Hydroides heterocerus ( Grube, 1868 )

Ben-Eliahu, M. Nechama & Ten Hove, Harry A., 2011, Serpulidae (Annelida: Polychaeta) from the Suez Canal- From a Lessepsian Migration Perspective (a Monograph) 2848, Zootaxa 2848 (1), pp. 1-147 : 26-30

Hydroides heterocerus ( Grube, 1868)

Figs 5F, G, 8–10 , presumably also Fig. 11

Serpula (Eupomatus) heterocerus Grube, 1868: 639 , pl. 7, figs 8a–c [Type locality: Red Sea].

Hydroides heterocera [sic]: Zibrowius 1971: 715, figs 38–39, synonymy and redescription [Beirut; Gulf of Suez; southern Red Sea; Gulf of Aden, Djibouti; Mozambique; Persian (Arabian) Gulf]; Zibrowius 1979b: 133–134 [ France, Toulon Port, biofouling removed from the aircraft carrier “Foch”].

Hydroides heterocerus: Zenetos et al. 2005: 73 [classified as an “established alien invasive species” in the Mediterranean].

Eastern Mediterranean

Hydroides heterocerus: Laubier 1966: 17 [ Lebanon, first Mediterranean record of this Lessepsian migrant; 25–30 m, 1.IX.1965]; Ben-Eliahu & ten Hove 1992: 35–53 [ Israel, entire coast from north to south, 1–24 m]; Ilan et al. 1994: 45, 51–52 [ Israel, 830 m]; Ben-Eliahu & Fiege 1996: 33–34, 38 [ Israel]; Ben-Eliahu & Payiatas 1999: 101, 117 [ Cyprus, Famagusta Harbour (empty tube), legit, det. H. Zibrowius 1998, first sample from Cyprus; Zibrowius & Bitar 2003: 71 [ Lebanon]; Çinar 2006: 227, fig. 4a–c [Levant coast of Turkey, Iskenderun Bay, 1–3 m, 11 m, on rocks, X.2005].

Hydroides heterocera: Zibrowius & Bitar 1981: 159–160 [ Lebanon, Beirut, Zaitouné, 5 m, on bivalve, 23.IX.1978]; Ben- Eliahu 1991b: 518, 520–522 [ Lebanon, Israel].

Suez Canal

Hydroides heteroceros [sic]: Potts 1928: 700 [from El Qantara, Km 46 and Km 152, collected in 1924 (see “Material examined”, below]; Ben-Eliahu 1972c: 232, Table 2 [citing Potts 1928, Laubier 1966].

Hydroides heterocerus: Ben-Eliahu 1972a: 77 [citing Potts 1928]; Wehe & Fiege 2002: 126 [Suez Canal; list of references].

Hydroides heterocera: Selim 1997b: 92–93 , fig. 5a–f [from Deversoir; Lake Timsah, collected in 1988, citing Mostafa 1992, see App. Table 4].

Gulf of Suez and Gulf of Aqaba

Hydroides heteroceros [sic]: Pixell 1913: 75, pl. 8 figs 2a–c [Gulf of Suez, wall of Suez quay, collected in 1905; Red Sea, Sudan; Suakin Harbour (see “Material examined”, below); Zanzibar]; Fauvel 1933a: 77 [Gulf of Suez, St. 17 bis, 33º23'E, 28º14' N; and ter, 33º23'– 33º24'E, 28º12– 28º14' N]; Fishelson 1971: 126, table 4 [Gulf of Aqaba, infratidal rocks]; Ghobashy & Ghobashy 2005: 94, Suez Bay, buoys, misquote of El-Komi et al. 1998.

Hydroides heterocera: El-Komi et al. 1998: 16 [Suez Bay, 1992–1993, buoys].

Red Sea proper-Indo-West-Pacific (excluding citations from Gulf of Suez and Gulf of Aqaba already given above)

Serpula (Eupomatus) heterocerus Grube 1868: 639 , pl. 7 figs 8 a–c [Type locality: Red Sea].

