Introduction

Taxonomy is the discipline describing, naming and classifying living organisms, it is essential to the inventory and understanding of biodiversity. Knowing and describing organisms in sufficient details allows (1) to identify and classify them accurately, (2) to study their biology and ecology, (3) to understand their geographical distribution, estimate biodiversity hotspots and define regions of interest for conservation, as well as (4) selecting species with economic potential. Incorrect identifications lead to errors on the quantification of biodiversity, on biological and ecological processes, on the definition of conservation zones, or on the wrong selection of the species containing the targeted molecule of interest. Taxonomy is in constant evolution and tributary of technology progress. The advents of electronic microscopy, as well as biochemical and molecular analyses have been factors responsible for the evolution of our view of taxonomy. Two hundred years ago, phycologists were describing species based on fragments collected as drifts during the first expeditions around the world (Turner, 1808, 1809, 1811; C. Agardh, 1820; Montagne, 1845). Nowadays, the world has been more extensively explored and phycologists study the morphological and molecular variability of populations based on tens of specimens collected at various geographical levels (Tatarenkov et al., 2007; Zhao et al., 2007; Cheang et al., 2008), sequence genomes (Oudot-Le Secq et al., 2002, 2006), and attempt to identify species with genetic barcodes (Saunders, 2005; Robba et al., 2006; Chase et al., 2007).

Sargassum C. Agardh, described 190 years ago (C. Agardh, 1820), represents today the most species rich genus of the marine macrophytes (estimated from Guiry & Guiry, 2010) and the morphologically most complex phaeophyceaen genera. Species are distributed worldwide and the genus is especially well represented in tropical and inter-tropical regions where it forms dense submarine forests. These forests structure an essential habitat for numerous marine species, and are equivalent to the temperate Fucus Linnaeus, Cystoseira C. Agardh or Kelp forests (Nizamuddin, 1962; Phillips, 1995; Steneck et al., 2002; Thibaut et al., 2005). Some species are economically important, especially in Asian countries where they are exploited by agro-food, textile, cosmetic and pharmaceutical industries. Chemical properties may vary from one species to another (Prud’homme van Reine, 2002; Smit, 2004). However, with roughly 1000 taxa, of which less than 40% are recognized as current, identifying a species is often a difficult task (Mattio et al., 2010). The placement of species within a section of the genus or its subdivisions is often difficult and illustrates the challenge between a high intra-specific morphological variability and a classification system based on ancient and fragmentary material not representative of species’ polymorphy (pers. obs.). Although Sargassum’s taxonomy has been the focus of increased attention since 1985 (Abbott, 2004), it is still in need of systematic re-examination (Mattio et al., 2010).

Morphology

The morphology of Sargassum is characterised by a thallus composed of a fixation holdfast, one to several main axes ramified into ‘branches’ of several orders which differentiate into foliar appendices named ‘leaves’, vesicles (aerocysts) and receptacles (reproductive organs). The overall shape of the thallus may be more or less linear or bushy, it may measure a few centimetres in exposed habitats (ex. S. spinuligerum var. crispata (Sonder) J. Agardh in Kiuva reef, Fiji—pers. obs.) to several meters in sheltered areas [ex. S. sp. in Colombia, O. Camacho-Hadad pers. comm.; up to 10 m for the invasive S. muticum (Yendo) Fensholt in France (Belsher & Pommellec, 1988)]. The holdfast is discoid, conical or rhizoidal and do no penetrate the substratum. Main axes are perennial, short, cylindrical or flattened in section, and bear the scars of deciduous branches. Secondary or other order axes or branches are cylindrical or flattened in section, with a smooth or ‘spinyFootnote 1’ surface, and are distichously or spirally arranged. In species belonging to S. section Polycystae Mattio et Payri some of the secondary branches are differentiated into stoloniferous axes bearing haptera (or secondary holdfasts). The shape of leaves is highly diversified (Fig. 1). They can be simple, bifid or divided several times, rond, spatulate, turbinate, lanceolate, ovoid, linear or of any intermediate forms. The basis of leaves is rounded or attenuate, symmetrical or not. The pedicel is inexistent or of variable length, cylindrical or flattened in section and smooth or ‘spiny’. The leaves’ margin may be simple or double at the apex, and be smooth, undulate, finely serrate, deeply dentate or any intermediate aspect. The midrib may be short and thick or thinner and reaching the apex, or any intermediate length. The apex may be acute, rounded or truncated, simple or showing a cup-like shaped depression. Cryptostomata, of variable number and size, are either randomly distributed over the leaves’ surface or aligned on each side of the midrib in one to several rows. Vesicles (or aerocysts) may be spherical, ovoid, pyriform or of any intermediate shape; they are smooth or bear a mucron which may be simple or multiple, thin and spine-like, foliar, or in crown. Vesicles are held by a pedicel variable in size, cylindrical, flattened or foliar. For some species, the vesicle may develop in the middle of leaf and is named phyllocyst (Fig. 2). Receptacles are either solitary or in tight to open clusters, simple, branched, bearing or not small vesicles and/or leaves (mixed receptacles), lanceolate or linear, smooth or ‘spiny’, of cylindrical or flattened section. Receptacles are said zygocarpic (composed or mixed), malacocarpic (cylindrical and smooth) or acanthocarpic (spiny), qualified of carpophylles or pseudocarpophylles, arranged in cymes, racemes or glomerules. In case of a dioecious species, a male/female dimorphism may be observed with male receptacles often slender than female receptacle shorter and stockier (Fig. 3). Sexual dimorphism may concern the whole thallus.

