Watersipora subtorquata (d’Orbigny, 1852)

Vieira, Leandro M., Jones, Mary Spencer & Taylor, Paul D., 2014, The identity of the invasive fouling bryozoan Watersipora subtorquata (d’Orbigny) and some other congeneric species, Zootaxa 3857 (2), pp. 151-182 : 155-162

Watersipora subtorquata (d’Orbigny, 1852)

( Figs 1–5 , 12–16 , 18–24 , 67 , 70 ; Table 1 )

Escharina torquata: d’Orbigny, 1842 : pl. 4, fig. 3; 1847: 11 [ Brazil].

Cellepora subtorquata d’Orbigny, 1852: 399 [ Brazil].?Non Cellepora subovoidea d’Orbigny, 1852: 402 [Red Sea; nomen dubium].

Schizoporella atrofusca: Hincks 1886: 269 (part; f. labiosa), pl. 10, fig. 5 (non fig. 4) [Arabian Sea]. Non Schizoporella atrofusca Busk, 1856: 178 [ Mexico].

Dakaria chevreuxi Jullien in Jullien & Calvet, 1903: 90, pl. 10, fig. 6 [ Senegal].

Lepralia? cucullata: Waters 1909: 150 (part), pl. 15, fig. 1 [Suez]. Non Lepralia cucullata Busk, 1854: 81 , pl. 96, figs 4–5 [Aegean Sea].

Watersipora cucullata: Hastings 1930: 729 (part), pl. 15, figs 102 [Suez].

Watersipora cucullata: Marcus 1937: 118 , pl. 24, fig. 63A, B [ Brazil].

Watersipora cucullata: Marcus 1938: 46 [ Brazil].

Watersipora cucullata: Osburn 1952: 472 (part), pl. 56, fig. 4 [ Colombia].

Dakaria subovoidea: Harmer 1957: 1022 (part).

Watersipora edmondsoni Soule & Soule, 1968: 215 , pl. 2, fig. 3 [Hawaii].

Watersipora subovoidea: Ryland 1974: 345 , fig. 3A [SE Australia].

Watersipora subtorquata: Soule & Soule 1975: 302 , pl. 3, fig. 3 [ Brazil]; 304, pl. 2, fig. 3 [ Virgin Islands]; pl. 2, fig. 5 [ Bermuda].

Watersipora subovoidea fide Harmer: Soule & Soule 1975: 302 (part), pl. 3, fig. 4 [Alexandria].

Watersipora subovoidea: Winston 1982: 139 , fig. 66 [Florida].

Watersipora subtorquata: d’Hondt 1988: 199 , figs. 6.1–2 [ Israel].

Watersipora subtorquata: Seo 1999: 222 (?part), fig. 1 [ Korea].

Watersipora subtorquata: Taylor & Gordon 2002: 4 (text), fig. 1A–C [ Brazil].

Watersipora subtorquata: Florence et al. 2007: 39 , fig. 14I, J [ South Africa].

Watersipora subtorquata: Abdel Salam & Ramadan 2008: 9 , fig. 3 [Alexandria].

Watersipora subovoidea: Ryland et al. 2009: 54 , figs. 4C, D, G, H [ Australia and Italy].

Watersipora subovoidea: Ramalho et al. 2011: 772 , fig. 3 [ Brazil].

