Research Article |
Corresponding author: Maria Capa ( maria.capa@ntnu.no ) Academic editor: Christopher Glasby
© 2016 Maria Capa, Anna Murray.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Capa M, Murray A (2016) Combined morphological and molecular data unveils relationships of Pseudobranchiomma (Sabellidae, Annelida) and reveals higher diversity of this intriguing group of fan worms in Australia, including potentially introduced species. ZooKeys 622: 1-36. https://doi.org/10.3897/zookeys.622.9420
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Pseudobranchiomma (Sabellidae, Annelida) is a small and heterogeneous group of fan worms found in shallow marine environments and is generally associated with hard substrates. The delineation and composition of this genus is problematic since it has been defined only by plesiomorphic characters that are widely distributed among other sabellids. In this study we have combined morphological and molecular (mitochondrial and nuclear DNA sequences) data to evaluate species diversity in Australia and assess the phylogenetic relationships of these and other related sabellids. Unlike morphological data alone, molecular data and combined datasets suggest monophyly of Pseudobranchiomma. In this study, a new species of Pseudobranchiomma is described and three others are considered as potential unintentional introductions to Australian waters, one of them reported for the first time for the continent. Pseudobranchiomma pallida sp. n. bears 4–6 serrations along the radiolar flanges, lacks radiolar eyes and has uncini with three transverse rows of teeth over the main fang. In the new species the colour pattern as well is characteristic and species specific.
new species, sabellids, feather duster worms, dichotomous key, taxonomy, invasive species, translocations
Pseudobranchiomma Jones, 1962 (Sabellidae, Annelida) is a heterogeneous worldwide-distributed genus of fan worms inhabiting shallow marine habitats. Their tubes are made of muddy sediment embedded into a mucous matrix usually attached to hard substrates. Some species of Pseudobranchiomma are considered fouling organisms, settling on artificial surfaces and in some cases are common in harbour environments (
Due to these attributes, some members of Pseudobranchiomma are susceptible to being translocated by attachment to ship hulls, and may settle in new locations, if environmental factors permit. Unintentional translocations have been assessed and are well documented in members of the related genus Branchiomma (e.g.
There are 16 species currently circumscribed within the genus (
Prior to the present study, Pseudobranchiomma has been reported from Australia as P. orientalis (
Pseudobranchiomma belongs to a group of sabellids possessing segmental eyespots between the noto- and neuropodia, spine-like chaetae arranged in oblique rows in the inferior thoracic fascicles, and well-developed conical abdominal neuropodia with chaetae arranged in C-shaped fascicles, together with Bispira Krøyer, 1856, Branchiomma Kölliker, 1858, Sabella Linnaeus, 1767, Sabellastarte Savigny, 1818 and Stylomma Knight-Jones, 1997 (e.g.
The aims of this study are (1) to assess monophyly of Pseudobranchiomma and relationships with other members of the clade - Bispira, Branchiomma, Sabella, Sabellastarte and Stylomma - integrating morphological data and available mitochondrial and nuclear sequences; (2) to test whether the artificial groups proposed by
