt% inside the tabula and 34.5 wt% at its outer surface. Calcium and magnesium were also present at values similar to those of the tube (average 19.7 wt% and 2.0 wt%, respectively).

Remarks

Complete tubes of S. israelitica are clearly distinguishable from Mediterranean congeners in having a row of alveoles in the lateral flanges on their attached parts. As a consequence the diagnosis of the genus can be amended. Similar lateral alveoles are characteristic of entire genera ( Pomatoceros , Spirobranchus , Filogranula ) and of certain species [ Semivermilia cribrata (O.G. Costa, 1981) and S. elliptica Imajima, 1978 ].

Serpula israelitica also differs from its Mediterranean congeners by having a smooth tube, without any particular ornamentation. Tubes of S. lobiancoi are also smooth, but in contrast to S. israelitica their proximal parts are typically “spaghettilike” coiled and peristomes occur in their distal ends.

Serpula israelitica is similar to S. vermicularis and S. cavernicola in having a shallow funnel-shaped operculum with many fused radii. In addition, tubes of S. israelitica and S. vermicularis are comparable in being single-layered, with a lamellofibrillar structure ( Vinn et al. 2008a,b; Sanfilippo, unpublished results).

The number of thoracic chaetigers in S. israelitica differs from that known in other congeners, being variable: seven to nine in the original description and 12 in the examined specimen.

The presence of geniculate instead of “ Serpula ”- type bayonet collar chaetae in this species is remarkable. It may represent infra-generic variability because the lack of special chaetae in the genus has been observed in some species from outside the Mediterranean ( Imajima, 1979).

Transverse gratings described by Hedley (1958) in some damaged tubes of Pomatoceros triqueter (Linnaeus, 1767) , a species also found in the Mediterranean, differ from those of S. israelitica in being curved, inclined at a much higher angle and with about half the number of holes (see text fig. 11: Hedley, 1958). A tabula of P. triqueter described by Vinn et al. (2008a) also differs in being markedly thinner in cross-section (30 µm) and in having a different microstructure (irregularly oriented short prismatic-to-cubic crystals). Like in S. israelitica , those tabulae are rich in organic matrix embedding the crystals.

Tabulae of S. israelitica differ considerably from the internal tube structures of Spiraserpula ( Pillai and ten Hove 1994) , but the sphaerulitic prismatic microstructure is the same in the internal keels of Spiraserpula caribensis ( Pillai and ten Hove 1994; Vinn et al. 2008b) and S. massiliensis (Sanfilippo, unpublished results).

To some degree the tube of S. israelitica resembles tubes in the genus Protula : having a smooth surface and cylindrical distal part. However, the tube is generally thinner in S. israelitica and has a peculiar micromorphology and wall structure (see below).

Key to the Mediterranean species of the genus Serpula Linnaeus, 1758

1. Operculum funnel-shaped with a denticulate edge, circular in diameter. Thoracic membrane forming ventral apron across the anterior abdominal chaetigers. Tube white, orange or pink, carinate or smooth................. 2 Operculum funnel-shaped with a denticulate edge, oval in diameter. Thoracic membrane ending at the second chaetiger, not forming ventral apron. Tube smooth, irregularly coiled in its proximal part; distal part erect with peristomes. Tube wall consisting of two layers: an internal thick, white, opaque, and a thinner external, pink, transparent............ S. lobiancoi

2. Operculum deep funnel-shaped (inverted bell) with about 20 fused radii, separated from peduncle by a constriction. Tube white, small-sized, consisting of a single opaque layer. Tube attached to substratum throughout its length, semicircular to trapezoidal in cross-section, with three to five longitudinal rounded ridges, equal in size............................ S. concharum Operculum shallow funnel-shaped (inverted cone) with 40 or more fused radii. Tube white or pink. Proximal part circular to triangular in crosssection; distal part often erect and circular in cross-section..............3

3. Operculum with 45–80 fused radii, not separated from peduncle by constriction. Tube white, large and thick, with a rugose surface. Proximal part (semi)circular in cross-section with a discontinuous longitudinal ridge, distal part with peristomes.................................. S. cavernicola Operculum with 40–60 fused radii, barely or not at all separated from peduncle by constriction. Proximal part of tube triangular to circular, distal part circular in cross-section..........................................4