Serpula (Hydroides) uncinata not (Philippi), sensu Gravier 1906b: 110 [South Red Sea]; Gravier 1908: 114–115, figs 463–466, pl. 8, figs 286–287, both citations synonymised by Zibrowius 1971: 715 [South Red Sea].

Hydroides heteroceros [sic]: Wesenberg-Lund 1949: 357–358, fig. 46b [Persian (Arabian) Gulf]; Day 1967: 807–808, figs 38.4.l [Red Sea, Indian Ocean, Madagascar]; Fishelson 1971: 126, table 4 [Red Sea]; Mohammad 1971: 301 [Persian (Arabian) Gulf: Kuwait]; Hartman 1974: 200 [Arabian Sea].

Hydroides heterocerus: Fishelson & Rullier 1969: 101–102 [S. Red Sea, Musseri Isl. (see “Material examined”, below]; Ishaq & Mustaquim 1996: 168, figs 4a–i [Arabian Sea, Pakistan]; Wehe & Fiege 2002: 126–127 [Red Sea, Persian (Arabian) Gulf, Gulf of Aden, Arabian Sea; list of references].

Hydroides heterocera: Vine & Bailey-Brock 1984: 141 .

Material examined ( Figs 8–10 , presumably also Fig. 11 ): Locations adjacent to the Suez Canal, Mediterranean side: Israel: 20 samples, [1]– [8–10]–[18–22] – 33 m (830 m outlier record); INCNH unpublished data, first Israeli sample, Haifa Port, legit G. Haas, 22.III.1937, det. M.N. Ben-Eliahu, HUJ-Poly-878 (previously AN-II-05) .

Suez Canal proper: Cambridge Expedition, El Qantara, det. F.A. Potts, CUZM-AN. I.1930, 1 spec., verticil with taller dorsal spine + 6 spines with lateral spinules, processes with lateral spinules positioned rather high (subdistally); 32 radii in funnel, 21 radioles, ca. 22 mm .

Suez Canal material reported herein: 35 samples with 106+?4 specs of which 4 belong to juvenile forms 1 and 2: One “new” Cambridge Expedition sample separated from a mollusc deposited at BM (NH); this single juvenile specimen preliminary named “form no. 1” ( Fig. 9 ) proved to be a Hydroides heterocerus juvenile (precise location in the canal not known [see App. Table 2A]).—Hebrew University-Smithsonian Expeditions, 1967–1973: 4 samples, 4 specs of which two were the juvenile forms named nos. 1 and 2. Great Bitter Lake , east of Deversoir-Km 97: SLC 72, 1 spec. ; SLC 74, 1 spec., juvenile form no. 1. Great Bitter Lake : SLC 117, 1 spec. , juvenile form no. 2 ( Fig. 10 ). SLC 123, 1 spec. — Great Bitter Lake “Yellow Fleet” Biofouling Samples, January 13–20, 1975: 25 +? 1 subsamples, 90 (1 juvenile) +?4 specs.— Bremerhaven dry dock, 18.VI.1975, 3 subsamples, 11 specs, all decaying; one notably large tube, ca. 4 mm outer diameter; worm without operculum 4.7 cm (branchia 6 mm) / 3 mm width.— Lake Timsah , El Tawan Beach , legit S.B. Shazly 10 / 19.XI.1988, ZMA V.Pol. 3819, 1 spec.

Locations adjacent to the Suez Canal, Red Sea side: Gulf of Suez, J.K. Lord Expedition of 1870, det. H.A. ten Hove 1969 (separated from a mixed sample BM (NH) 1870:12:23:31 by HAtH 1969, see Material Examined S. tetraceros ), BM (NH) 1870:12:23:61, specimen bioperculate, body rotted with epidermis abraded.—Gulf of Suez, Suez Quay, 3.7–18.3 m, legit J.S. Gardiner 1905 (the Percy Sladen Trust Expedition), det. H.L.M. Pixell (1913, Pl. 8, figs 2a–c), confirmed M.N. Ben-Eliahu, several specs.—?Gulf of Suez, Suez, Stn R5, Cambridge Expedition, 1924, CUZM AN. I.1930, empty coiled tube, present in test-tube with Serpula vermicularis not Linnaeus, sensu Potts (1928: 700), presumably tube of Hydroides heterocerus ( Fig. 11 ).