Fourteen Pseudobranchiomma terminals, including at least two species of each of the groups proposed by
Matrix of morphological character states (‘–’, inapplicable; ‘?’, uncertain/unknown, V, variable).
Species | 1 | 5 | 10 | 15 | 20 | 25 | 30 | 33 | |||||||||||||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Pseudopotamilla cf. P. reniformis | 0 | 0 | 0 | - | 0 | 0 | 1 | 1 | 1 | 1 | 0 | 1 | 0 | 1 | 0 | 1 | 0 | 0 | 2 | 0 | 0 | 1 | 0 | 1 | 0 | 0 | 1 | 1 | 1 | 1 | 0 | 1 | ? |
Bispira manicata | 0 | 1 | 1 | 0 | 1 | 0 | 1 | 1 | 3 | 0 | - | 0 | 1 | 0 | 1 | 0 | 1 | 2 | 2 | 1 | 1 | 1 | 0 | 1 | 1 | 1 | 0 | 0 | 1 | 0 | 0 | 0 | 1 |
Bispira porifera | 0 | 1 | 0 | - | 0 | 0 | 1 | 0 | - | 1 | 0 | 0 | 1 | 1 | 1 | 0 | 1 | 0 | 2 | 1 | 1 | 1 | 0 | 1 | 1 | 1 | 0 | 0 | 1 | 0 | 0 | 0 | ? |
Bispira serrata | 0 | 1 | 1 | 1 | 0 | 0 | 1 | 1 | 3 | 1 | 0 | 0 | 1 | 1 | 1 | 0 | 1 | 0 | 2 | 1 | 1 | 0 | 0 | 1 | 1 | 1 | 0 | 0 | 0 | 0 | 0 | 1 | ? |
Branchiomma sp. 1 | 0 | 0 | 0 | - | 1 | 1 | 0 | 1 | 3 | 0 | - | 0 | 1 | 1 | 1 | 0 | 1 | 0 | 0 | 1 | 1 | 0 | 1 | 0 | 1 | 1 | 0 | 0 | 0 | 0 | 0 | 1 | 1 |
Branchiomma bairdi | 0 | 0 | 0 | - | 1 | 1 | 0 | 1 | 3 | 0 | - | 0 | 1 | 1 | 1 | 0 | 1 | 0 | 0 | 1 | 1 | 0 | 1 | 0 | 1 | 1 | 0 | 0 | 0 | 0 | 0 | 1 | 1 |
Sabella spallanzanii | 1 | 1 | 0 | - | 1 | 0 | 0 | 0 | - | 0 | - | 0 | 1 | 0 | 1 | 0 | 1 | 0 | 1 | 1 | 1 | 1 | 0 | 1 | 1 | 1 | 0 | 0 | 1 | 0 | 0 | 0 | 1 |
Sabella pavonina | 1 | 1 | 0 | - | 1 | 0 | 0 | 0 | - | 0 | - | 0 | 1 | 0 | 1 | 0 | 1 | 0 | 2 | 1 | 1 | 1 | 0 | 1 | 1 | 1 | 0 | 0 | 1 | 0 | 0 | 0 | 1 |
Sabellastarte australiensis | 1 | 1 | 0 | - | 0 | 0 | 1 | 0 | - | 1 | 0 | 0 | 1 | 0 | 0 | 1 | 1 | 0 | 0 | 1 | 1 | 1 | 0 | 0 | 1 | 1 | 0 | 0 | 1 | 0 | 1 | 0 | 1 |
Sabellastarte sp. | 1 | 1 | 0 | - | 0 | 0 | 1 | 0 | - | 1 | 0 | 0 | 1 | 0 | 0 | 1 | 1 | 0 | 0 | 1 | 1 | 1 | 0 | 0 | 1 | 1 | 0 | 0 | 1 | 0 | 1 | 0 | 1 |
Stylomma palmatum | 0 | 1 | 1 | 0 | 0 | 0 | 1 | 1 | 2 | 1 | 1 | 0 | 0 | 0 | 0 | 0 | 1 | 0 | 0 | 1 | 1 | 1 | 0 | 1 | 1 | 1 | 0 | 0 | 1 | 0 | 0 | 0 | ? |
Stylomma juani | 0 | 1 | 1 | 1 | 0 | 0 | 1 | 1 | 0 | 1 | 1 | 0 | 0 | 0 | 0 | 0 | 1 | 0 | 0 | 1 | 1 | 1 | 0 | 1 | 1 | 1 | 0 | 0 | 1 | 0 | 0 | 0 | ? |
P. emersoni | 0 | 0 | 1 | 1 | ? | 0 | 0 | 0 | - | 0 | - | 0 | 1 | 0 | 1 | 0 | 1 | 1 | 2 | 1 | 1 | 0 | 1 | 0 | 1 | 1 | 0 | 0 | 0 | 0 | 0 | 1 | 1 |
P. cf. P. emersoni (Australia) | 0 | 0 | 1 | 1 | 1 | 0 | 0 | 0 | - | 0 | - | 0 | 1 | 0 | 1 | 0 | 1 | 1 | 2 | 1 | 1 | 0 | 1 | 0 | 1 | 1 | 0 | 0 | 0 | 0 | 0 | 1 | ? |
P. minima | 0 | 0 | 0 | - | 1 | 0 | 0 | 0 | - | 0 | - | 0 | 1 | 0 | 1 | 0 | 1 | 1 | 1 | 1 | 1 | 0 | 1 | 0 | 1 | 1 | 0 | 0 | 0 | 0 | 0 | ? | 1 |
P. orientalis | 0 | 1 | 1 | 1 | 1 | 0 | ? | 0 | - | 0 | - | 0 | 1 | 0 | 1 | 0 | 1 | 0 | 2 | 1 | 1 | 0 | 1 | 0 | 1 | 1 | 0 | 0 | 0 | 0 | 0 | 1 | ? |
P. cf. P. orientalis (Australia) | 0 | 1 | 1 | 1 | 1 | 0 | 1 | 0 | - | 0 | - | 0 | 1 | 0 | 1 | 0 | 1 | 0 | 2 | 1 | 1 | 0 | 1 | 0 | 1 | 1 | 0 | 0 | 0 | 0 | 0 | 1 | ? |
P. pallida sp. n. | 0 | 0 | 1 | 1 | 0 | 0 | 0 | 0 | - | 0 | - | 0 | 1 | 0 | 1 | 0 | 1 | 1 | 1 | 1 | 1 | 0 | 1 | 0 | 1 | 1 | 0 | 0 | 0 | 0 | 0 | ? | ? |
P. paraemersoni | 0 | 0 | 1 | 1 | 1 | 0 | 0 | 0 | - | 0 | - | 0 | 1 | 0 | 1 | 0 | 1 | 1 | 2 | 1 | 1 | 0 | 1 | 0 | 1 | 1 | 0 | 0 | 0 | 0 | 0 | ? | ? |
P. paulista | 0 | 0 | 1 | 1 | 1 | 0 | 0 | 0 | - | 0 | - | 0 | 1 | ? | 1 | 0 | 1 | V | 2 | 1 | 1 | 0 | 1 | 0 | 1 | 1 | 0 | 0 | 0 | 0 | 0 | ? | ? |
P. perkinsi | 0 | 0 | 0 | - | 0 | 0 | 0 | 1 | 3 | 0 | - | 0 | 1 | 0 | 1 | 0 | 1 | 2 | 2 | 1 | 1 | 0 | 1 | 0 | 1 | 1 | 0 | 0 | 0 | 0 | 0 | 1 | 1 |