Fig. 1
figure 1

Leaves morphology (S. subgen. Sargassum). Leaves may be simple (eg. c, m, u), bifid (eg. e), trifid (eg. a, p), divided several times (eg. o, q, r); the general shape may be round (eg. k), spatulate (eg. s, x, y), turbinate (eg. t), lanceolate (eg. b, c), ovoid (eg. h), or oblong (eg. f, j, w), linear (eg. n, v); undulate (eg. a, j, w) or strait in lateral view (eg. n, v, x). The basis may be ronded (eg. a, k) or attenuate (eg. e, n, x), symetrical (eg. v, x) or asymetrical (eg. p, s, z). The margin may be smooth (eg. e, v), finely serrulate (eg. d, p, w), profoundly dentate (eg. u, x, y); simple (eg. c, n, w), or double (eg. t, y). The apex may be acute (eg. c, v), or obtuse (eg. f, j, s); simple (eg. d, m) or with a depression (eg. j, k)

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Fig. 2
figure 2

Vesicles morphology (S. subgen. Sargassum). The general shape may be spherical (eg. h, n, s), or ovoid (eg. c, t, v); vesicles may be smooth (eg. e, k, p), with a mucro which may be thin (eg. c, o, q), foliar (eg., d, r), expanded into a crown (eg. t) or forming ear-like expansions (eg. m). The pedicel may be of variable size cylindrical (eg. g, m, q), flattened (eg. v, x) or foliar (eg. a, c, u)

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Fig. 3
figure 3

Receptacles morphology (S. subgen. Sargassum). The general shape of receptacles may be lanceolate (eg. f, q) or linear (eg. a, k), margins may be smooth (eg. a, l) or with spine-like protuberances (eg. c, g, p), with a section cylindrical (eg. b, o) or more or less flattened (eg. e, p); arranged in cymes (eg. a, h, o), in racemes (eg. d, m) or in glomerules (eg. i, j). Receptacles may be zygocarpic (eg. m, f), acanthocarpic (eg. h, i, p) or malacocarpic (eg. a, k, o). Example of male/female dimorphism (k/l, m/n, o/p)

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Morphological characters may present a high intra-specific morphological plasticity, either between populations, within populations or even within one individual. Kilar and Hanisak (1989) have identified as many as 47 different morphotypes within the same S. polyceratium Montagne population in Florida. They have also pointed out that a number of morphological variations depend on seasons, habitat type, and water motion. In a review on the phenotypical variability of Sargassum, Kilar et al. (1992) underlined the influence of environmental conditions, age and period of reproduction on the size, shape and aspect of leaves. According to these authors, the morphological characters of a given species may vary in time, at intra- or inter-individual level, depending on environmental conditions and spatially (inter-population).

The systematic of Sargassum is based on various morphological characters. Subgenera are mainly recognizable by the organisation and aspect of their axes, but S. subgen. Bactrophycus J. Agardh and Arthrophycus J. Agardh are differentiated by their receptacle morphology (Yoshida, 1989a, b). However, the several morphological characters used for distinguishing further subdivisions do not show a consensus. Sections of S. subgen. Bactrophycus are first recognizable by the shape and organisation of axes, and then by the receptacle morphology while sections of S. subgen. Sargassum are originally exclusively recognizable based on receptacle morphology. The sub-divisions of these sections are based on a more detailed description of receptacle morphology and reproduction strategies (dioecy, monoecy, male/female dimorphism or not), and to a less extent on the morphology of vesicles, holdfast or axes. Within each subdivision, species are identified on supplementary morphological characters including, most often, morphological variation in the aspect and shape of leaves, vesicles and receptacles. Infra-specific ranks such as varieties and formas are mainly identified according to minor morphological variations which are difficult to differentiate from a simple ecomorph. For instance, some taxa are distinguished by the absence or presence of vesicles (eg. S. tahitense Grunow and S. boraborense (Grunow) Setchell), whereas the abundance of vesicles is clearly influenced by environmental conditions such as hydrodynamism (Kilar et al., 1992; Mattio et al., 2008).

Taxonomical Ambiguities

Nomenclatural ambiguities have been documented since the establishment of Sargassum (Silva et al., 1996: 930), which is consensually recognized as a difficult genus in need for a significant taxonomic revision. Taxonomic ambiguities are found at two levels: (i) the level of terminal taxa, ie. ambiguities in species distinction, and (ii) the level of classification, ie. ambiguities in the attribution of a particular species to one of the genus’ numerous subdivisions. The classification and description of most species date back to the 19th century mainly with the works of C. Agardh (1820, 1824) and J. Agardh (1848, 1889). Monographies and collections of these authors are representative of the genus taxonomy at this time. Diagnoses mainly consist in short paragraphs describing briefly the type material, which was most of the time not properly designated. The latter is often represented by an incomplete dry sample in bad shape, collected as drift in an imprecise locality during the first expeditions around the world (pers. obs. Museum of Lund, Agardh’s collection). As a consequence and without knowledge of individuals in their natural habitat, C. and J. Agardh and their contemporaries may have described several taxa from fragments belonging to the same species. The situation is even increased by the substance of diagnoses, which without illustrations, may correspond to several very different species (pers. obs.). In addition, it is difficult to retrieve collections and type specimens as some of them might have disappeared or been destroyed (eg. the fire of the Berlin’s Museum during the Second World War).

The origin of these taxonomic confusions is probably linked to the high polymorphy of the genus as it was likely underestimated at this time. Morphological characters used for Sargassum taxonomy may show important phenotypic variations related to habitat diversity, exposition or seasons (De Wreede, 1976; Magruder, 1988; Killar et al., 1992; Trono, 1992; Gillespie & Critchley, 1997, 2001). This polymorphy has sometimes been wrongly interpreted as inter-specific variations, thus creating several epithets for the same species (Womersley & Bailey, 1970; Guiry & Guiry, 2010). Considering this morphological variability, Grunow (1915, 1916a, b) described numerous varieties and formas, thus increasing the complexity of the genus taxonomy. Many of these infra-specific taxa have been considered as superfluous by various authors (Womersley, 1987; Yoshida, 1987; Mattio & Payri, 2009) and there is often a lack of information about taxa’s morphological variability. Consequently, identifying species often remains uncertain.