Gulf of Aqaba: No records.

Red Sea: Sudan, Suakin Harbour, legit C. Crossland 1904–1905, det. H.L.M. Pixell, H. Zibrowius, BM (NH) 1972.23, tube lacking, permanent mount dated 20.VII.1904.— Eritrea, Dahlak Archipelago , Musseri Island, 15°37’N, 40°43’ E, 27.5 m, Israel South Red Sea Expedition 1965, Stn 10, legit Ch. Lewinsohn 23.X.1965, det. F. Rullier, TAU-NS-1873, 1 spec.

Gulf of Aden : Somalia, Ras Katib, outside harbour on a block of dead coral, legit, det. T.G. Pillai 29.III.1982, ZMA V.Pol. 3851, 2 specs .

Suez Canal depth and substrates: Shallow, 1–2.5 m, 10 m; on sponges; on bivalves, Brachidontes pharaonis and Spondylus spinosus ; on barnacles, bryozoans, tunicates; on sandstone; on artificial substrates: Rubber fenders and iron frames.

Distribution. Indo-West Pacific: Red Sea, Zanzibar, Madagascar, Persian (Arabian) Gulf, Sri Lanka,? New Caledonia. Lessepsian migrant to the Mediterranean: Israel, Lebanon, Cyprus, Turkey.

Remarks. Potts (1928: 700–701) noted: “In one specimen, lateral processes of spines were 1/3 length from the apical process, in the other, just under the apical process. Other authors have shown that there is a great deal of variation in their position.” A non-quantitative survey of the present material showed that most of the lateral spinules were positioned close to the apical process (e.g., Fig. 8A ) and there appeared to be some variability in height of the spines in different individuals (a more thorough analysis of these characters is intended). Much more pronounced is the variability in the form of the marginal radii of the opercular funnel, ranging from “bowling-pin-shaped” radii with blunt or even stubby tips ( Wesenberg-Lund 1949 and Ishaq & Mustaquim 1996, respectively; Fig. 8E ) to those with more developed side spinules as in Fig. 8D , “T” or “anchor-shape” tips ( Pixell 1913, Zibrowius 1971; Fig. 8F ), with intermediate forms between them. Specimens from the Sudanese Red Sea ( Fig. 8F ) had much more developed side spinules than those in the Suez Canal population where the most developed of the side spinules were like those of Fig. 8D ; and less like Fig. 8E . The number of verticil spines with lateral spinules in the both the Suez Canal population and the Lessepsian migrant population ranged from 5–7, 5.59 ± 0.53 spines, N = 59, Suez Canal and 5.78 ± 0.64, N = 27, the Lessepsian migrant population, respectively, the differences between them were not significant (T-test, p = 0.198). Çinar (2006 fig. 4a, b) shows the tips of the marginal radii of the Lessepsian migrant from the Levant coast of Turkey to be like those of the Suez Canal population ( Fig. 8E ).

Specimens removed from the “Münsterland” in the Great Bitter Lake in January 1975 were large: The largest, 63 mm; verticil with 1+6 spines; funnel with anchor-tip to rounded marginal radii. However, the material sampled from the “Münsterland” in the Bremerhaven dry dock (in June 1975, 6 months later) gave the impression of even larger size (one tube had an outer diameter of 4 mm; the tubes were the largest of any taxon present in the assemblage) and many tubes were coiled. Most of the Hydroides heterocerus tubes from the Suez Canal were rounded (anterior end not attached to substrate) with marked transversal ridges; only 3 showed three longitudinal ridges, most marked in a small specimen ( Fig. 5G), less marked in the two others. We believe that the large coiled tube found in Potts’ (1928) nominal Serpula “ vermicularis ” sample from the Gulf of Suez rather belongs to H. heterocerus ( Fig. 11 ). Lessepsian migrant H. heterocerus specimens had marginal teeth like Figs 8D or E, or forms ranging between them.