P. punctata | 0 | 1 | 0 | - | 1 | 0 | 1 | 0 | - | 1 | 0 | 0 | 1 | 0 | 1 | 1 | 1 | 1 | 0 | 1 | 1 | 0 | 1 | 0 | 1 | 1 | 0 | 0 | 0 | 0 | 0 | ? | 1 |
P. serratibranchis | 0 | 0 | 1 | 1 | 1 | 0 | 0 | ? | ? | ? | - | 0 | 1 | 0 | 1 | 0 | 1 | 0 | 0 | 1 | 1 | ? | 1 | 0 | 1 | 1 | 0 | 0 | 0 | 0 | 0 | ? | ? |
P. schizogenica | 0 | 1 | 1 | 1 | 1 | 0 | ? | 0 | - | 0 | - | 0 | 1 | 0 | 1 | 0 | 1 | 1 | 2 | 1 | 1 | 0 | 1 | 0 | 1 | 1 | 0 | 0 | 0 | 0 | 0 | 1 | 1 |
P. cf. P. schizogenica (Australia) | 0 | 1 | 1 | 1 | 1 | 0 | 0 | 0 | - | 0 | - | 0 | 1 | 0 | 1 | 0 | 1 | 1 | 2 | 1 | 1 | 0 | 1 | 0 | 1 | 1 | 0 | 0 | 0 | 0 | 0 | 1 | 1 |
P. tarantoensis | 0 | 0 | 0 | - | 1 | 0 | 1 | 0 | - | 0 | - | 0 | 1 | 0 | 1 | 0 | 1 | 0 | 1 | 1 | 1 | 1 | 1 | 0 | 1 | 1 | 0 | 0 | 0 | 0 | 0 | 1 | 0 |
Morphological characters and states scored in the matrix (Table
1. | Lobes: (0) semicircular or involuted; (1) spiral. |
2. | Basal membrane: (0) absent (or reduced, shorter than one thoracic segment); (1) present (longer than one thoracic segment). |
3. | Radiolar flanges: (0) absent or reduced to ridges; (1) present. |
4. | Serrations of radiolar flanges: (0) absent; (1) present. |
5. | Transverse pigment bands on radioles: (0) absent; (1) present. |
6. | Stylodes: (0) absent; (1) present. |
7. | Number of rows of vacuolated cells supporting radioles: (0) four; (1) more than four. |
8. | Radiolar eyes: (0) absent; (1) present. |
9. | Radiolar eyes arrangement: (0) ocelli; (1) unpaired proximal compound eyes on radiole dorsal margin; (2) unpaired terminal compound eyes on inner peduncule; (3) paired compound eyes; |
10. | Dorsal basal flanges: (0) absent; (1) present. |
11. | “Press-stud” structure present on dorsal basal flanges: (0) absent; (1) present. |
12. | Ventral basal flanges: (0) absent; (1) present. |
13. | Dorsal lip radiolar appendage vacuolated cells (skeleton): (0) absent; (1) present. |
14. | Dorsal pinnular appendages: (0) absent; (1) present. |
15. | Position of ventral sacs: (0) inside the radiolar crown; (1) outside the radiolar crown. |
16. | Dorsal margin of posterior peristomial ring collar: (0) widely separated; (1) fused to the faecal groove. |
17. | Interramal eyespots: (0) absent; (1) present. |
18. | Number of thoracic segments: (0) 8; (1) generally less than 8; (2) generally more than 8. |
19. | Gap between thoracic tori and ventral shields: (0) absent, all ventral shields in contact with tori; (1) gap between ventral shields and tori of anterior thoracic segments; (2) present, gap in all thoracic segments. |
20. | Thoracic chaetal fascicles (notopodia): (0) transverse rows; (1) longitudinal bundles. |
21. | Inferior thoracic notochaetae shape: (0) paleate; (1) spine-like. |
22. | Rows of teeth on thoracic uncini: (0) few (1–5); (1) numerous (>5). |
23. | Length of thoracic uncini handles: (0) medium length (more than distance from breast to tip of main fang); (1) short (shorter than distance of breast to tip of main fang). |
24. | Thoracic companion chaetae: (0) absent; (1) present. |
25. | Abdominal neurochaetal tori: (0) transverse ridges; (1) conical lobes. |
26. | Abdominal neurochaetal fascicles: (0) transverse row(s); (1) spiralled. |
27. | Superior row of abdominal neurochaetal fascicles: (0) elongated narrowly hooded; (1) broadly hooded. |
28. | Inferior row of abdominal chaetae: (0) spine-like; (1) broadly hooded. |
29. | Abdominal uncini number of rows: (0) few (1–5); (1) numerous (>5). |
30. | Abdominal uncini breast: (0) well developed, expanded; (1) narrow, swelling. |
