Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Invertebrate Systematics Invertebrate Systematics Society
Systematics, phylogeny and biogeography
RESEARCH ARTICLE

The ‘giant phyllosoma’ are larval stages of Parribacus antarcticus (Decapoda : Scyllaridae)

Ferran Palero A F , Guillermo Guerao B , Michael Hall C , Tin Yam Chan D and Paul F. Clark E
+ Author Affiliations
- Author Affiliations

A Unitat Mixta Genòmica i Salut CSISP-UV, Institut Cavanilles, Universitat de Valencia, C/Catedrático Jose Beltran 2, 46980 Paterna, Spain.

B IRTA, Unitat de Cultius Aqüàtics, Sant Carles de la Ràpita, Tarragona, Catalonia, Spain.

C Australian Institute of Marine Science, PMB No. 3, Townsville MC, Townsville, QLD 4810, Australia.

D Institute of Marine Biology and Center of Excellence for the Oceans, National Taiwan Ocean University, Keelung 20224, Taiwan, ROC.

E Department of Life Sciences, The Natural History Museum, Cromwell Road, London SW7 5BD, England, UK.

F Corresponding author. Email: ferran.palero@uv.es

Invertebrate Systematics 28(3) 258-276 https://doi.org/10.1071/IS13037
Submitted: 25 November 2013  Accepted: 3 February 2014   Published: 30 June 2014

Abstract

Early reports on larval distributions are frustratingly obscure due to ambiguous identification of plankton samples. A particularly striking case is posed by the so-called ‘giant phyllosoma’ which attain 80 mm in total length and are among the largest larvae known in marine invertebrates. Based on the supposition that these giant larvae are produced by local species, Philip Robertson (1968) assigned them to Parribacus. In the present study, 12 phyllosoma larvae collected in the Coral Sea and corresponding to intermediate stages VI to IX are described in detail. The identity of these freshly caught specimens was confirmed as belonging to Parribacus antarcticus (Lund, 1793) by using DNA barcoding methods. This new collection further allowed us to complete the larval series for the genus. The intermediate stage VI, which was missing in previous accounts, is described here for the first time. Besides the Coral Sea larvae, another five phyllosoma specimens previously deposited in UK and German museum collections are also described. Given that no useful DNA could be obtained from the old collection specimens, these larvae were identified as Parribacus sp. based on morphology only. Furthermore, a complete morphometric analysis of Parribacus larvae was undertaken including information from literature dating back to 1830. The first detailed description of all dactyli from a complete phyllosoma of the genus Parribacus is presented, with further comparison with those from other genera of Scyllaridae.

Additional keywords: DNA barcoding, ‘giant larvae’, Scyllaridae, slipper lobster.


References

Atkinson, J. M., and Boustead, N. C. (1982). The complete larval development of the scyllarid lobster Ibacus alticrenatus Bate, 1888 in New Zealand waters. Crustaceana 42, 275–287.
The complete larval development of the scyllarid lobster Ibacus alticrenatus Bate, 1888 in New Zealand waters.Crossref | GoogleScholarGoogle Scholar |

Baisre, J. A. (1994). Phyllosoma larvae and the phylogeny of Palinuroidea (Crustacea: Decapoda): a review. Australian Journal of Marine and Freshwater Research 45, 925–944.
Phyllosoma larvae and the phylogeny of Palinuroidea (Crustacea: Decapoda): a review.Crossref | GoogleScholarGoogle Scholar |

Booth, J. D., Webber, W. R., Sekiguchi, H., and Coutures, E. (2005). Diverse larval recruitment strategies within the Scyllaridae. New Zealand Journal of Marine and Freshwater Research 39, 581–592.
Diverse larval recruitment strategies within the Scyllaridae.Crossref | GoogleScholarGoogle Scholar |

Boxshall, G. A., and Damià, J. (2009). Exopodites, epipodites and gills in crustaceans. Arthropod Systematics & Phylogeny 67, 229–254.

