Spirobranchus schmardai, Kupriyanova & Flaxman & Burghardt, 2022

Kupriyanova, Elena K., Flaxman, Beth & Burghardt, Ingo, 2022, A Puzzle No More: The Identity of Spirobranchus tetraceros (Schmarda, 1861) (Annelida, Serpulidae) is Revealed, Records of the Australian Museum (Rec. Aust. Mus.) 74 (5), pp. 201-214 : 209-213

Spirobranchus schmardai sp. nov.

urn:lsid:zoobank.org:act:52EEB181-5C75-4AC3-95DD-DB7EE76F5FB4

Figs 5 , 6

In part Pomatoceros elaphus Haswell, 1885, pp. 663–665 , pl. 31, fig. 7, pl. 32 figs 9–10. [Port Jackson, Sydney. Description; figure of operculum, peduncular wings and radioles]

In part Spirobranchus giganteus .— Dew, 1959, pp. 45–46, fig. 17. [several localities in Australia, from New South Wales to Queensland]

In part Spirobranchus tricornis .—Straughan, 1967, p. 244, fig. 14b–d. [New South Wales]

In part Spirobranchus tetraceros .— Day & Hutchings, 1979, p. 147 [checklist of Australian records and specimens]

Holotype Australian Museum W. 42389 without tube, northeast of Kurnell , “Anchor Reef”, 34°00'33"S 151°13'51"E; 17.8 m . Paratypes W.42393, same data as for holotype, 1 spec. without tube and operculum prepared for SEM; W.51857, Port Botany , off La Perouse Point, 33°59'36"S 151°13'39"E, 1 spec. in tube .

Description

Tube: missing in the holotype and in paratype AM W.42393; in paratype AM W.51857 predominantly pink outside, white inside, circular in cross-section, without a tooth over entrance ( Fig. 5 ). One distinct irregular higher median keel and two or three lower lateral keels and some transversal ridges ( Fig. 5B ).

Radiolar crown: radioles in two circles ( Fig. 5A ). Radioles square-shaped in cross-section, external side smooth, internal sides with two rows of pinnules of the same length, becoming slightly shorter towards tips of radioles. Terminal filaments without pinnules. Stylodes absent.

Interradiolar membrane: high, connecting over half of radiolar length without distinct lappets (processes), but some thickenings between radioles present ( Figs 5A , 6A ).

Peduncle: three times as thick as normal radioles, inserted on the left of median line, pigmented with white/blue colours ( Fig. 5A ). Lateral distal wings wide, with pointed tips bearing finger-like processes on their inner margins ( Fig. 5A ).

Operculum: with circular flat calcareous endplate bearing three groups of dichotomously branched (antler-like) spines, position of spines always the same: one group medio-ventrally and two latero-dorsally ( Fig. 5A, B ).

Collar and thoracic membranes: collar short, covering only the bases of radioles ( Figs 5A , 6A ), divided into one ventral and two lateral lobes. Tonguelets present between lateral and ventral lobes. Latero-dorsal lobes continuing into thoracic membranes ( Figs 5A , 6A ) producing a short ventral apron. Collar chaetae of two types: special Spirobranchus - type with basal bosses covered with minute denticles and simple limbate ( Fig. 6B ).

Thorax: with seven thoracic chaetigers, including six uncinigerous ( Fig. 6A ). Thoracic chaetae simple limbate of two sizes ( Fig. 6C ). Uncini saw-shaped 12-14 teeth with anterior peg flat, nearly triangular-shaped ( Fig. 6D ). Ventral ends of thoracic uncinigerous tori widely separated anteriorly, gradually approaching one another towards the end of thorax, thus leaving a triangular depression ( Fig. 6A ).

Abdomen: abdominal chaetae long (approximately of the same length as thoracic chaetae) throughout the abdomen, not becoming significantly longer posteriorly; true trumpet-shaped ( Fig. 6F ). Uncini saw-shaped throughout the abdomen, with 11–12 teeth per row, anterior pegs flat, nearly triangular ( Fig. 6E )

Colour of preserved specimens: anterior end of thorax, distal ends of radioles, peduncle, and opercular endplate blue or white with blue specks ( Fig. 5A–C ).

Etymology. The species is named after Ludwig K. Schmarda, the author of Pomatoceros tetraceros .