31. | Length of abdominal uncini handles: (0) short (shorter than distance of breast to tip of main fang); (1) medium (1–2 times distance of breast to tip of main fang). |
32. | Pygidial shape: (0) rim; (1) bilobed. |
33. | Scissiparity: (0) absent; (1) present. |
More than 100 specimens deposited in Australian museum collections were examined and identified to species to assess the species diversity in Australian waters. These included specimens identified for the Darwin Ports Survey and mentioned in the report by
Comparison of species from Group A (according to
TAXON | Distribution | Radiolar eyes | Radioles (pairs) | Radiolar serrations (pairs) | Radiolar lobes | Dorsal lips/crown length | Crown pigment | Body pigment alive (preserved) | Interramal eyespots | Thoracic tori and ventral shields | Thoracic segments | Teeth thoracic uncini |
---|---|---|---|---|---|---|---|---|---|---|---|---|
P. emersoni Jones, 1962 | Jamaica, Florida (USA), Cape Verde Islands? | no | 14† | 10 | semicircular? | 1/4 | irregular | brownish with spots (same) | large† | gap† | 4–6 (8‡) | 5 (5–6)† |
P. cf. P. emersoni | Queensland, Australia | no | 17 | 10 | semicircular | 1/6 | irregular | pale with large anterior spots | small | gap | 7 | 3 |
P. grandis (Baird, 1865) | New Zealand | yes‡, §, ¶ | >10 (≤30)¶ | ? (>18)¶ | semicircular | ? | 9 (4–9)¶ irregular bands | pale with brown/purple spots¶ (dark brown) | small¶ | Almost in contact¶ | 7 (8)¶ | ? |
P. serratibranchis (Grube, 1878) | Philippines | yes‡, § | 17 | 30 | semicircular- | ? | 7–8 bands | ? | ? | ? | 8 | ? |
P. orientalis (McIntosh, 1885) | Hong Kong | no | 26 | 13–16† | involuted | 1/4† | 23 bands | internal purple-brown spots on ventral lappets (colourless#) | present only in abdomen | gap# | 8†,# | 6–7 (4–5)† |
P. cf. P. orientalis | Queensland, and Northern Territory, Australia | no | 10–30 | 10–20 | involuted~1 whorl | 1/6–1/3 | 10–20 bands | (pale with few anterior spots) | tiny | gap | 7–8 | 5–7 |
P.
paraemersoni
|
São Paulo, Brazil | no | 6 | 3–4 | semicircular | 1/4 | 3–4 bands | bright yellow with few spots (white) | large | gap | 4–5 | 4–5 |
P.
paulista
|
São Paulo, Brazil | no | 22–25 | 13–19 | semicircular | 1/6 | 10–19 bands | pale yellow with purple spots (white with spots) | small | gap | 6–10 | 4–5 |
P. pallida sp. n. | Queensland, Australia | no | 9 | 4–5 | semicircular | 1/6 | No banding | colourless | large | gap | 7 | 3 |
P. schizogenica Tovar-Hernández and Dean, 2014 | Gulf of California, Mexico | no | 6–9 | 6–11 | semicircular | 1/4 | 4 or more purple bands with orange and translucent bands between | bright yellow with few purple spots (pale yellow) | large | ? | 5 | 4 |
P. cf. P. schizogenica | North Australia and Hawaii | no | 9 | 4–6 | semicircular | 1/3 | 4–6 bands and orange band in base | pale with spots | large | gap | 4–7 | 3 |
Genomic DNA was extracted from sample tissue using standard protocols for the DNeasy Animal tissues protocol (manufactured by QIAGEN Pty Ltd). Sections of two mitochondrial genes cytochrome b (cob) and cytochrome oxidase I (cox1), and one nuclear gene ribosomal internal transcribed spacer 1 (ITS1), were then amplified using the primers Cytb 424F (RT-1) and cobr825 (Burnette et al. 2005) for cob, HCO2198 and LCO1490 (
Taxa and GenBank accession numbers for the genes sequenced for the present study. NSW, New South Wales; NT, Northern Territory, QLD, Queensland; SA, South Australia; WA, Western Australia.