According to Kilar et al. (1992), taxonomic ambiguities are linked to a considerable variability in species description. Authors list 11 potential reasons for taxonomic confusions: (i) an important morphological plasticity, (ii) variable ontogenic forms, (iii) a high polymorphism, (iv) morphological characters which may be absent (eg. vesicles and receptacles), (v) too much importance given to highly variable characters such as leaves, (vi) hybridization which may produce specimens with intermediate forms, (vii) the possibility of polyploidy which may produce divergent morphologies, (viii) the number of varieties and formas described in the literature, (ix) the absence of polymorphy representation by type specimens which are often fragments, (x) absence of a consensus underlying characters of taxonomic importance, (xi) absence of relevant information concerning ecology, development, and reproduction of most of the species. With the aim of circumscribing taxa’s morphological variability, Kilar et al. (1992) made several recommendations notably including studies on a sufficient number of specimens, in various seasons and issued from populations submitted to various environmental conditions. These authors also recommend in vitro reproduction tests and genetic analyses.

Once species have been identified, classifying them into the various subdivisions of the genus is often confusing (Womersley, 1954; Yoshida, 1983; Mattio et al., 2009, 2010). This is mainly due to the combination of factors such as a high intra-specific polymorphy, and a classification system based on ancient and fragmentary material. For example, S. mcclurei Setchell was first placed within S. subgen. Arthrophycus (Setchell, 1933), then transferred to S. subgen. Bactrophycus sect. Phyllocystae Tseng (Tseng et al., 1985), and finally to S. subgen. Sargassum when S. sect. Phyllocystae was transferred to this subgenus by Stiger et al. (2000). Womersley (1954) proposed to include S. subgen. Schizophycus J. Agardh into S. subgen. Sargassum and did not recognize the various subdivisions of S. subgen. Phyllotrichia (Areschoug) J. Agardh, which according to him are based on insignificant morphological variations. Later, in an attempt to resolve main ambiguities, Yoshida (1983) proposed to classify Sargassum subgenera in two groups: (i) those with leaves perpendicular to main axis (ie. horizontally oriented) (S. subgen. Bactrophycus and Arthrophycus), and (ii) those with leaves parallel to the main axis (ie. vertically oriented) (S. subgen. Phyllotrichia, Schizophycus, and Sargassum). In their revision of S. subgen. Sargassum from China, Tseng and Lu (1988, 1992a, b, 1995a, b, c, 1997a, b, 1999, 2002a, b, c, d) clarified and synthesized characters having taxonomic significance for the identification of sections, subsections, series and species groups. But according to Abbott (1992: 1–3), the entire Sargassum classification system is confusing and in some cases too vague to be useful. The author points out inconsistencies at all levels including for the distinction of subgenera. According to her, abandoning subgenera wouldn’t be the solution, and a new taxonomic approach is necessary to better appreciate the composition and organisation of the genus.

Sargassum Taxonomy, First Period (1820–1988)

In botany, even if several genera are divided into subgenera, there are only few taxa with sufficient species number to justify the use of inferior sub-divisions such as for example sections, subsections and series. In the case of Sargassum, the hundreds of taxa attributed to one subgenus are traditionally classified into sections, subsections, series and species groups, the latter having not taxonomic value according to the International Code of Botanical Nomenclature (ICBN, McNeill et al., 2006). The first sargasso species, originally attributed to the genus Fucus, were described by Linnaeus (1753) (F. natans Linnaeus, F. acinarium Linnaeus, F. lendigerus Linnaeus), then by Turner (1808, 1809, 1811) (36 species). The genus Sargassum was established by C. Agardh (1820), who was the first to lay the foundations of a new classification system for seaweeds. Sargassum represents the first genus listed in C. Agardh’s order Fucoidae, and contains 62 species partitioned into seven unnamed groups recognizable by the following morphological characters: (i) axillary receptacles and whole leaves; (ii) axillary receptacles and pinnatifid leaves; (iii) vesicules and leaves of small size (Microphylla); (iv) terminal receptacles; (v) leafy vesicles, and spatulate and inflated leaves; (vi) axes flattened, pinnatifid and foliar, and axillary vesicles and receptacles; (vii) leaves without midribs, receptacles marginal and fixed to leaves, and solitary capsules in each tubercule. Later on, two of these groups were recognised as genera: Turbinaria Lamouroux (group iv) and Carpophyllum Greville (group vii). This classification was used by Montagne (1842, 1845) and Greville (1848, 1849). Nevertheless, Kützing (1843, 1845) proposed a completely different classification system, maintaining only part of the species in the genus Sargassum (mainly those corresponding to J. Agardh (1889)’s S. series Malacocarpicae and Zygocarpicae according to Setchell 1931), and attributing the other part to the genera Carpacanthus Kützing, Halochloa Kützing, Pterocaulon Kützing, Spongocarpus Kützing and Stichophora Kützing. J. Agardh (1848) did not retain Kützing’s work and proposed a new classification composed of sections divided into ‘tribus’ (no taxonomic value according to ICBN) themselves divided into species groups which were organised according to morphological characters or a common geographical distribution. At this stage, the genus Sargassum contained three sections organised as follows:

  1. (i)

    S. sect. Pterophycus J. Agardh with one tribus:

    • tribus Pterocaulon (Kützing) J. Agardh (type unknown);

  2. (ii)

