Schizoporella, Hincks, 1877

Ryland, John S., Holt, Rohan, Loxton, Jennifer, Spencer Jones, Mary E. & Porter, Joanne S., 2014, First occurrence of the non-native bryozoan Schizoporella japonica Ortmann (1890) in Western Europe, Zootaxa 3780 (3), pp. 481-502 : 495-496

Schizoporella on the Pacific coast of North America

Schizoporella unicornis , a Recent bryozoan originally described in a work on the Coralline Crag by Johnston (in Wood 1844; see Tompsett et al. 2009 for details) is a well-known European species ( Johnston 1847; Hincks 1880; Ryland 1965; Hayward & Ryland 1995, 1999; but not Marcus 1940 (= S. errata , absent from northern Europe)) that is unknown on the Pacific coast of North America. Because of undue reliance on European literature, generally inappropriate for the Pacific coast (e.g. Ryland & Porter 2012), the characteristics of this species ( Hayward & Ryland 1995, 1999; Tompsett et al. 2009), especially the marginally fluted but virtually non-porous ovicell, were missed by authors or deliberately ignored (e.g. Ross & McCain 1976) and the name unicornis has been incorrectly applied to at least two quite different species. Osburn (1952) —before S. japonica had been recognized in the northwest—included only one nominate species that would now be included in the genus Schizoporella , using the name S. unicornis , from various localities in California. Osburn’s account is now known to have been based on a mixture of S. japonica and S. errata (Powell 1970) and S. pseudoerrata (described by Soule et al. 1995). The current distribution of S. errata is unclear since the species is not discussed by Soule et al. (1995, 2007), though it is certainly common in San Francisco Bay ( Zabin et al. 2010). The differences between S. unicornis and S. errata are in fact numerous and considerable (this paper and Ryland 1965; Hastings 1968; Hayward & Ryland 1999; Hayward & McKinney 2002; Tompsett et al. 2009). Whether S. errata should be regarded as a single species, a complex, or several species is another issue ( Winston & Hayward 2012), which cannot be resolved here.

While Schizoporella errata , being a well-known fouling species, seems likely to have been introduced to the Pacific coast well before its first recorded occurrences (as S. unicornis , by Osburn 1952), S. japonica is most certainly a recent alien. However, Powell (1970) established that it (as S. unicornis ), as opposed to S. errata , was present in Newport Bay, Los Angeles, as long ago as 1938 (material collected by G. E. MacGinitie); he assumed that it had arrived with Pacific oysters, Crassostrea gigas , which had been imported from Japan (first to Morro Bay) since 1932. This is the earliest record for this species on the west coast of North America. Powell (1970) referred to additional material in USNM from Newport, collected 1943, and Morro Bay, collected 1968. Powell (1970) himself found it (still using the name S. unicornis ) from the Strait of Georgia, Canada. It had not been found earlier by O’Donoghue & O’Donoghue (1923, 1925, 1926) but was found by Powell during 1966–69 from several stations in the San Juan Islands, on Vancouver Island, and from as far north as Pendrell Sound (50° N). As for California, he attributed its arrival to the extensive importation of Pacific oysters from Japan in the period 1926– 1935. Its recorded range was extended to further localities in Washington State by Ross & McCain (1976), who conducted a thorough study of zooidal shape [the variability noted earlier that arises from the growth pattern of circular colonies, a topic also investigated in this species by Thorpe & Ryland (1987)]. It was also collected in San Francisco Bay during 1977 (NHMUK 1978.1.4.2). Whereas S. errata , as a warm-water species, is likely to be commonest south of San Francisco, the converse is true for S. japonica . It has spread northwards through Canada to southern Alaska ( Dick et al. 2005) but, as already noted, it extends southwards beyond San Francisco to Morro Bay (#14) and (historically at least) to the Los Angeles area.