Taxon | Voucher | cox1 | cob | ITS1 | Locality |
---|---|---|---|---|---|
Pseudopotamilla cf. P. reniformis |
|
KX894903 | KX894900 | KX894909 | Darwin, NT, Australia |
Branchiomma sp. |
|
– | KF429111 | KX894915 | Oahu, Hawaii, USA |
Branchiomma bairdi |
|
KP254646 | KF429105 | KF459971 | Fort Pierce, Florida, USA |
Bispira serrata |
|
KX894907 | – | KX894916 | Lizard Island, QLD, Australia |
Bispira manicata |
|
KX894904 | KX894902 | KX894910 | Aquarium at Oceanword, NSW, Australia |
Sabella spallanzanii |
|
KX894905 | – | – | SA, Australia |
Stylomma palmatum |
|
KX894908 | KX894901 | KX894914 | Ningaloo Reef, WA, Australia |
Sabellastarte australiensis |
|
– | KF429134 | KF460007 | Cape Banks, NSW, Australia |
Sabellastarte sp. |
|
KX894906 | – | KX894913 | Port Phillip Bay, VIC, Australia |
Pseudobranchiomma pallida sp. n. |
|
– | – | KX894911 | Heron Island, QLD, Australia |
P. cf. P. schizogenica (Australia) |
|
– | – | KX894912 | Heron Island, QLD, Australia |
P. cf. P. schizogenica (Hawaii) |
|
– | KF429108 | KF459975 | Oahu, Hawaii, USA |
Nucleotide sequences of cob, cox1 and ITS1 were aligned with MAFFT v. 6.0 (
Maximum parsimony (MP) heuristic searches used 10,000 replicates of random taxon addition and tree bisection-reconnection (TBR) branch swapping algorithm, saving 100 trees per replicate using TNT 1.1 (
Maximum likelihood (ML) analyses were conducted using RAxML (
Species | 1 | 5 | 10 | 15 | 20 | 25 | 30 | 33 | |||||||||||||||||||||||||
Pseudopotamilla cf reniformis | 0 | 0 | 0 | - | 0 | 0 | 1 | 1 | 1 | 1 | 0 | 1 | 0 | 1 | 0 | 1 | 0 | 0 | 2 | 0 | 0 | 1 | 0 | 1 | 0 | 0 | 1 | 1 | 1 | 1 | 0 | 1 | ? |
Bispira manicata | 0 | 1 | 1 | 0 | 1 | 0 | 1 | 1 | 3 | 0 | - | 0 | 1 | 0 | 1 | 0 | 1 | 2 | 2 | 1 | 1 | 1 | 0 | 1 | 1 | 1 | 0 | 0 | 1 | 0 | 0 | 0 | 1 |
Bispira serrata | 0 | 1 | 1 | 1 | 0 | 0 | 1 | 1 | 3 | 1 | 0 | 0 | 1 | 1 | 1 | 0 | 1 | 0 | 2 | 1 | 1 | 0 | 0 | 1 | 1 | 1 | 0 | 0 | 0 | 0 | 0 | 1 | ? |
Branchiomma sp. | 0 | 0 | 0 | - | 1 | 1 | 0 | 1 | 3 | 0 | - | 0 | 1 | 1 | 1 | 0 | 1 | 0 | 0 | 1 | 1 | 0 | 1 | 0 | 1 | 1 | 0 | 0 | 0 | 0 | 0 | 1 | 1 |
Branchiomma bairdi | 0 | 0 | 0 | - | 1 | 1 | 0 | 1 | 3 | 0 | - | 0 | 1 | 1 | 1 | 0 | 1 | 0 | 0 | 1 | 1 | 0 | 1 | 0 | 1 | 1 | 0 | 0 | 0 | 0 | 0 | 1 | 1 |
Sabella spallanzanii | 1 | 1 | 0 | - | 1 | 0 | 0 | 0 | - | 0 | - | 0 | 1 | 0 | 1 | 0 | 1 | 0 | 1 | 1 | 1 | 1 | 0 | 1 | 1 | 1 | 0 | 0 | 1 | 0 | 0 | 0 | 1 |
Sabellastarte sp. | 1 | 1 | 0 | - | 0 | 0 | 1 | 0 | - | 1 | 0 | 0 | 1 | 0 | 0 | 1 | 1 | 0 | 0 | 1 | 1 | 1 | 0 | 0 | 1 | 1 | 0 | 0 | 1 | 0 | 1 | 0 | 1 |
Stylomma palmatum | 0 | 1 | 1 | 0 | 0 | 0 | 1 | 1 | 2 | 1 | 1 | 0 | 0 | 0 | 0 | 0 | 1 | 0 | 0 | 1 | 1 | 1 | 0 | 1 | 1 | 1 | 0 | 0 | 1 | 0 | 0 | 0 | ? |
P. pallida sp. n. | 0 | 0 | 1 | 1 | 0 | 0 | 0 | 0 | - | 0 | - | 0 | 1 | 0 | 1 | 0 | 1 | 1 | 1 | 1 | 1 | 0 | 1 | 0 | 1 | 1 | 0 | 0 | 0 | 0 | 0 | ? | ? |
P. cf P. schizogenica (Australia) | 0 | 1 | 1 | 1 | 1 | 0 | 0 | 0 | - | 0 | - | 0 | 1 | 0 | 1 | 0 | 1 | 1 | 2 | 1 | 1 | 0 | 1 | 0 | 1 | 1 | 0 | 0 | 0 | 0 | 0 | 1 | 1 |
P. cf P. schizogenica (Hawaii) | 0 | 1 | 1 | 1 | 1 | 0 | 0 | 0 | - | 0 | - | 0 | 1 | 0 | 1 | 0 | 1 | 1 | 2 | 1 | 1 | 0 | 1 | 0 | 1 | 1 | 0 | 0 | 0 | 0 | 0 | 1 | 1 |
Maximum parsimony analyses of the complete morphological matrix (Table
Phylogenetic hypothesis of Pseudobranchiomma and related taxa. A Strict consensus of six most-parsimonious trees after analyses of morphological data (33 characters) and 26 members of Sabellidae rooted with Pseudopotamilla. Jack-knife support values are given (>50) B Strict consensus of three most parsimonious tree after implementation of implied weighting (constant of concavity k = 7) C Tree after maximum likelihood analyses of mitochondrial and nuclear dataset. Bootstrap values on nodes if >50; scale: average of nucleotide substitutions per site D Single most-parsimonious tree after analyses of the combined morphological and molecular datasets (12 taxa and 2239 characters); Jack-knife support values are given (>50).