Bracken-Grissom, H. D., Felder, D. L., Vollmer, N. L., Martin, J. W., and Crandall, K. A. (2012). Phylogenetics links monster larva to deep-sea shrimp. Ecology and Evolution 2, 2367–2373.
Phylogenetics links monster larva to deep-sea shrimp.Crossref | GoogleScholarGoogle Scholar | 23145324PubMed |

Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17, 540–552.
Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXisVSgt7g%3D&md5=b9e72f4f43e92e5aaa6c2696c6b069dbCAS | 10742046PubMed |

Clark, P. F., Calazans, D. K., and Pohle, G. W. (1998). Accuracy and standardization of brachyuran larval descriptions. Invertebrate Reproduction & Development 33, 127–144.
Accuracy and standardization of brachyuran larval descriptions.Crossref | GoogleScholarGoogle Scholar |

Coutures, E. (2001). On the first phyllosoma stage of Parribacus caledonicus Holthuis, 1960, Scyllarides squammosus (H. Milne-Edwards, 1837) and Arctides regalis Holthuis, 1963 (Crustacea, Decapoda, Scyllaridae) from New Caledonia. Journal of Plankton Research 23, 745–751.
On the first phyllosoma stage of Parribacus caledonicus Holthuis, 1960, Scyllarides squammosus (H. Milne-Edwards, 1837) and Arctides regalis Holthuis, 1963 (Crustacea, Decapoda, Scyllaridae) from New Caledonia.Crossref | GoogleScholarGoogle Scholar |

Dana, J. D. (1852). Conspectus Crustaceorum quae in Orbis Terrarum circumnavigatione, Carolo Wilkes e Classe Reipublicas Foederatae Duce, lexit et descripsit. Proceedings Academy Natural Sciences Philadelphia, 6, 6–10, 10–28, 73–86.

Drummond, A. J., Suchard, M. A., Xie, D., and Rambaut, A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29, 1969–1973.
Bayesian phylogenetics with BEAUti and the BEAST 1.7.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFagu7fO&md5=beec25ccf0d2a98903aa512fd45babe5CAS | 22367748PubMed |

Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.
MUSCLE: multiple sequence alignment with high accuracy and high throughput.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXisF2ks7w%3D&md5=0f644003e0450eab42e285b06371fbb5CAS | 15034147PubMed |

Folmer, O., Black, M., Hoeh, W., Lutz, R., and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.
| 1:CAS:528:DyaK2MXjt12gtLs%3D&md5=41891c10f444b637826cbf6001a4954cCAS | 7881515PubMed |

Forest, J. (1954). Scyllaridea. Crustacés Décapodes Marcheurs des Iles de Tahiti et des Tuamotu. Bulletin du Museum National d’Histoire Naturelle 26, 345–352.

Guérin-Méneville, F. E. (1833). Mémoire sur l’organisation extérieure des Phyllosomes et monographie de ce genre de Crustacés. Magasin de Zoologie, 33 pp.

Gurney, R. (1936). Larvae of decapod Crustacea. Part III. Phyllosoma. Discovery Reports 12, 400–440.

Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.
| 1:CAS:528:DC%2BD3cXhtVyjs7Y%3D&md5=6aaad10f45ced27e84f44de743042b56CAS |

Holthuis, L. B. (1960). Preliminary descriptions of one new genus, twelve new species and three new subspecies of scyllarid lobster (Crustacea Decapoda Macrura). Proceedings of the Biological Society of Washington 73, 147–154.

Holthuis, L. B. (1967). Some new species of Scyllaridae. Proceedings Koninklijke Nederlandse Akademie Wetenschappen 70, 305–308.

Holthuis, L. B. (1985). A revision of the family Scyllaridae (Crustacea: Decapoda: Macrura). I. Subfamily Ibacinae. Zoologische Verhandelingen 218, 1–130.

Holthuis, L. B. (1991). FAO species catalogue. Vol. 13 Marine lobsters of the world. An annotated and illustrated catalogue of species of interest to fisheries known to date. FAO Fisheries Synopsis No. 125.