    S. sect. Arthrophycus J. Agardh with three tribus:

    • tribus Schizophylla J. Agardh (type unknown),

    • tribus Holophylla J. Agardh (type unknown),

    • tribus Heterophylla J. Agardh (type: S. heterophyllum C. Agardh);

  3. (iii)

    S. sect. Eusargassum with eigth tribus:

    • tribus Carpophylla J. Agardh (type: S. carpophyllum J. Agardh),

    • tribus Glandularia J. Agardh (type unknown),

    • tribus Siliquosae J. Agardh (type: S. siliquosum J. Agardh),

    • tribus Biserrulae J. Agardh (type: S. biserrula J. Agardh),

    • tribus Acanthocarpa J. Agardh (type unknown),

    • tribus Acinaria J. Agardh (type: S. acinaria C. Agardh),

    • tribus Ligularia J. Agardh (type: S. ligulatum C. Agardh),

    • tribus Cymosae J. Agardh (type: S. cymosum C. Agardh).

Later, J. Agardh (1889), following the basis of his 1848’s classification, published the most complete classification and divided the genus Sargassum into five subgenera, themselves divided into several series, each sub-divided into ‘tribus’:

  1. (i)

    S. subgen. Phyllotrichia (Areschoug) J. Agardh with five tribus:

    • tribus Heteromorphae J. Agardh (type: S. heteromorphum J. Agardh),

    • tribus Cladomorphae J. Agardh (type unknown),

    • tribus Phyllomorphae J. Agardh (type unknown),

    • tribus Pteromorphae (Kützing ?) J. Agardh (type unknown),

    • tribus Dimorphae J. Agardh (type unknown);

  2. (ii)

    S. subgen. Schizophycus J. Agardh (type: S. patens C. Agardh) monospecific;

  3. (iii)

    S. subgen. Bactrophycus J. Agardh (type unknown) with two unnamed species groups;

  4. (iv)

    S. subgen. Arthrophycus J. Agardh (type S. heterophyllum C. Agardh) with two unnamed species groups;

  5. (v)

    S. subgen. Eusargassum with three series:

    • S. ser. Zygocarpicae (J. Agardh) Setchell with one tribus:

      • * tribus Carpophyllae J. Agardh (type: S. carpophyllum) with two unnamed species groups;

    • S. ser. Acanthocarpicae J. Agardh with two tribus:

      • * tribus Glomerulatae J. Agardh (type unknown) with four unnamed species groups;

      • * tribus Biserrulae J. Agardh (type: S. biserrula) with four named species groups:

        • # Ilicifolia (founding species: S. ilicifolium (Turner) C. Agardh),

        • # Coriifolia (founding species: S. coriifolium J. Agardh),

        • # Parvifolia (founding species: S. parvifolium (Turner) C. Agardh),

        • # Dentifolia (founding species: S. dentifolium (Turner) C. Agardh);

    • S. ser. Malacocarpicae J. Agardh with three tribus:

      • * tribus Fruticuliferae J. Agardh (type unknown),

      • * tribus Cymosae J. Agardh (type: S. cymosum),

      • * tribus Racemosae J. Agardh divided into three ‘sub-tribus’:

        • Acinariae (type: S. acinaria),

        • Glandulariae (type unknown),

        • Siliquosae (type: S. siliquosum).

In 1849, Kützing described two supplementary genera: Anthophycus Kützing and Platylobium Kützing for Sargassum longifolium (Turner) C. Agardh (1820) and S. platylobium (Mertens) C. Agardh (1820), respectively. The J. Agardh (1848)’s classification was largely adopted by subsequent authors such as Grunow (1915, 1916a, b), Setchell (1931, 1933, 1935a, b, 1936, 1937) and Yoshida (1983), and was slightly modified till recently. The main modifications were those of Abbott et al. (1988), and Tseng and Lu (various works) who proposed a number of corrections to J. Agardh’s classification, mainly to follow the Art.4.1 of the ICBN, by transferring the majority of series to the rank of section and ‘tribus’ to the rank of subsections. Certain species groups proposed by J. Agardh (1889) and Grunow (1915, 1916a, b) were transferred to the rank of series, and authors, including Tseng and Lu (various works) and Ajisaka et al. (1995), have defined several new species groups. Species groups are meant to cluster taxa a priori related but the ICBN do not recognize a taxonomic status for them. However according to Art.4.2, species groups may be used as supplementary ranks under subseries. According to Ajisaka et al. (1995), after thorough population study, a species group could be either elevated to a recognized rank or reduced to only one species, all members of the species groups being then considered as conspecific. A view of Sargassum classification at this stage is given in Appendix 1. More recently, studies using DNA markers have underlined the necessity to reassess the whole Sargassum classification.

Sargassum Taxonomy, Second Period (2000–2010): The Advent of DNA Phylogenies

Molecular analyses of DNA offer an alternate method to test taxonomic, systematic and phylogenic traditional concepts. In phycology, systematic studies using nucleic acids have apprehended phylogenies in a new way as soon as the 1980s (Olsen, 1990). Since then, numerous studies have demonstrated how useful DNA markers are to understand taxa’s evolutionary history (Kooistra et al., 1992; Hoarau et al., 2007; Phillips et al., 2008a, b), and phylogenetic relationships (Kogame et al., 1999; Coyer et al., 2006; De Clerck et al., 2006), or resolve taxonomic ambiguities (Coyer et al., 2001; Hayden et al., 2003; Faye et al., 2004; Mattio et al., 2010). Regarding Phaeophyceae, the first complete phylogenies (Draisma et al., 2001; Rousseau et al., 2001) have confirmed the monophyly of the majority of orders whereas the Laminariales and Sphacelariales appeared as paraphyletic. The phylogeny of Fucales was explored by several authors using nuclear markers SSU and LSU (rDNA) (Rousseau et al., 1997; Rousseau & de Reviers, 1999) or chloroplastic psaA (Cho et al., 2007). These studies have pointed out the monophyly of Fucales as well the majority of families currently classified into this order, exception of Cystoseiraceae. Two new families have been proposed and the Cystoseiraceae were merged to the Sargassaceae. More recently, Draisma and Rousseau (2010) have proposed several significant revisions within the Sargassaceae using a combined analysis of psbA and mt23S. A considerable number of studies have been dedicated to Fucales and in particular to Fucus species which play a major role in European marine ecosystems (Wallace et al., 2004; Engel et al., 2005; Coyer et al., 2006; Oudot-Le Secq et al., 2006). However, only few authors take an active interest in Sargassum despite its ecological importance in inter-tropical regions and taxonomic significance.