Material examined. Holotype: MNHN, d’Orbigny Collection 13637, Rio de Janeiro, Brazil . Other material: MZUSP 0257 , Watersipora subtorquata, Araçá , São Sebastião , São Paulo, Brazil, 7 July 2009 . NHMUK 1863.8 .2.41, dry, Watersipora cucullata , Alexandria, Egypt, Station 34a, Eastern Harbour, O’Donoghue coll. NHMUK 1879.4 .25.23, dry slide, Schizoporella atrofusca, Naples , Italy, A.W. Waters coll. NHMUK 1884.4 .21.2, dry, Watersipora cucullata , South Chinese Seas . NHMUK 1885.1.26.6–7, dry, Watersipora subovoidea , Red Sea, A. Carpenter Esq . NHMUK 1888.11 .14.110, dry slide, Schizoporella sp. , Port Phillip Heads , Australia, January 1887, K. Bracebridge Wilson coll. NHMUK 1888.11 .14.111, dry slide, Schizoporella cucullata, Port Phillip Heads , Australia, January 1887, J. Bracebride Wilson coll. NHMUK 1888.11 .14.358, dry slide, Lepralia cucullata, Port Phillip Heads , Australia, January 1887, J. Bracebride Wilson coll. NHMUK 1899.5 .1.974 [one dry slide and one balsam slide], Schizoporella atrofusca form. labiosa, Type, Arabian Sea , T. Hincks coll. NHMUK 1899.7 .1.139, dry slide, Lepralia cucullata, John Adams Bank, H.M.S. Herald, G. Busk coll . NHMUK 1899.7 .1.5061, dry slide, Phylactella sp. , Pensian Gulf ?, G. Busk coll. NHMUK 1899.7 .1.5214, dry slide, Lepralia cucullata, Tangiers , Morocco, 35 fm [62.18 m], HMS Shearwater , G. Busk coll. NHMUK 1913.6 .4.11, dry slide, Leraplia cucullata , Muscat, Oman, 8–10 fm [14.6–18.3 m], Major S.G. Knox . NHMUK 1926.9 .6.164, dry slide, Lepralia cucullata , Suez Canal, K 13, 4 November 1924, A. Hastings . NHMUK 1926.9 .6.165, dry slide, Lepralia cucullata , Suez Canal, K 13, 4 November 1924, A. Hastings . NHMUK 1926.9 .6.166, balsam slide, Lepralia cucullata , Suez Canal, K 13, 4 November 1924, A. Hastings . NHMUK 1929.8 .31.1, balsam slide, Watersipora cucullata, Shema Creek , Malta, Mediterranean . NHMUK 1948.2 .16.28, wet, Watersipora cucullata, Santos , Brazil, E. Marcus coll. NHMUK 1968.1 .16.77, dry, Watersipora cucullata, St James , South Africa, 15 February 1933, F78, O’Donoghue coll. NHMUK 1963.8.2.41pt, dry, Watersipora subovoidea, J. Soule & D. Soule det., Alexandria, Egypt, Station 34a, Eastern Harbour, O’Donoghue coll. NHMUK 1973.1 .10.3, dry, Accra , Ghana, No. 13B, 14 February 1949, Bassindale coll. NHMUK 1973.1.10.4pt, dry slide, Watersipora cucullata, Pram Pram 0.25 m, Gold coast [ Ghana], 6 February 1950, Bassindale coll. NHMUK 1980.1 .12.3, dry slide, Watersipora subovoidea, Townsville harbour, Queensland, Australia, D. Hall . NHMUK 1981.4 .1.2, dry slide, Schizoporella cucullata, Hurghada , Red Sea, Yellow 935 . NHMUK 1986.8 .14.3, dry