4. Seven thoracic chaetigers (including collar chaetae). Tube white to pink/ orange. Proximal part subtriangular in cross-section, with a longitudinal median denticulate ridge and two or three pairs of lateral smaller ridges. Distal part, if free, relatively short and circular in cross-section with faint keels and wide peristomes............................. S. vermicularis Seven to 12 thoracic chaetigers (including collar chaetae). Tube white, smooth. Proximal part semi-circular in cross-section. Long, free, cylindrical distal part without peristomes............................ S. israelitica

Figures

Figure 1. Serpula israelitica. (A) Branchial crown bearing operculum on the left and a rudimentary club-shaped pseudoperculum on the right. (B) Operculum shallow funnel-shaped with a denticulate edge, transition/operculum marked by a slight constriction. Sample Ciclopi 2G. (C) A coloured specimen within its tube. Sample CANCAP 7.031 (Photo F. Verbiest). (D) Thorax in lateral view, trilobed collar and 12 pairs of chaetigers. Sample Ciclopi 2G. Scale bars 1 mm.

Figure 2. Serpula israelitica. (A) Collar chaetae: slender limbate capillaries. (B) Collar chaeta: geniculate with a narrow distal tip. (C) Thoracic chaetae: limbate capillaries. (D) Thoracic uncinus. (E) Capillary simple chaeta from the 12th thoracic chaetiger. (F) Abdominal chaeta with flat trumpet-shaped end. Scale bars 10 µm. Sample Ciclopi 2G.

Figure 3. Serpula israelitica. (A) Attached tube parts irregularly curved and widely encrusting a corallinae algal fragment. Scale bar 1 mm. Sample AM/91 2D. (B) Encrusting tube circular in cross-section, with smooth shiny surface and two evident lateral flanges. Scale bar 1 mm. Sample AP07. (C) Detail of smooth outer surface from the attached part of the tube. Scale bar 200 µm. Sample AP07. (D) Row of alveoles inside a broken part of the basal flange. Alveoles are equally sized and regularly aligned. Scale bar 500 µm. Sample AM/91 2D. (E) Internal view of an alveole showing a subquadrangular undulate contour and crystals paving the lumen surface. Scale bar 50 µm. Sample AM/91 2D. (F) Detail of alveole on its inner surface with elongate prismatic crystals irregularly arranged in an unoriented structure. Scale bar 5 µm. Sample AM/91 2D. (G) Encrusting tube still with its proximal end (arrow). Scale bar 1 mm. Sample AP 07. (H) Detail of proximal end of tube, circular in cross-section, weak and lacking ornamentation, separated from the rest of the tube by a narrow rim (arrow). Scale bar 100 µm. Sample AP 07.

Figure 4. Serpula israelitica. (A) Tube distal parts. Scale bar 2 mm. Sample Noto 10N. (B) Old-looking tube flaking off in irregular layers. Scale bar 1 mm. Sample Ciclopi 2G. (C) Tube of a young specimen with a shiny outer surface and slight growth lines. Scale bar 1 mm. Sample CR/10. (D) Micromorphology of outer surface of the tube of a young specimen showing rounded and symmetric in section growth lines. Scale bar 200 µm. Sample Ciclopi 2G. (E) Smooth outer surface from a tube distal part corresponding to the adult/old stage, growth lines disappearing with further calcification. Scale bar 200 µm. Sample Noto 10N.

Figure 5. Serpula israelitica. (A) Cross-section of the tube wall flaked in layers of different thickness. Scale bar 100 µm. Sample Noto 10G. (B) Detail. Scale bar 20 µm. Sample Noto 10G. (C) Prismatic crystals from the tube wall ordered in a lamellofibrillar structure partially obliterated by organic matrix within the prisms. Scale bar 10 µm. Sample Noto 10G. (D, E) Ventral and lateral view of a mineralized tabula closing the posterior end of a broken unattached distal end. Scale bar 1 mm. Sample Ciclopi 2G. (F–H) Progressively closer views of a tabula in cross-section showing a sphaerulitic prismatic structure. Scale bars 500 µm (F) and 100 µm (G, H). Sample Noto 10N. (I) Abundant organic matrix overlying the outer surface of a tabula. Scale bar 5 µm. Sample Noto 10N.