The first authors to challenge the traditional classification and phylogenetic relationships in Sargassum using DNA markers were Phillips (1998), Phillips and Fredericq (2000), Phillips et al. (2005), Stiger et al. (2000, 2003), and Yoshida et al. (2000, 2002, 2004). These studies only led to few taxonomic revisions as markers for the ITS-2 region and the partial rbcLS-operon, used independently, showed poor taxon representation and limited interspecies resolution. Stiger et al. (2000, 2003) transferred S. sect. Phyllocystae from S. subgen. Bactrophycus to S. subgen. Sargassum and the genus Hizikia Okamura to section level within S. subgen. Bactrophycus. Yoshida et al. (2004) merged S. subgen. Schizophycus into S. subgen. Sargassum. These rearrangements provided strong evidence of the necessity to re-assess taxonomic concepts within Sargassum. In more recent studies, combining detailed results provided by a three markers-DNA phylogeny, analyses of morphology, and old herbarium collections including types, Mattio and Payri (2009) and Mattio et al. (2008, 2009, 2010) provided taxonomic clarifications of Sargassum diversity for South Pacific islands. The authors confirmed the polyphyletic nature of S. sect. Acanthocarpicae, re-assessed the status of numerous species, resolved several taxonomic incongruities, and provided an advanced revision of S. subgen. Sargassum’s sections. A detailed review of each Sargassum subgenera is discussed hereafter.

Sargassum subgen. Phyllotrichia & Schizophycus

Phyllotrichia was described by Areschoug as a distinct genus [Areschoug, 1854: 332, type species: Phyllotrichia sonderi (J. Agardh) Areschoug, basionym: Cystoseira sonderi J. Agardh, 1848: 247] and was later considered as a subgenus of Sargassum by J. Agardh [1889: 35, type species: S. sonderi (J. Agardh) J.Agardh]. J. Agardh (1889) further subdivided this subgenus into five ‘tribus’ mainly established based on differences in vesicles’ shape: (i) Heteromorphae (2 species), (ii) Cladomorphae (3 species), (iii) Phyllomorphae (4 species), (iv) Pteromorphae (4 species) et (v) Dimorphae (2 species). Beside, Sargassum subgen. Schizophycus was originally described by J. Agardh (1848) as a ‘tribus’ of his section Arthrophycus and later elevated to subgenus rank (J. Agardh, 1889) containing only one species: S. patens J. Agardh.

In his revision of Australian species of S. subgen. Phyllotrichia, Womersley (1954) proposed that S. subgen. Schizophycus be merged to S. subgen. Phyllotrichia based on morphological evidences. The author further enumerates eigth Australian species of S. subgen. Phyllotrichia (S. decurrens (R. Brown ex Turner) C. Agardh, S. peronii, S. heteromorphum, S. sonderi, S. decipiens (R. Brown ex Turner) C. Agardh, S. howeanum Lucas, S. varians Sonder, et S. verruculosum C. Agardh), three East Asian species (S. piluliferum (Turner) C. Agardh, S. pinnatifidum Harvey, et S. patens), and one from Canary Islands (S. desfontainesii (Turner) C. Agardh). Womersley (1954) also pointed out that the ‘tribus’ of J. Agardh were a source of confusion and should be avoided. Later, Goldberg and Huisman (2004) described a new S. subgen. Phyllotrichia species: S. kendrickii N. A. Goldberg et Huisman, while five species were transferred to S. subgen. Sargassum: S. desfontainesii (Diaz-Villa et al., 2007), S. howeanum (Goldberg & Huisman, 2004), S. piluliferum and S. patens (Stiger et al., 2003), and S. pinnatifidum (along with three other ex-S. subgen. Schizophycus species, Yoshida et al., 2004). Finaly, Draisma and Rousseau (2010), using molecular markers and a large Sargassaceae dataset, demonstrated that S. decurrens (= S. scabripes J. Agardh and S. boryi C. Agardh) should be placed back in Sargassopsis Trevisan (1843: 332) (not Sargassopsis Nizamuddin et al., 1993) of which it should be considered the type species. The authors recommend a thorough revision before other S. subgen. Phyllotrichia species may be transferred to Sargassopsis. All these taxonomic changes point out the necessity for a re-evaluation of the species traditionally ascribed to S. subgen. Phyllotrichia as well as the morphological characters used to characterize this subgenus. Currently, only seven species should be attributed to S. subgen. Phyllotrichia: S. peronii, S. heteromorphum, S. sonderi, S. decipiens, S. varians, S. verruculosum, and S. kendrickii.

Sargassum subgen. Bactrophycus & Arthrophycus

Sargassum subgen.