slide, Watersipora subovoidea, Hutchinson Island , Florida, 14 November 1974, JWD coll . NHMUK 1996.9 .4.1, dry, Watersipora subtorquata ,? Site 4, Punta Mochila, Venezuela, October 1971, J.S. Ryland . NHMUK 1996.9 .4.2, dry, Watersipora subtorquata, Site 1, West of Punto Arrecifes , West of Caracas, Venezuela, 8 October 1971, J.S. Ryland . NHMUK 1997.3 .12.7, dry, Watersipora subtorquata, Mochina Bay , nr. Naiguatá , coast of Caracas , Venezuela, Loc. 2a, West shore of Gay, 11 October 1971, J.S. Ryland . NHMUK 1997.3 .12.3, dry, Watersipora subtorquata, Site 5, Playa Caribe , Juan Griego, Venezuela, 12 October 1971, J.S. Ryland . NHMUK 1998.8 .5.2, dry, Watersipora subtorquata , Mughsay’ , near Salalah, Southern Oman, 10 October 1983, J.D. Taylor coll. NHMUK 2012.6 .30.3, dry slide A/B [part of NHMUK 1998.8.5.2], Watersipora subtorquata , Mughsay’ , near Salalah, Southern Oman, 10 October 1983, J.D. Taylor coll. NHMUK 1999.3 .30.11, dry slide, Watersipora sp. , New Caledonia, Beach of Ile du Phare (Lighthouse), Noumea, A. Willey . NHMUK 2007.12 .14.2, balsam slide, Watersipora subovoidea, J.S. Ryland det., Naples , Italy, 20 October 1960 . NHMUK 2007.12 .14.3, balsam slide, Watersipora subovoidea, J.S. Ryland det., Arrawarra , New South Wales, Australia, January 1972 . NHMUK 2007.12 .14.4, balsam slide, Watersipora subovoidea, J.S. Ryland det., Arrawarra , New South Wales, Australia, January 1972 . NHMUK 2007.12 .14.5, balsam slide, Watersipora subovoidea, J.S. Ryland det., Arrawarra , New South Wales, Australia, January 1972, J.S. Ryland coll. NHMUK 2007.12 .14.6, balsam slide, Watersipora subovoidea, J.S. Ryland det., Genoa Harbour , Italy, 12 November 2007, M. Faimali coll. NHMUK 2007.12 .14.7, balsam slide, Watersipora subovoidea, J.S. Ryland det., Genoa Harbour , Italy, 12 November 2007, M. Faimali coll. NHMUK 2007.12 .14.8, balsam slide, Watersipora subovoidea, J.S. Ryland det., Genoa Harbour , Italy, 12 November 2007, M. Faimali coll. NHMUK 2012.6 .30.15, dry, Watersipora subovoidea, Shaab Baraja , Sudan, Red Sea, Large lump covered in soft coral, 23m, 15 September 1978, Dumont coll. NHMUK 2012.6 .30.16, dry, Watersipora subovoidea, Shaab Baraja , Sudan, Red Sea, 25º52’N, 37º24’W, coral rock, 20 m, 22 September 1978, Dumont coll. NHMUK 1926.9 .6.167, balsam slide, Lepralia cucullata , Suez Canal, K 2, 17 October 1924, A. Hastings . NHMUK 2012.6 .30.2, dry slide [part of NHMUK 1973.1.10.3], Watersipora subovoidea, Accra , Ghana, No. 13B, 14 February 1949, Bassindale coll. NHMUK 2012.6 .30.4, dry slide [part of 1970.6.1.23], Watersipora subovoidea, Mikhmoret , Israel, 16 October 1967, G. Eitan .