Holthuis, L. B. (2002). The Indo-Pacific scyllarine lobsters (Crustacea, Decapoda, Scyllaridae). Zoosystema 24, 499–683.

Hong, S. Y. (1988). The prezoeal stage in various decapod crustaceans. Journal of Natural History 22, 1041–1075.
The prezoeal stage in various decapod crustaceans.Crossref | GoogleScholarGoogle Scholar |

Johnson, M. W. (1951). A giant phyllosoma larva of a loricate crustacean from the tropical Pacific. Transactions of the American Microscopical Society 70, 274–278.
A giant phyllosoma larva of a loricate crustacean from the tropical Pacific.Crossref | GoogleScholarGoogle Scholar |

Johnson, M. W. (1968). The phyllosoma larvae of scyllarid lobsters in the Gulf of California and off Central America with special reference to Evibacus princeps (Palinuridea). Crustaceana 2, 98–116.

Johnson, M. W. (1971). The phyllosoma larvae of slipper lobsters from the Hawaiian Islands and adjacent areas (Decapoda, Scyllaridae). Crustaceana 20, 77–103.
The phyllosoma larvae of slipper lobsters from the Hawaiian Islands and adjacent areas (Decapoda, Scyllaridae).Crossref | GoogleScholarGoogle Scholar |

Knight, M. D. (1984). Variation in larval morphogenesis within the southern California Bight population of Euphausia pacifica from winter through summer, 1977–1978. California Cooperative Oceanic Fisheries Investigations Reports 25, 87–99.

Lund, N. T. (1793). Slaegten Scyllarus. Jagttagelser til Insekternes Historie. Kongelige Danske Videnskabers Selskab Skrifter 2, 17–24.

Matzen da Silva, J., Creer, S., dos Santos, A., Costa, A. C., Cunha, M. R., Costa, F. O., and Carvalho, G. R. (2011). Systematic and evolutionary insights derived from mtDNA COI barcode diversity in the Decapoda (Crustacea: Malacostraca). PLoS ONE 6, e19449.
Systematic and evolutionary insights derived from mtDNA COI barcode diversity in the Decapoda (Crustacea: Malacostraca).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmtlKlurs%3D&md5=92a70ee4e30b176816987ff11a0d3c90CAS | 21589909PubMed |

Michel, A. (1971). Note sur les puerulus de Palinuridae et les larves phyllosomes de Panulirus homarus (L). Cahiers O. R. S. T.O.M., (Oceanographie) 9, 459–473.

Nylander, J. A. A. (2004). MrAIC. Program Distributed by the Author. (Evolutionary Biology Centre: Uppsala University, Sweden.)

Palero, F., Guerao, G., and Abelló, P. (2008). Morphology of the final stage phyllosoma larva of Scyllarus pygmaeus (Crustacea: Decapoda: Scyllaridae), identified by DNA analysis. Journal of Plankton Research 30, 483–488.
Morphology of the final stage phyllosoma larva of Scyllarus pygmaeus (Crustacea: Decapoda: Scyllaridae), identified by DNA analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlslyltbs%3D&md5=39ea50f5018f02aac5debc06fe4a301dCAS |

Palero, F., Crandall, K. A. C., Abelló, P., Macpherson, E., and Pascual, M. (2009). Phylogenetic relationships between spiny, slipper and coral lobsters (Crustacea, Decapoda, Achelata). Molecular Phylogenetics and Evolution 50, 152–162.
Phylogenetic relationships between spiny, slipper and coral lobsters (Crustacea, Decapoda, Achelata).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFamurvP&md5=fba89d28eaddb978576c50f9afdc7061CAS | 18957325PubMed |

Palero, F., Hall, S., Clark, P. F., Johnston, D., Mackenzie-Dodds, J., and Thatje, S. (2010a). DNA extraction from formalin-fixed tissue: new light from the Deep Sea. Scientia Marina 74, 465–470.
DNA extraction from formalin-fixed tissue: new light from the Deep Sea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFKkurfP&md5=4e3f2ed807b065c94ea4b18e845f82b7CAS |

Palero, F., Guerao, G., Clark, P. F., and Abelló, P. (2010b). Final-stage phyllosoma of Palinustus A. Milne-Edwards, 1880 (Crustacea: Decapoda: Achelata: Palinuridae) – the first complete description. Zootaxa 2403, 42–58.