Bactrophycus was described by J. Agardh (1889) based on 14 species distributed in four morphological groups mainly defined by the organisation of axis and the shape of vesicles. This subgenus was studied in detail by Yoshida (1983, 1989a) and Tseng et al. (1985), and S. horneri was designated as type of S. subgen. Bactrophycus (Yoshida, 1983). Sargassum subgen. Bactrophycus currently contains 35 taxa including 22 species and one variety endemic to Japan. These taxa were divided into four sections by Yoshida (1983): S. sect. Halochloa (Kützing) Yoshida, S. sect. Repentia Yoshida, S. sect. Spongocarpus (Kützing) Yoshida and S. sect. Teretia Yoshida. Tseng (1985) described a fifth section: S. sect. Phyllocystae Tseng to classify species with phyllocysts. Later, based on molecular studies, Stiger et al. (2000, 2003) proposed to transfer S. sect Phyllocystae from S. subgen. Bactrophycus to S. subgen. Sargassum, as well as the reinstatement of S. fusiforme (Harvey) Setchell (= Hizikia fusiformis (Harvey) Okamura) to be placed in a new section: S. sect. Hizikia (Okamura) Yoshida.

Sargassum subgen.

Arthrophycus was described by J. Agardh (1889) based on 20 species distributed into four morphological groups mainly distinguished on the shape of receptacles. According to Yoshida (1989b), no type species has ever been designated for the subgenus. The basionym of S. subgen. Arthrophycus is S. sect. Arthrophycus which was divided into three ‘tribus’: Schizophylla, Holophylla and Heterophylla (J. Agardh, 1848). Only eigth species of ‘tribus’ Heterophylla were transferred by J. Agardh (1889) to S. subgen. Arthrophycus. The other two ‘tribus’ were respectively transferred to S. subgen. Schizophycus and Bactrophycus (J. Agardh, 1889). In this context, we propose to consider S. heterophyllum (nomen typificatum for ‘tribus Heterophylla’) as the type species of S. subgen. Arthrophycus. In a general trend, S. subgen. Arthrophycus is badly known and only sequences for two species are currently available on GenBank (S. fallax Sonder, partial Rubisco, Phillips & Fredericq, 2000—S. sinclairii J. D. Hooker et Harvey, ITS-2, Mattio & Payri, 2009). Lindauer et al. (1961) listed three taxa belonging to S. subgen. Arthrophycus in New Zealand: S. sinclairii, S. undulatum J. Agardh and S. undulatum f. serratifolium Lindauer. However, according to Adams (1994) the two latter should be considered as synonyms of S. sinclairii which is the most common Sargassum species in New Zealand. According to Womersley (1987), five species of S. subgen. Arthrophycus are common along the coast of Australia. These studies appear to be ones of the rare works undertaken about this subgenus.

Sargassum subgen.

Bactrophycus and Arthrophycus are morphologically close and distinguished only by the shape of receptacles and their distinct geographical distribution. Hence, S. subgen. Arthrophycus is distinguished from S. subgen. Bactrophycus by the presence of compound receptacles (Yoshida, 1983), and according to Setchell (1931), species of S. subgen. Arthrophycus are exclusively found in the southern hemisphere along the coast of Australia, Tasmania, New Zealand and South Africa. Nevertheless, Setchell (1933) attributed two species from Hong-Kong (S. mcclurei Setchell, S. herklotsii Setchell) to S. subgen. Arthrophycus. Yoshida (1983, 1989b) prefers to consider that this subgenus is only distributed in the southern hemisphere while S. subgen. Bactrophycus is restricted to the northern hemisphere, mainly in the East Asian region.

Analyses of the nuclear ITS-2 marker were carried out for 26 species of S. subgen. Bactrophycus (available on GenBank from Stiger et al., 2000, 2003) and one species of S. subgen. Arthrophycus (S. sinclairii, available on GenBank from Mattio & Payri, 2009). Results (Appendix 2) demonstrate a low genetic polymorphism between members of the S. sect. Halochloa and Repentia suggesting that both taxa should be considered as only one section. Based on the same results, Stiger et al. (2003) interpreted the low genetic polymorphism to a recent radiation of both sections. However, because sequences for both section’s type (respectively S. siliquosum and S. okamurae, see Appendix 2 table) are identical, we propose to merge S. sect. Repentia Yoshida into S. sect. Halochloa (Kützing) Yoshida. Results of the ITS-2 analysis also show the clustering of sequences available for S. sinclairii from New Zealand with the Halochloa/Repentia clade. Consequently, we propose the transfer of S. sinclairii from S. subgen. Arthrophycus to S. subgen. Bactrophycus. The geographical distribution of S. subgen. Bactrophycus should not anymore be considered as restricted to the Northern hemisphere. The study of further markers and samples of S. subgen. Arthrophycus, especially for the type species S. heterophyllum, should provide us with a revised view of S. subgen. Arthrophycus and Bactrophycus.

Sargassum subgen. Sargassum

Sargassum sect.

Sargassum (75 species subdivided in eigth ‘tribus’) was elevated to subgenus rank by J. Agardh (1889) who subdivided it into three series: Zygocarpicae, Malacocarpicae and Acanthocarpicae (95 species in total). Series were later elevated to sectional rank (Setchell, 1935b; Abbott et al., 1988) and subdivided into subsections, series and species groups (cf. Appendix 1). The traditional identification of S. subgen. Sargassum’s sections is exclusively based on the morphology of receptacles. Sargassum sect. Acanthocarpicae is conventionally recognized on the basis of flattened and spiny receptacles arranged in dense glomerules (S. subsect. Glomerulatae) or racemes (S. subsect. Biserrulae), and possibly exhibiting malacocarpic male receptacles (S. subsect. Biserrulae ser. Plagiophyllae). Sargassum sect. Zygocarpicae is conventionally identified by ‘mixed’ receptacles (ie. receptacles associated to small leaves and/or vesicles) which pedicels may be absent and only associated with leaves or with leaves and vesicles (S. subsect. Holozygocarpicae) or which pedicels are often present and only associated with leaves or only with vesicles (S. subsect. Pseudozygocarpicae). Sargassum sect. Malacocarpicae is traditionally recognized by the presence of smooth and cylindrical receptacles which may be arranged in cymes brush-like and pedicelate (S. subsect. Fruticuliferae), in fascicules and branched (S. subsect. Cymosae), or arranged in racemes with branches supported by a sterile pedicel (S. subsect. Racemosae) (Appendix 1). This system of classification was accepted by the majority of the authors but because in practice it is based on very slight variations of receptacles’ morphology, it has been used by few of them.