Juvenile specimens: The operculum of the juvenile form from the Cambridge Expedition (form we named, “no. 1”, App. Table 2A), had sharply pointed radii tips in the funnel ( Figs 9B, C ), a marked deviation from the species description. A second specimen was obtained when searching through Brattström and Taasen’s biofouling material from the Great Bitter Lake. We attribute form “no. 1” to Hydroides heterocerus , taking note of the variability in form that can prevail during Hydroides ontogeny (see ten Hove & Ben-Eliahu 2005). A single juvenile specimen, “form no. 2”, was similarly found in the biofouling samples. In contrast, the funnel of this specimen had expanded T- or anchor-shaped marginal teeth; some of its verticil spines were characteristic for Hydroides heterocerus , while others appeared to be deviant, malformed ( Figs 10A, B ). We attribute this specimen to Hydroides heterocerus as well. In studying the Hydroides heterocerus population from the Great Bitter Lake, we encountered additional specimens with malformations such as a lateral spinule on the dorsal verticil spine, or a stub of a verticil spine rather than a fully developed one.

Figures

FIGURE 8. Hydroides heterocerus. Variability in forms of opercula from different regions: A–D. Operculum of specimen from the Great Bitter Lake aggregate removed by J.P. Taasen from the M/S “Münsterland” after its journey to the Hapag-Lloyd dry dock in Bremerhaven (18.VI.1975, 7 m). A—Lateral view, B–D—Apical views, B—Focus on tips of verticil spines, C—Focus on basal spinules of verticil, D—Enlargement of marginal teeth of funnel; the expansion of the tips of the marginal teeth in “D” is intermediate between “E” and “F,” E—“Bowling-pin-shaped” radii with blunt or even stubby tips, specimen from Little Bitter Lake opposite Kabrit (sample SLC 123), F—More expanded, “T”-shaped tips found in specimen from the Sudanese Red Sea (BM(NH) 1972.23, legit C. Crossland, 1904–1905). Lessepsian migrants with marginal radii like “D” or like “E”. Scale: 1 mm.

FIGURE 9. Operculum of Hydroides heterocerus juvenile form no. 1 (specimen from Cambridge Expedition mollusc deposited at the Natural History Museum in London, precise location unknown [See App. Table 2A]). A—Apical view, drawing and photograph, respectively, B—Profile view of drawing and photograph, C—Three-quarters view; note sharply pointed marginal teeth of funnel radii (in contrast with those in Fig. 8), D—Collar chaetae (magnification, <10 x). Scales: B—0.5 mm, D—100 µm.

FIGURE 10. Operculum of Hydroides heterocerus juvenile form no. 2 (specimen scraped from mollusc from the Great Bitter Lake [SLC 117, Y. Eytam, St. 4]). A, B—Funnel radii with some typical “anchor-shaped” (T-shaped) tips; some verticil spines approaching typical adult form, other spines deviating from the typical form, e.g., dorsal spine, upper right, bifid, aberrant. Scale: 100 µm.

FIGURE 11. Large spiralled serpulid tube. The tube was present in the test-tube labelled "Serpula vermicularis" by F.A. Potts but should rather be attributed to Hydroides heterocerus (The nominal "Serpula vermicularis" specimen collected by the Cambridge Expedition in the Gulf of Suez that was described in detail by Potts 1928 was no longer present [CUZM]). The abdominal uncini and chaetae shown below were found on skin still attached to the lumen of the tube. A—Upper view of tube (note spirorbid tubes encrusted on outer surface of the tube), B—Ventral view of tube, C—3/4 frontal view of tube, D—Abdominal uncinus, lateral view, F+5, E—Same, frontal view, left, F+10, F—Abdominal chaetae. Scales: A, B—5 mm, C—1 mm, D, F—10 µm.