Description. Colony encrusting, multiserial, primarily unilamellar on flat substrata, becoming multilamellar on irregular substrata, sometimes erect, foliaceous and bilamellar; orange ( Figs 20–21 ) to brownish-purple or black in life, dried colonies becoming dark-orange to grey. Zooids subrectangular to hexagonal, about twice as long as wide, separated by slightly raised lateral walls. Frontal shield flat to slightly convex, sometimes raised more distally than proximally, with numerous round pseudopores about 25 µm in diameter; latero-oral and disto-oral pseudopores sometimes smaller than frontal pseudopores. Latero-oral intrazooidal septula absent. Frontal shield obscured by transparent cuticle in unbleached material. Orifice large, subcircular to oval, slightly wider than long, with well-defined proximal sinus; orificial rim often with raised subtriangular projections on each side of sinus; condyles triangular, projecting distomedially, tooth-like, sometimes inconspicuous and obscured by proximal raised projections. Operculum with broad, parallel-sided dark central band demarcated by sclerites; two lucidae proximally, adjacent to condyles. Avicularia absent. Ooecia absent; orange-red embryos brooded internally, filling most of coelom of maternal zooid. Polypides bright red-orange, lophophore with 20–22 tentacles.

Remarks. We figure scanning electron micrographs of specimens from Mediterranean Israel (NHMUK 1970.6.1.23, Figs 12 , 18 ), the Indian Ocean [ Oman (NHMUK 1998.8.5.2, Fig. 13 )] and the Atlantic [ Ghana (NHMUK 1973.1.10.3, Figs 14–16 ), as well as from Brazil (MZUSP 0257; Fig. 19 )] to show their similarity with the holotype of W. subtorquata ( Figs 1–5 ). Ryland et al. (2009), followed by Ramalho et al. (2011), used the name W. subovoidea in error for this species. Watersipora subtorquata is characterized by a suborbicular orifice with a sinus demarcated by triangular condyles and an operculum with a parallel-sided dark band and two well-defined lucidae adjacent to the condyles. Ryland et al. (2009) suggested that Lepralia cucullata of Waters (1909) comprised two species. Based on the figured specimens we suggest that the Suez specimens belong to W. subtorquata and the Naples specimens ( Waters 1909, pl. 15, figs 2–4) to an undescribed species. We also found a species from Naples in the NHMUK collection (NHMUK 1912.12.21.1019, Fig. 17) that differs from W. subtorquata in the operculum and in having a wider orifice compared with the Brazilian specimens; this specimen resembles Waters’s specimens from Naples, which are here reassigned to Watersipora souleorum n. sp. (see below). Mawatari (1952) erected the ‘variety’ watersi for specimens of Lepralia cucullata reported by Waters (1909), but this name is preoccupied by a fossil, Microporella watersi de Stefani, 1884 , which is supposedly a species of Watersipora (see Waters 1909). Japanese specimens assigned to W. cucullata var. watersi by Mawatari (1952, fig. 1G) lack the triangular condyles and lucidae in the operculum and probably belong to Watersipora subatra (see below).

Ryland et al. (2009) noted that the rim of the orifice in W. subtorquata (as W. subovoidea ) may be elevated on either side of the sinus, a character easily recognizable in colonies on algae from Israel and Brazil ( Figs 18–19 ). Gordon (1989) showed a range of orificial morphologies in New Zealand specimens identified as W. subovoidea , which all seem to represent one species (D.P. Gordon pers. comm. to LMV, 2013). He described two latero-oral intrazooidal septula in his specimens ( Gordon 1989, p. 40), a character we also saw in specimens from New Zealand deposited at the NHMUK ( Fig. 47 ). Thus, the New Zealand specimens are here reassigned to Watersipora subatra .

Hincks (1886) and Calvet (in Jullien & Calvet 1903) both independently introduced ‘ labiosa ’: as Schizoporella atrofusca f. labiosa Hincks, 1886 (p. 269, pl. 10, fig. 5), from the Arabian Sea; and Schizoporella cucullata var. labiosa Calvet in Jullien & Calvet, 1903 (p. 141, pl. 16, fig 7), from Cape Verde. The specimens identified as form labiosa by Hincks (1886) are conspecific with other specimens examined from the Arabian Sea ( Fig. 13 ) and belong to W. subtorquata . The specimens previously identified as var. labiosa from the Azores by Calvet (in Jullien & Calvet 1903) (MOM 420379) are distinct in having a deep sinus and an operculum with a narrow, biconcave dark central band; these specimens are badly preserved, but they may be conspecific with W. souleorum n. sp. (see below).

Seo (1999, 2005) figured specimens of putative Watersipora subtorquata from Korea, with reddish-brown to black colonies ( Seo 2005: pls 154–156). The size of the orifice in her specimens ( Seo 2005: pl. 156B) resembles W. subtorquata but the condyles are sometimes minute and obscured by the proximal peristome.

Material reported as W. subtorquata by Ryland et al. (2009) has shallow, bar-shaped condyles and an operculum with a proximal biconcave band, quite distinct from W. subtorquata and W. cucullata ; these specimens are here identified as Watersipora subatra (see below).