Recently, Norris (2010) published four new sections of S. subgen. Sargassum according to four morphological groups described by Dawson (1944): S. sect. Johnstonii E. Y. Dawson ex J. N. Norris, S. sect. Lapazeanum E. Y. Dawson ex J. N. Norris, S. sect. Sinicola E. Y. Dawson ex J. N. Norris and S. Herporhizum E. Y. Dawson ex J. N. Norris. These four sections are mainly identified on the morphology of leaves, vesicles and/or attachment type.

With the advent of DNA markers in Sargassum taxonomy, several revisions have been proposed for S. subgen. Sargassum. Stiger et al. (2000) proposed the transfer of S. sect. Phyllocystae from S. subgen. Bactrophycus to S. subgen. Sargassum based on ITS-2 sequences analysis of S. mcclurei and S. quinhonense Nguyen Huu Dai. However, Mattio et al. (2010) underlined that the effective transfer of the section should await confirmation by an analysis of the sequences for the section’s type (S. phyllocystum Tseng et Lu). Using combined analyses of nuclear ITS-2, chloroplastic partial Rubiso and mitochondrial cox3 markers, Mattio et al. (2009, 2010) have: (i) described S. sect. Polycystae Mattio et Payri. to fit species with stolon-like branches; (ii) synonymised S. sect. Malacocarpicae and Acanthocarpicae to the autonymous S. sect. Sargassum; and (iii) elevated S. ser. Binderiana Tseng et Lu and S. ser. Ilicifolia (J. Agardh) Tseng et Lu to sectional rank and emended their descriptions according to new sets of morphological characters to accommodate species with respectively cylindrical to slightly compressed axes possibly twisted, alternately and spirally arranged, and strongly flattened axes distichously arranged in one plan.

For the purpose of the present work, analyses of the nuclear ITS-2 marker (Appendix 3) were carried out for 19 taxa of S. sect. Sargassum (available on GenBank from Stiger et al. 2000, 2003; Mattio & Payri, 2009; Mattio et al., 2008, 2009). Results show six well sustained clades, five of them representing S. sect. Sargassum, Zygocarpicae, Polycystae, Binderiana and Ilicifolia. One clade, clustering sequences for S. piluliferum and S. yendoi Okamura et Yamada, form a sister group to the clade representing S. sect. Sargassum. These results are similar to those of Stiger et al. (2003) but the low representation of S. sect. Sargassum (two species) in their work did not allow the authors to interpret this clade as a distinct group from S. sect. Sargassum. Similarly using partial Rubisco marker, Mattio et al. (2010) showed S. platycarpum Montagne as a sister group to S. sect. Sargassum and Zygocarpicae and raised the hypothesis of a new section to be elevated from S. ser. Platycarpae. The hypothesis of a sixth section to fit S. piluliferum- and S. yendoi-like species and a seventh section to fit S. platycarpum-like species need to be confirmed with the help of further markers and morphological analysis. Similarly, we recommend that the four sections published by Norris (2010) (S. sect. Johnstonii, sect. Lapazeanum, sect. Sinicola, and sect. Herporhizum) be assessed with DNA markers and diagnostic morphological characters be revised. Actually, the three species classified within S. sect. Herporhizum (S. herporhizum Setchell et N. L. Gardner, S. brandegeei Setchell et N. L. Gardner, and S. liebmannii J. Agardh) exhibit stolon-like branches arising from a discoid holdfast which is a diagnostic character of S. sect. Polycystae. The examination of S. herporhizum syntypes (UC 484236, 484241, 484252, 484253) confirmed that S. sect. Herporhizum should be considered as a synonym of S. sect. Polycystae.

Sargassum subgen.

Sargassum assorts the majority of the genus’ species but is it is difficult to estimate an accurate species number. If we consider the current genus species number (344) given by Guiry and Guiry (2010), and the species number estimated for other subgenera from the above discussions (S. subgen. Phyllotrichia = 7; S. subgen. Bactrophycus = 27; S. subgen. Arthrophycus = about 20), the number of S. subgen. Sargassum species could be around 300. This number may be largely overestimated considering the numerous possible synonym epithets which have not yet been proposed. Actually, recent studies have demonstrated that the current species diversity as listed by Guiry and Guiry (2010) is wider than the existing diversity in the field. As an example, latest works by Mattio and collaborators (2008, 2009, 2010) pointed out 47 new synonymies and underlined numerous misidentifications thus reducing the 67 epithets listed in the literature for South Pacific Islands to 14 taxa (20%). By the transfer of S. decurrens to the reinstated genus Sargassopsis, Draisma and Rousseau (2010) further reduced this number to 13 species (Table 1). These works are based on the analysis of types corresponding to 103 taxa, relevant original diagnoses, vouchers listed in the literature and new extensive collections from worldwide localities. It must be noted here that Guiry and Guiry (2010)’s list does not encompass all existing Sargassum’s taxon names (species, varieties and formas; pers. obs.) which renders the estimation of Sargassum taxa number even more uncertain.