Thus it now appears that three distinct species of Schizoporella occur in central California (i.e. the Monterey Bay area), S. errata , S. japonica , and S. pseudoerrata , the first two, at least, being introductions. Sorte et al. (2010) listed an unidentified Schizoporella from Bodega Harbor, most likely S. japonica (see #21) but possibly S. errata , and Zabin et al. (2012) recorded unidentified Schizoporella from two sites at Santa Cruz. Schizoporella pseudoerrata at present has a very localized confirmed distribution ( Soule et al. 1995) although it has been listed as present at two sites in the northern part of San Francisco Bay—Richmond Marina ( Blum et al. 2007) and Tiburon ( Crooks et al. 2011). It is possible that these records are based on misidentifications and might be either of the other two species. With all three species now recognized and described, it should be possible to correctly identify Schizoporella specimens from the Pacific coast. The characteristics of the three Californian species are summarised in Table 7 (particularly note the distinctive condyles, observation of which requires the preparation of specimens with a hypochlorite bleach such as Clorox: see Material and Methods above), which should be used in conjunction with Figures 2–4 and 10 .

In addition to morphometric methods, genetic techniques have recently been applied in two non-native fouling bryozoan species-groups. In Bugula neritina (Linnaeus) , three biological species were identified. One of these, haplotype S, was globally distributed ( Fehlauer-Ale et al. 2013). In Watersipora subtorquata , three clades were identified by Mackie et al. (2012). These studies provide evidence for cryptic speciation in the fouling community. Genetic studies on Schizoporella japonica are currently underway to investigate the potential for cryptic species in this taxon.

Figures

FIGURE 2. Schizoporella japonica. A, Colonies on fenders, Holyhead marina, June 2011; B, closer view of encrustations on the centre fender in A; C, Close-up of same encrustation (photos A–C, RH); D, macro-photograph of expanded zooids on flat substratum, Friday Harbor, WA, July 1986; E, balsam preparation of decalcified material stained with borax carmine and picric acid to show opercula, Holyhead marina, February 2011; F, enlarged view of operculum in E (photos D-F, JSR).

FIGURE 3. Schizoporella japonica. A, SEM of part of cleaned colony, Holyhead marina, February 2011; B, SEM at higher magnification; C, close-up of ovicell; D, close-up of non-ovicellate orifice, condyles and avicularium lateral to orifice. (A–D, SEMs at NHMUK by P. D. Taylor); E, balsam mount seen with transmitted light from same material showing variation in zooid width caused by row division; F, orifice from E at high magnification to show details of condyles (photos E–F, JSR). Scalebars: A, 500 µm; B, 200 µm; C, 100 µm; D, 50 µm.

FIGURE 4. Schizoporella japonica. A, Ancestrula and early astogeny (one distal and symmetrical distolateral zooids); B, C, ancestrulae; (A–C from young colonies on a settlement plate immersed at 0.5 m in Stromness marina, Orkney Islands, December 2012); D, established colonies on a prototype tidal turbine following a two-year sea trial in the Orkney Islands (photo Andrew Want, EMEC,) January 2013; E, type specimen of S. japonica (MZS Bry001 in the Strasbourg Museum; photo Marie Meister); F, young colonies, Jakle’s Lagoon, San Juan Island WA, collected by the late C. G. Reed and photographed by JSR in July 1986 (at the present time this lagoon is cut off from the sea by a shingle barrier); G, heavy settlement on hull of beached vessel, Orkney Islands (photo JSP).

FIGURE 10. Schizoporella errata (A–C) and S. pseudoerrata (D–G). A, S. errata colony showing typically massive structure produced by repeated frontal budding (Coyote Point, San Francisco Bay, coll. J. T. Carlton, 11 October 2009); B, S. errata, orifice and condyles, transmitted light (Pearl Harbor, HI, coll. J. T. Carlton 7 June 2011), scale bar 50 µm; C, S. errata, SEM (photo MSJ), NHMUK 2009.1.26.2 (Nisida Harbour, Nisida Island, Naples, 1 m depth, coll. S Tompsett, 11/9/2008); D–E, S. pseudoerrata, SEM, parts of colonies (Elkhorn Slough, Monterey Bay, CA, coll. J. D. and D. F. Soule, 1995; SEMs H. Chaney), inset (F) shows orifice with paired suboral avicularia; G, S. pseudoerrata, SEM, detail (same provenance as D–E).