The low success obtaining sequences out of tissue from members of Pseudobranchiomma (only three terminals belonging to two morphospecies), restricted the outcomes of the present study. Analyses of the combined molecular dataset yielded a phylogenetic hypothesis where Pseudobranchiomma was monophyletic and sister to Sabella + Sabellastarte (Fig.
Pseudobranchiomma
Jones, 1962: 198–201, figs 115–124;
Pseudobranchiomma emersoni Jones, 1962.
Radioles with or without radiolar flanges, serrated or smooth. Some species with paired compound eyes along radioles. Four rows of vacuolated cells supporting the radioles; a multicellular supporting axis of the radiolar appendages of the dorsal lips. Ventral sacs located outside the radiolar crown. Dorsal margins of collar separated from the faecal groove by a wide gap and without “pockets”. Segmental eyespots between the noto- and neuropodia. Spine-like chaetae arranged in oblique rows in the inferior thoracic fascicles. Thoracic companion chaetae absent. Well-developed conical abdominal neuropodia with chaetae arranged in C-shaped fascicles.
There is no apparent morphological synapomorphy supporting Pseudobranchiomma. The monophyly of the genus Pseudobranchiomma has not been tested prior to this study. The group has been defined by a combination of homoplastic characters: presence of radiolar flanges (shared with Stylomma and some Bispira species but absent in P. longa (Kinberg, 1867)); ventral sacs located outside the radiolar crown (shared with Bispira, Branchiomma and Sabella); dorsal margins of the collar separated from the faecal groove by a wide gap and without “pockets” (shared by Bispira, Stylomma and some species of Branchiomma); and absence of thoracic companion chaetae (shared with Branchiomma and Sabellastarte) (e.g.
? Pseudobranchiomma emersoni
Jones, 1962:198–201, figs 115–124;
Australia: Queensland:
Ten pairs of short flat radiolar serrations evenly distributed along entire length of radioles. RRadiolar eyes absent. Small gap between anterior thoracic ventral shields and neuropodial tori. Thoracic and abdominal uncini with five transverse rows of teeth surmounting main fang. Radiolar crown with wide purple band at base, irregular transverse purple bands on radioles and flanges and yellow band on distal end of radioles. Body pale with distinct interramal eyespots and purple pigment spots on thorax and dorsally on abdomen.
Gravid female, incomplete; body measuring 20 mm long and 2 mm wide, with seven thoracic (Fig.
Pseudobranchiomma cf. P. emersoni
Line drawings of chaetae and uncini of Pseudobranchiomma species in Australia; A–F Pseudobranchiomma cf. P. emersoni G–L Pseudobranchiomma cf. P. orientalis M–T Pseudobranchiomma pallida sp. n. U–Z, A1 Pseudobranchiomma cf. P. schizogenica; A Thoracic uncinus B Abdominal uncinus C Superior thoracic chaeta D Inferior thoracic chaeta E, F Inferior abdominal chaetae G Thoracic uncinus H Abdominal uncinus I Superior thoracic chaeta J Inferior thoracic chaeta K, L Inferior abdominal chaetae M, N Thoracic uncini O Abdominal uncinus P, Q, R Inferior thoracic chaetae S Superior abdominal chaeta T Inferior abdominal chaeta U, V Thoracic uncini W Abdominal uncinus X, Y Superior thoracic chaetae Z, A1 Inferior thoracic chaetae. Scale bars: A–F = 2 µm; G–L = 4 µm; M–T = 2 µm; U–Z, A1 = 2 µm.
Body pale with distinct interramal eyespots of same size in thorax and abdomen (Fig.
Pseudobranchiomma emersoni Jones, 1962 is a species that was originally described from Jamaica, but has also been reported from the Cape Verde Islands (according to
Species known from Jamaica, Florida (USA), Cape Verde Islands, and now Heron Island, Queensland, Australia, where it inhabits coral rubble at shallow depths.
? Dasychone orientalis McIntosh, 1885: 498—500, pl. LII, fig 5, Pl.XXXA, figs 19–21, pl. XXXIXA, fig 4.