Remarks

The holotype of S. schmardai sp. nov. has already been reported (along with the corresponding cyt b sequence) in Palero et al. (2020) as “ S. tetraceros sensu stricto from NSW”. Since the present study shows lack of obvious phenotypic differentiation between the sibling species, the description of morphological characters of S. schmardai sp. nov. follows that of S. tetraceros included above. Also, the reliable synonymy for the new species is problematic, as either of the two cryptic sympatric species could have been reported under the names S. tetraceros , S. elaphus , and S. tricornis . The only potentially important morphological difference between the two species is the obvious lack of Discussion

lappets between radioles in S. tetraceros and the presence of slight inter-radiolar thickenings in S. schmardai sp. nov. Morphological species delimitation is notoriously difficult However, these subtle inter-radiolar characters have never within the genus Spirobranchus because of their high been given consistent attention in previous descriptions and intraspecific variability in opercular structures, traditionally they might turn out to be common throughout the complex. considered the major taxonomic characters of the genus. Thus, following the example of Halt et al. (2009, for Mainly because of this high opercular variation, ten Hove Galeolaria caespitosa Lamarck, 1818 and G. geminoa Halt (1970) initially synonymized 22 nominal taxa under the et al., 2009), we included the molecular diagnostic characters name S. tetraceros . However, already 20 years later, mainly of S. schmardai sp. nov. ( Table 3). on biogeographic insights, ten Hove’s synonymy was acknowledged as an oversimplification and ever since the name S. tetraceros has been regarded as a complex of species (e.g., Frank & ten Hove, 1992; ten Hove, 1994; Fiege & ten Hove, 1999; ten Hove & Kupriyanova, 2009; Ben-Eliahu & ten Hove, 2011; Perry et al., 2018), in fact the taxon thus should be regarded to be a species inquirenda. Both genetic data in Palero et al. (2020) and the results of our study clearly support the morphology-based conclusion at the beginning of this discussion. Moreover, the molecular characterization of specimens from the Mediterranean by Palero et al. (2020), including specimens with either simple conical opercula or those with branching spines, confirms that this morphological variability is a result of intraspecific plasticity.

It is remarkable that although numerous studies worldwide have been using the name Spirobranchus tetraceros (reviewed in Perry et al., 2018), this study is the first to describe and illustrate specimens collected from the type locality of the original species. Schmarda (1861) collected the specimen (his entire diagnosis suggests a single specimen only) of what he described as Pomatoceros tetraceros during a voyage around the world (1853–1857). As type locality for this species, he only mentioned “ New South Wales ” without specifying any further. However, the only Australian localities mentioned in the introduction of his account of the voyage are Melbourne, Sydney, and the Blue Mountains. Moreover, all his other new Australian species described in the taxonomic part of the Schmarda (1861) monograph were from New South Wales. For eight of them the type locality was specified as “Port Jackson” (modern day Sydney) and one was from the “ Coast of Illawarra” (just south of Sydney). Based on this information, we argue that Sydney was the type locality for his Pomatoceros tetraceros .

While we designated here a neotype for S. tetraceros based on topotypical material from Sydney, our phylogenetic analyses also provided compelling evidence for the existence of two sympatric well-supported clades within the S. tetraceros sensu stricto morphotype. These two clades show a mean interspecific p-distance of 36%, which actually exceeds those observed for the same cyt b fragment within the Spirobranchus kraussii complex (14.6–26.9%, see Nishi et al., 2022) and other serpulid genera, such as, for example, Ficopomatus (19.2%, Styan et al., 2017), Galeolaria (22.8–24.5%, Halt et al., 2009), and Hydroides (15.8–23.1%, Sun et al., 2016). Thus, although we detected no consistent morphological differences between the specimens of the two clades, we treated them as sympatric cryptic species and in addition to designating the neotype of S. tetraceros , we also described the sister species as S. schmardai sp. nov.

As expected on biogeographical grounds, specimens from NSW (Greater Sydney in this case) and tropical Queensland belong to different taxa and probably also to separate faunas. The clear difference between the northern tropical and southern temperate marine Australian faunas ( Ekman, 1953; Briggs, 1974), with a transition zone on the East and West Coasts (Wilson & Allen, 1987) has been long recognized. Apparently, there is a strong historical and environmental influence in the composition of the Australian marine faunas. The northern tropical fauna is similar to a broad Indo-Pacific one that has developed in the Tertiary period, particularly with the emergence of coral reefs. The southern fauna in south-eastern Australia consists of a Palaeoaustral component that can be traced to the late Eocene–Mid Miocene (reviewed in Poore & O’Hara, 2007).

Moreover, the phylogenetic results of this study support this biogeography-based conclusion as the Australian species of the S. tetraceros complex do not form a monophyletic group. Instead, the species from tropical Queensland are shown to be more closely related to the Indo-Pacific S. multicornis and the Mediterranean introduced taxon of unknown origin from Palero et al. (2020). Unfortunately, our results do not provide unequivocal evidence whether the entire S. tetraceros complex constitutes a monophyletic group, so further phylogenetic studies of the complex are needed.