Phillips, B. F., Brown, P. A., Rimmer, D., and Braine, S. J. (1981). Description, distribution and abundance of late larval stages of the Scyllaridae (slipper lobsters) in the south-eastern Indian Ocean. Australian Journal of Marine and Freshwater Research 32, 417–437.
Description, distribution and abundance of late larval stages of the Scyllaridae (slipper lobsters) in the south-eastern Indian Ocean.Crossref | GoogleScholarGoogle Scholar |

Prasad, R. R., Tampi, P. R. S., and George, M. J. (1975). Phyllosoma larvae from the Indian Ocean collected by the Dana Expedition 1928–1930. Journal of the Marine Biological Association of India 17, 56–107.

Rambaut, A., and Drummond, A. J. (2007). Tracer v1.4. Available at http://beast.bio.ed.ac.uk/Tracer

Richters, F. (1873). Die Phyllosomen. Ein Beitrag zur Entwicklungsgeschichte der Loricaten. Zeitschrift fur Wissenschartliche Zoologie 23, 623–646.

Robertson, P. B. (1968). A giant scyllarid phyllosoma larva from the Caribbean Sea, with notes on smaller specimens (Palinuridea). Crustaceana 2, 83–97.

Saisho, T. (1966). Studies on the phyllosoma larvae with reference to the oceanographical conditions. Memoirs of the Faculty of Fisheries, Kagoshima University 15, 177–239.

Scholtz, G., and Richter, S. (1995). Phylogenetic systematics of the reptantian Decapoda (Crustacea, Malacostraca). Zoological Journal of the Linnean Society 113, 289–328.
Phylogenetic systematics of the reptantian Decapoda (Crustacea, Malacostraca).Crossref | GoogleScholarGoogle Scholar |

Sekiguchi, E. L. (1990). Four species of phyllosoma larvae from the Mariana waters. Bulletin of the Japanese Society of Fisheries and Oceanography 54, 242–248.

Sims, H. W. (1965). The phyllosoma larvae of Parribacus. Quarterly Journal of the Florida Academy of Science 28, 142–172.

Sims, H. W., and Brown, C. (1968). A giant scyllarid phyllosoma larva taken north of Bermuda (Palinuridea). Crustaceana 2, 80–82.

Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.
MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1eiu73K&md5=5ee5a71f721d24a7782516dc0ff5fcfcCAS | 21546353PubMed |

Webber, W. R., and Booth, J. D. (2001). Larval stages, developmental ecology, and distribution of Scyllarus sp. Z (probably Scyllarus aoteanus Powell, 1949) (Decapoda: Scyllaridae). New Zealand Journal of Marine and Freshwater Research 35, 1025–1056.
Larval stages, developmental ecology, and distribution of Scyllarus sp. Z (probably Scyllarus aoteanus Powell, 1949) (Decapoda: Scyllaridae).Crossref | GoogleScholarGoogle Scholar |

Yang, C.-H., Bracken-Grissom, H. D., Kim, D., Crandall, K. A., and Chan, T.-Y. (2012). Phylogenetic relationships, character evolution, and taxonomic implications within the slipper lobsters (Crustacea: Decapoda: Scyllaridae). Molecular Phylogenetics and Evolution 62, 237–250.
Phylogenetic relationships, character evolution, and taxonomic implications within the slipper lobsters (Crustacea: Decapoda: Scyllaridae).Crossref | GoogleScholarGoogle Scholar | 22008407PubMed |

Yoneyama, S., and Takeda, M. (1998). Phyllosoma and nisto stage larvae of slipper lobster, Parribacus, from the Izu-Kazan Islands, southern Japan. Bulletin of the National Science Museum Series A 24, 161–175.