? Pseudobranchiomma orientalis
:
Australia: Queensland:
Ten to 25 serrations evenly distributed along entire length of radiolar flanges, Radiolar eyes absent. Thoracic ventral shields and uncinal tori separated by a small gap. Thoracic and abdominal uncini with 5–7 transverse rows of teeth over main fang. Radiolar crown with broad purple basal band, and approximately 20 transverse purple pigment bands along radioles, interspersed with orange and thin white bands; body with few pigment spots and with small, indistinct interramal eyespots.
Specimens 5–24 mm long (with 12 mm long crown on longest specimen), 3 mm maximum width; 7–8 thoracic and 50 abdominal chaetigers. Crown strongly involuted ventrally (Figs
Pseudobranchiomma cf. P. orientalis
Pseudobranchiomma cf. P. orientalis
Preserved specimens may have few pigment spots on body, with some pigment on end of the faecal groove and dark patches on bases of ventral lappets, internally. Crown with pigments units coinciding with serrations, about 20 thin transverse purple-brown bands on outer side of radioles and flanges, continuing in one or two pinnules, and orange and white bands in between, which may fade (Fig.
These Australian specimens are identified as P. cf. P. orientalis, a species originally described from Hong Kong. Knight-Jones reviewed, and illustrated the types (previously unpublished but shared with MC and reproduced here as Fig.
Pseudobranchiomma orientalis Type BMNH 85.12.1.393. Line drawings by Phyllis Knight-Jones. A–C Second dorsal radiole from different views D Holotype, divided in two, and partially covered by the tube, lateroventral view E Base of crown and anterior thoracic chaetigers, ventral view F Same, lateral view G Same, dorsal view H Thoracic parapodium I Abdominal parapodium. Scale bars: A–C = 1 mm; D = 2 mm; E–G = 1 mm; H–I = unknown.
Pacific Ocean (Hong Kong, Australia: Northern Territory and Queensland).
Australia, Queensland. Holotype
Approximately six pairs of low serrations evenly distributed along radiolar flanges. Radiolar eyes absent. Thoracic ventral shield separated from uncinal tori. Uncini with three transverse rows of teeth over main fang. Radiolar crown with broad purple band at base and distal third with wide yellow band, rest colourless white bands; body pale with distinct interramal eyespots.
Specimen incomplete; body measuring 10 mm long (including crown) and 1 mm wide, with six thoracic and more than 18 abdominal segments (Fig.
Pseudobranchiomma pallida sp. n.
Body pale with distinct interramal eyespots (Fig.
Pseudobranchiomma pallida sp. n. is characterised by the remarkable colour pattern of the radiolar crown with a purple basal band and yellow radiolar tips, instead of the characteristic bands, as well as the absence of pigment spots on the body. This species belongs to the artificial Group A of
Australia (Queensland, Heron Island).
This species is named after its colour pigmentation, pale compared with other Pseudobranchiomma species, and completely lacking pigment spots on the body.
Pseudobranchiomma schizogenica Tovar-Hernández & Dean, 2014: 936–945, figs 1–5.
Australia: Queensland:
Hawaii:
Three to six pairs of digitiform radiolar serrations evenly distributed along entire length of radioles. Radiolar eyes absent. Thoracic ventral shields and neuropodial tori separated by a gap. Thoracic and abdominal uncini with about four transverse rows of teeth surmounting main fang. Radiolar crown with transverse dark purple and orange bands at base and 4–6 irregular purple bands along radioles. Body pale, or with some purple patches; large interramal eyespots decreasing posteriorly.
Specimens range from 3–19 mm long, 0.2–1 mm wide, with 4–7 thoracic and numerous abdominal segments. One complete specimen from
Pseudobranchiomma cf. P. schizogenica.
Pseudobranchiomma cf. P. schizogenica. Scanning electron micrographs. A–F specimen from Queensland
Pseudobranchiomma cf. P. schizogenica from Hawaii
Body pale with large interramal eyespots (Fig.
This species, originally described from the Gulf of California, is characterised by having radioles with short and digitiform serrations along the entire radiolar length, ventral shield of collar trapezoidal and divided into two halves, thoracic superior chaetae and abdominal chaetae with hoods narrower than shafts and thoracic inferior chaetae spine-like with hoods as wide as shafts (
Southern Gulf of California (Mexico), northern Australia and Hawaii. This species is associated with coral rubble and epifauna attached to hard substrates in shallow depths (0–15 m).