Based on the results of our study, the taxonomic status of S. tetraceros reported from Queensland (Kupriyanova et al., 2015) and Western Australia (Johansson, 1918; Pillai, 2009) needs to be revised. The specimens from Queensland (Mackay, Gladstone, Burnet Heads, Pialba) reported as Spirobranchus semperi Mörch, 1863 by Straughan (1967: 246-247) likely belongs to either S. cf. tetraceros sp. B, S. cf. tetraceros sp. C of this study, or both. The type locality of Mörch’s species is the Philippines (unspecified further), so further studies are needed to determine the taxonomic status of the tropical Indo-Pacific populations of S. cf. tetraceros in Queensland and here no name is suggested for these specimens.

Here, however, we suggest resurrecting the older available name S. multicornis Grube, 1862 for the Red Sea population of Spirobranchus cf. tetraceros (examined in Perry et al. (2017, 2018)). The original description by Grube (1862) is very short: “ S. multicornis n. sp. was brought in by Professor Ehrenberg from the Red Sea (see Fig. 3 , p. 59). The opercular plate bearing a circle of six projections, of which only three were preserved, these are antler-like, every antler branched with multiple tines; the wide peduncle, with wings right and left, is inserted above the left radiolar lobe, the radioles in a simple circle” (translated by H. ten Hove).

Spirobranchus multicornis specimens associated with corals in the Red Sea (as S. cf. tetraceros in Perry et al., 2017, fig. 3E; 2018, fig. 5A) have a circular opercular plate with three pairs of antler-like spines positioned in the middle of the plate and not arising from a common base; each spine is forked at the tip. Also, in S. multicornis the inter-radiolar membrane bears distinct lappets between radioles. In contrast, although the opercular structure is notoriously variable in this group, S. tetraceros and S. schmardai sp. nov. have opercular spines roughly arising from the common base and lack inter-radiolar lappets.

Specimens of another Spirobranchus cf. tetraceros recently discovered in the Mediterranean by Palero et al. (2020) are also characterized by the interradiolar membrane and anterior margin of peduncular wings bearing finger-like processes, thus are morphologically more similar to S. multicornis than to S. tetraceros or S. schmardai sp. nov. Genetic distance between the Red Sea ( S. multicornis ) specimens and Mediterranean S. cf. tetraceros is large enough to be considered as belonging to distinct taxa. Thus, the widely accepted hypothesis of Ben-Eliahu (1991) that S. cf. tetraceros is a Lessepsian migrant passively crossing the Suez Canal to the Mediterranean was not supported by Palero et al. (2020). The identity and origin of the introduced Mediterranean population will remain a mystery until the source population is found.

In summary, the results of this study call for a revision of the Spirobranchus tetraceros complex both in Australia and worldwide. In particular, it will help to determine the identity and origin of the introduced established population of S. cf. tetraceros from the western Mediterranean reported in Palero et al. (2020).

ACKNOWLEDGEMENTS. This study was funded by Australian Biological Resources Study (ABRS) grants RF 213-19 and RG18–21 to EKK. We are grateful to Harry ten Hove for sharing his numerous notes and insights on the Spirobranchus tetraceros complex and translating the description of S. multicornis by Grube, 1862. We thank Nurul Hassan (University of Malaysia at Terengganu), Olivia Prentice (University of Newcastle, NSW) and William Zhang (University of Sydney) who took photos of specimens, and Simon Ho (University of Sydney) for his help with phylogenetic analyses. Sue Lindsay (Macquarie University, Sydney) helped with SEM. To all these colleagues, we express our sincere gratitude. We thank Drs Harry ten Hove and Yanan Sun for their thorough reviews of the manuscript.

Figures

Figure 3. Photographs of the neotype and additional specimens of Spirobranchus tetraceros sensu stricto. (A) original drawings of Pomatoceros tetraceros by Schmarda (1861); (B) original drawing of Pomatoceros elaphus by Haswell (1885); (C) neotype of S. tetraceros W.51859; (D) specimen W.49841 in tube; and (E) specimen W.49844, operculum (left), a tube fragment (right).

Figure 5. Photographs of S. schmardai sp. nov. holotype and paratype. (A) anterior part of the holotype W.42393, ventral view (left), lateral view (right); (B) paratype W.51857 in tube.

Figure 6. Scanning electron microscopic micrographs of S. schmardai sp. nov.paratype W.42393.(A) lateral view of the anterior part; (B) collar chaetae bundle with special Spirobranchus-type chaetae; (C) thoracic chaetae; (D) thoracic uncini; (E) anterior abdominal uncini; (F) anterior abdominal chaetae.