Examination of the holotype material of Watersipora edmondsoni Soule & Soule, 1968 (SBMNH 96310, AHF 149; Fig. 20–22 ) revealed it to be W. subtorquata . We believe, however, that the additional specimens examined by Soule & Soule (1968, 1975) probably include one or more additional species from the same locality [e.g. the specimen reported as W. edmondsoni ( Soule & Soule 1975, pl. 1, fig. 7)]. Specimens recently reported as Watersipora subovoidea sensu Harmer by Dick et al. (2006) belong to an undescribed species that may be conspecific with W. edmondsoni sensu Soule & Soule, 1975 (non Soule & Soule, 1968).

Distribution. Atlantic ( Brazil, Caribbean, Virgin Islands, Florida, Cape Verde, Senegal, Ghana and South Africa), Mediterranean ( Italy, Alexandria), Red Sea, Arabian Sea and Pacific ( China Sea, Korea, Hawaii and Australia).

Figures

FIGURES 1–5. Watersipora subtorquata (d’Orbigny, 1852), MNHN, d’Orbigny Collection 13637, holotype, Rio de Janeiro, Brazil. 1, general view of the colony; 2, autozooidal arrangement around the ancestrular area; 3, autozooids; 4, close-up of the ancestrula, showing the orifice with projecting proximo-lateral wings; 5, close-up of orifice with wide sinus and condyles.

FIGURES 12–16. 12–15, Watersipora subtorquata (d’Orbigny, 1852); 12, colony from Israel (NHMUK 1970.6.1.23); 13, colony from Oman (NHMUK 1998.8.5.2); 14–16, colony from Ghana (NHMUK 1973.1.10.3); 14, autozooidal arrangement; 15, close-up of autozooids; 16, close-up of an orifice showing a condyle and the absence of a latero-oral intrazooidal septulum. 17, Watersipora souleorum n. sp., NHMUK 1912.12.21.1019, Naples, Italy; specimen previously misidentified as W. subtorquata; the zooids are wider than those of W. subtorquata.

FIGURES 18–22. Watersipora subtorquata (d’Orbigny, 1852); 18, 19, orifices with projecting proximolateral wings; 18, colony from Israel (NHMUK 1970.6.1.23); 19, colony from São Sebastião, Brazil (MZUSP 0257); 20–22, SBMNH 96310, AHF 149 (holotype of Watersipora edmondsoni Soule & Soule, 1969), Hawaii; 20, colony; 21, 22, close-up of zooids.

FIGURES 23, 24. Living colonies of Watersipora subtorquata (d’Orbigny, 1852) from São Sebastião, Brazil.

FIGURES 65–68. Schematic drawings of opercula of Watersipora. 65, Watersipora cucullata (Busk, 1852), Aegean Sea (redrawn from Hastings 1930, pl. 15, fig. 98); 66, Watersipora subatra (Ortmann, 1890), New Zealand; 67, W. subtorquata (d’Orbigny, 1982), Brazil; 68, Watersipora souleorum n. sp., Cape Verde (redrawn from Hastings 1930, pl. 15, fig. 104).

FIGURES 69–71. Opercula of some species of Watersipora. 69, Watersipora subatra (Ortmann, 1890), NHMUK 2007.12.14.18, Guersey; 70, Watersipora subtorquata (d’Orbigny, 1982), NHMUK 1926.9.6.165A, Suez Canal; 71, Watersipora souleorum n. sp., NHMUK 1899.7.1.1393, Cape Verde.

FIGURES 43–47. Watersipora subatra (Ortmann, 1890), NHMUK 2005.5.26.19, New Zealand. 43, autozooidal arrangement; 44, autozooid; 45, close-up of an orifice; 46, close-up of the frontal shield; 47, close-up of the lateral edge of the orifice, showing the condyle and the latero-oral intrazooidal septulum.