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190 Years of Sargassum Taxonomy, Facing the Advent of DNA Phylogenies

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Abstract

Sargassum C. Agardh is one of the morphologically most complex phaeophyceaen genera and represents the most species-rich genus of the brown algal order Fucales Bory de Saint-Vincent (Phaeophyceae). The genus’ classification system dates back to the 19th century and is based on observed differences in macro-morphological characters. Those morphological characters may display important variation within individual species, and several authors have linked the taxonomic complexity of the genus to its highly polymorphic nature and phenotypic plasticity. Among the large choice of existing species and subspecies epithets (about 1000), identifying taxa accurately is a difficult task, often relying on authors’ interpretation of short Latin diagnoses or descriptions published in local Floras. Recently, the study of individual species’ morphological range and DNA phylogenies underlined inconsistencies within low taxonomic levels (sections, subsections, series and species groups). Results highlighted the weak taxonomic value of traditional characters used to classify species, and pointed out significant taxonomic issues. The four Sargassum subgenera (S. subgen. Arthrophycus, Bactrophycus, Sargassum and Phyllotrichia) are now subdivided into a total of 12 sections and further subdivisions were abandoned. Two possible new sections need to be assessed. In the present paper, we raise the hypothesis that S. subgen. Arthrophycus could be merged to S. subgen. Bactrophycus, and that S. subgen. Phyllotrichia could be transferred to the recently reinstated genus Sargassopsis Trevisan. We also propose that two sections of the S. subgen. Bactrophycus: S. sect. Halochloa and Repentia be merged. A summary of the actual classification is given along with an identification key for Sargassum subdivisions.

Résumé

Sargassum C. Agardh représente le genre le plus complexe et le plus riche de l’ordre des Fucales Bory de Saint-Vincent (Phaeophyceae). La classification du genre remonte au 19ème siècle et se base sur l’observation de plusieurs caractères macromorphologiques, lesquels peuvent montrer des variations importantes au niveau intra-spécifique. Plusieurs auteurs on mis en évidence le lien existant entre la complexité taxonomique du genre et sa nature polymorphique ainsi que sa plasticité phénotypique. Ainsi parmi le large choix d’épithètes d’espèces et de sous-espèces disponible pour Sargassum (près de 1000), identifier un taxon de façon précise est une tâche difficile reposant souvent sur l’interprétation de courtes diagnoses en Latin ou de descriptions disponibles dans des Flores locales. Récemment, l’analyse combinée de la variabilité morphologique et ADN pour des espèces étudiées individuellement, ont permis de mettre en évidence des incohérences au niveau infra-générique (sections, subsections, series et groupes d’espèces). Les résultats ont souligné la faible valeur taxonomique des caractères utilisés pour classer les espèces, et mis en évidence un certain nombre de conséquences taxonomiques. Les quatre sous-genres de Sargassum (S. subgen. Arthrophycus, Bactrophycus, Sargassum et Phyllotrichia) sont dorénavant sous-divisés en 12 sections, et les sous-divisions inférieures ont été abandonnées. Deux nouvelles sections potentielles nécessitent d’être évaluées. Dans ce papier, nous émettons deux hypothèses: (i) la fusion de S. subgen. Arthrophycus avec S. subgen. Bactrophycus, et (ii) le transfert de S. subgen. Phyllotrichia au genre Sargassopsis Trevisan récemment réintégré. Nous proposons la fusion de deux sections de S. subgen. Bactrophycus: S. sect. Halochloa et Repentia. Un résumé de la classification actuelle est donné avec une clef d’identification pour les sous-divisions du genre Sargassum.

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Notes

  1. Note that the term ‘spiny’ is commonly employed in Sargassum taxonomy, however, it may refer to various types of spine-like protuberances which depending on their aspect may be of taxonomic significance.

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Acknowledgments

We would like to express our gratitude to all curators involved in the search for and loans of specimens, especially B. de Reviers, curator of PC (Museum national d’histoire naturelle de Paris). E. Raffy is thanked for improving the English of the manuscript. We are indebted to the anonymous reviewers for their useful comments. This work is part of L. Mattio research which was supported by a Province Sud (New Caledonia) Doctoral Research Scholarship, UR 227 CoRéUs (Biocompléxité des écosystèmes coralliens de l’Indo-Pacifique), UMR 7158 (IRD-Nouméa, New Caledonia) and UMR6540 (Centre d’Océanologie de Marseille, France). The DNA analyses were conducted at the ‘Plateforme du Vivant’ (IRD, Nouméa, New Caledonia). M. Verlaque is thanked for co-supervising the PhD project. Part of this research was funded by the Agence Nationale pour la Recherche (ANR BIONEOCAL).

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  1. Institut de Recherche pour le Développement, Unité 227 CoRéUs, BPA5, 98848, Nouméa, New Caledonia

    Lydiane Mattio & Claude E. Payri

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  1. Lydiane Mattio
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Correspondence to Lydiane Mattio.

Appendices

Appendix 1

Table 5 Bibliographic synthesis of the Sargassum classification before the advent of molecular analyses; key morphological characters and type species as compiled from J. Agardh (1848, 1889), Womersley (1954), Yoshida (1983, 1989a, b), Abbott et al. (1988), Tseng and Lu (1988, 1992a, b, 1995a, b, c, 1997a, b, 1999, 2002a, b, c, d); the list of species in each subdivision is non exhaustive
Full size table

Appendix 2

ITS-2 analyses based on the alignment of 31 GenBank sequences available for species of S. subgen. Bactrophycus and Arthrophycus

figure a

Neighbour-Joining (NJ) analysis based on 31 GenBank sequences, 475 pb-long (including gaps), representing 27 taxa of S. subgen. Bactrophycus and Arthrophycus. Bootstrap values are indicated for NJ/MP(Maximum Parsimony)/ML(Maximum Likelihood) when above 60% and were based on 1000 (NJ/MP) or 100 (ML, GTR + G + I) replicates. Root: Turbinaria ornata. JP: Japan, NZ: New Zealand. The number of identical sequences is indicated between brackets when relevant and detailed the table below. * S. sinclairii is traditionally classified in S. subgen. Arthrophycus.

List of identical sequences not shown on the tree

References on the tree

Identical sequences not on tree

AB043106 S. siliquastrum

AB043575 S. autumnale

AB043574 S. macrocarpum

AB043610 S. micracanthum

AB043609 S. micracanthum

AB043578 S. okamurae

AB043579 S. okamurae

AB043612 S. serratifolium

AB043568 S. trichophyllum

AB043107 S. yamamotoi

AB043611 S. yesoense

AB038271 S. confusum

AB038273 S. microceratium

Appendix 3

ITS-2 analyses based on the alignment of 33 GenBank sequences available for species of S. subgen. Sargassum.

figure b

Neighbour-Joining (NJ) analysis based on 33 GeneBank sequences, 475 pb-long (including gaps), representing 19 taxa of S. subgen. Sargassum. Bootstrap values are indicated for NJ/MP (Maximum Parsimony)/ML (Maximum Likelihood) when above 60% and were based on 1000 (NJ/MP) or 100 (ML, GTR + G + I) replicates. Root: Turbinaria ornata. FJ: Fiji Islands, FP: French Polynesia, HI: Hawaii, JP: Japan, M: Malaysia, NC: New Caledonia, S: the Solomon Islands, Va: Vanuatu, V: Vietnam.

Appendix 4

Table 6  
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Mattio, L., Payri, C.E. 190 Years of Sargassum Taxonomy, Facing the Advent of DNA Phylogenies. Bot. Rev. 77, 31–70 (2011). https://doi.org/10.1007/s12229-010-9060-x

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