The number of Pseudobranchiomma species considered as currently valid (17) follows
1 | Radioles with distinct, paired, serrated flanges | 2 |
– | Radioles with flanges reduced to low ridges (lacking distinct serrations) | 9 |
2 | Serrations distinct along most (or all) length of radioles | 3 |
– | Serrations only distinct on distal parts of radioles | 7 |
3 | Radioles with paired compound eyes present |
P. grandis (Baird, 1865) (New Zealand) (Fig. |
– | Radioles without distinct radiolar eyes | 4 |
4 | Radioles with over 10 pairs of serrations on lateral flanges | 5 |
– | Radioles with maximum of 10 pairs of serration on lateral flanges | 6 |
5 | Radioles with up to 25 serrations and coloured transverse bands; thorax generally with 8 thoracic chaetigers; thoracic uncini with 6–7 rows of teeth | P. orientalis (McIntosh, 1885) (Hong Kong) |
– | Radioles with 13–19 serrations and 10–19 transverse pigmented bands; thorax with 6–10 thoracic chaetigers; 4–5 rows of teeth in thoracic uncini |
P. paulista |
6 | Radiolar crown without pigmented transverse dark bands; radiolar lobes pigmented with purple and radioles white with yellow tips. Radioles with six serrations along their length; three rows of teeth above main fang of thoracic uncini | P. pallida sp. n. (Australia) |
– | Radiolar crown with several pigmented transverse bands (regular or irregular) | 7 |
7 | Radioles with up to 10 serrations and 10 narrow irregular purple bands; thorax with 4–8 chaetigers; 5–6 rows of teeth above main fang of thoracic uncini | P. emersoni Jones, 1962 (Caribbean) |
– | Radioles with 3–4 serrations and transverse bands (purple and yellow; a few white); thorax with 4–5 thoracic chaetigers; 4–5 rows of teeth above main fang of thoracic uncini |
P. paraemersoni |
– | Radioles with 6–11 serrations and 4–6 transverse bands (of purple-orange-white); four rows of teeth above main fang of thoracic uncini; lateral margins of collar oblique and covering anterior peristomial ring |
P. schizogenica |
8 | Radiolar eyes reportedly* present | P. odhneri (Fauvel, 1921) (Madagascar) or* P. bocki (Johansson, 1922) (Japan) |
– | Radiolar eyes absent | 8 |
9 | Radiolar crown with 12 dark pigment bands (and 7 wide yellow bands between) | P. tricolor (Grube, 1881) (Japan) |
– | Radiolar crown whitish, darker at base, lacking transverse pigmented bands; thorax with eight thoracic chaetigers; thoracic uncini with over five rows of teeth | P. zebuensis (McIntosh, 1885) (Philippines) |
10 | Peristomial collar fused dorsally to sides of faecal groove | P. punctata (Treadwell, 1905) (Hawaii) |
– | Collar with free dorsal margins, widely separated from faecal groove | 10 |
11 | Radioles with paired compound eyes | 11 |
– | Radioles without distinct compound eyes (may have granular pigment patches) | 12 |
12 | Thorax broader than long (with up to 8 thoracic chaetigers); each side of crown in spiral of up to 5 whorls (mature specimens) | P. longa (Kinberg, 1867) (South Africa) |
– | Thorax longer than broad (with up to 13 thoracic chaetigers); radiolar lobes never spiralled | P. perkinsi Knight-Jones & Giangrande, 2003 (Florida) |
13 | Thorax with 4–6 segments; first thoracic chaetiger less than 1.5 times length of the following ones | P. minima Nogueira & Knight-Jones, 2002 (Brazil) |
– | Thorax with 8 segments; first thoracic chaetiger 2–3 times length of the following ones | P. tarantoensis Knight-Jones & Giangrande, 2003 (Italy) |
The genus Pseudobranchiomma was erected based on the short thorax (with less than the usual eight thoracic chaetigers), absence of compound radiolar eyes (unlike members of Branchiomma and some Bispira), and the presence of ‘reduced stylodes’ (
Relationships within the genus indicate that the groups proposed by
In this study, a new species, Pseudobranchiomma pallida sp. n., is herein described, and another species, P. cf. P. schizogenica is reported in Australia for the first time, an indication that the group is more diverse than previously considered. Nevertheless, this diversity could be due, in part, to unintentional translocations. Some specimens in this study could be assigned to three species, P. cf. P. emersoni, P. cf. P. orientalis and P. cf. P. schizogenica, originally described from distant and disjunct geographic areas (Jamaica, Southern Gulf of California and Hong Kong, respectively) but also reported from other worldwide localities (
The specimens examined and included in this study were mainly collected during the CReefs surveys (Census of Marine Life) and the Polychaete Workshop 2013 at Lizard Island. We would like to thank Julian Caley, Pat Hutchings, Lena Kupriyanova, Anne Hoggett and Lyle Vail for organising these expeditions and BHP Billiton and the Lizard Island Reef Research Foundation for funding. Robin Wilson, Skipton Woolley and Elizabeth Greaves helped with collecting in Melbourne. We gratefully acknowledge Phyllis Knight-Jones who provided unpublished description and drawings of P. orientalis and also thank Joao M. M. Nogueira for his useful comments and sending Brazilian specimens of Pseudobranchiomma for comparison. We would like to thank Michelle Yerman who helped photograph specimens and with early stages of this project and Sue Lindsay who assisted with SEM, and Hannelore Paxton for German translations. We also thank Chris Glasby and Sue Horner for the loan of specimens from Museum and Art Gallery of Northern Territory, and Geoff Read (NIWA, New Zealand) for his generous help with features of P. grandis, as well as the Cawthron Institute New Zealand, and Rod Asher (Biolive, New Zealand) for the use of his live photographs of this species. Thanks to Willi Hennig Society for the use of TNT v1.1.