Table 1 Number of Sargassum taxa listed in the literature and number of actual taxa after taxonomic revision for South Pacific Islands according to (a) Mattio et al. (2008), (b) Mattio et al. (2009), and (c) Mattio and Payri (2009)
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Conclusion, Perspectives and Recommendations

Currently, Sargassum is divided into four subgenera (S. subgen. Sargassum, Bactrophycus, Arthrophycus and Phyllotrichia). However, new insights have led to the hypothesis that S. subgen. Arthrophycus could be merged to S. subgen. Bactrophycus, and that S. subgen. Phyllotrichia could be transferred to the reinstated genus Sargassopsis. These hypothesis need to be tested implementing studies based on a larger sampling, including the type species for these subdivisions. Beside, only S. subgen. Bactrophycus, and S. subgen. Sargassum are subdivided into sections. In this paper, we propose that two sections of the S. subgen. Bactrophycus: S. sect. Halochloa and Repentia be merged, thus reducing the number of S. subgen. Bactrophycus sections from five to four (S. sect. Halochloa, Hizikia, Spongocarpus, and Teretia). The subdivisions of S. subgen. Sargassum were considerably simplified since its establishment by J. Agardh (1889), all below-section ranks have been abandoned and traditional sections have been significantly revised. The subgenus is now currently subdivided into eight sections: S. sect. Sargassum, Zygocarpicae, Polycystae, Ilicifolia, Binderiana, Johnstonii, Lapazaenum, and Sinicola. The last three sections as well as two possible new ones need to be assessed further. A summary of the actual classification is given in Fig. 4 and Appendix 4 along with an identification key for Sargassum subdivisions in Table 2.

Fig. 4
figure 4

Taxonomy history synthesis for taxa sequenced since year 2000. The synthetic topology presented was compiled visually from results obtained with ITS-2, partial Rusbisco and cox3 by Stiger et al. (2000, 2003), Phillips and Fredericq (2000), Phillips et al. (2005), Mattio et al. (2008, 2009, 2010); Mattio and Payri (2009), and Draisma and Rousseau (2010). (?) indicate the likely position of taxa not yet confirmed by DNA analyses. The classification proposed by the authors of taxa (by default by J. Agardh, 1889), the revision of this classification by following authors, and the latest classification as proposed the most recently are indicated. Abbreviations follow Table 3 and bibliographic references are listed in Table 4

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Table 2 Identification key for Sargassum subdivisions. NB: Norris (2010)’s sections could not be considered for the construction of the key because the available diagnoses could fit several of the below sections (cf. main text for more details)
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Table 3 Abbreviations used in Fig. 4
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Table 4 Bibliographic references used in Fig. 4
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Phylogenetic methods have become routinely used in systematic. According to Stuessy and König (2008), the main rules of these methods are: (i) only synapomorphies are important for the discrimination of a phylogenetic tree’s branches, (ii) only monophyletic groups are acceptable, (iii) the classification must only be based on topologic patterns, and (iv) sister clades should be of same rank. DNA markers used recently in the study of Sargassum (ITS-2, partial Rubisco, cox3, 23S) have led to significant new insights on the genus’ phylogeny and allowed reconsidering the taxonomic placement of several entities. Notably, they confirmed the monophyly of S. subgen. Sargassum and detected the polyphyly of several of its subdivisions (S. sect. Zygocarpicae and Acanthocarpicae) thus pointing out to the incongruity of morphological characters traditionally used to define them. Several new sections have been proposed and part of the genus has been revised according to a simplified scheme (Fig. 4, Table 2, Appendix 4).

The efficiency of traditional morphological characters used to differentiate taxa (subgenera, sections or infrageneric taxonomic ranks) has been questioned, and the consideration of these characters, one by one, showed few synapomorphies (Mattio et al., 2010). Molecular phylogenies are not based on morphological characters; it is thus not surprising that they cluster taxa, originally classified in groups considered as morphologically homogeneous into different clades. For example, S. sect. Acanthocarpicae, which was traditionally identified on ‘spiny’ receptacles, appeared as polyphyletic (Mattio et al., 2010). In this case, the appendices traditionally named ‘spines’ are probably from different ontogenic origin. Thus, the ‘spines’ of S. hystrix (S. sect. Sargassum) are different from that of S. aquifolium (S. sect. Binderiana) or S. ilicifolium (S. sect. Ilicifolia). In the first one, they appear as extensions on the surface of receptacles, thin and linear like a ‘hair’, whereas in the latter two the receptacle’s margin is dented. These expansions of different types, and probably different origins, had been interpreted as the same character named ‘spine’ leading previous authors to classify S. hystrix and S. ilicifolium within the same section (S. sect. Acanthocarpicae). Similar situations may be encountered for other Sargassum infrageneric groups.

To overcome these difficulties and to progress toward a simplified taxonomy, more representative of the real diversity of the genus, we recommend that the genus be drastically revised following a two-pronged approach: first, the revision of the species diversity carried out by geographical region and second, the revision of the classification.

The species diversity may be re-evaluated through a four step taxonomic revision approach including:

  1. (i)

    An alpha-taxonomic study of the specimens based on morphological characters of traditional taxonomic value (see section  Morphology of this paper) to distinguish morphotypes. Morphotypes are considered as groups of morphologically similar specimens, showing characters included within a morphological range which may represent a taxonomic entity corresponding to a species or an inferior taxonomic rank. The morphological range is defined according to the polymorphism of the specimens of interest as observed at intra-individual, and intra and inter-population levels taking into account as much as possible the ontogenic and phenotypic variability for various worldwide localities.

  2. (ii)

    An analysis of at least three DNA markers for which comparative data are available in the literature and on GenBank, in the case of Sargassum: the nuclear ITS-2, the chloroplastic partial Rubisco and the mitochondrial cox3. Supplementary and more variable markers need to be assessed for discriminating the closely-related species of S. sect. Sargassum. Draisma and Rousseau (2010) underlined that the mitochondrial spacer proposed by Coyer et al. (2006) could be used as DNA barcode marker in Sargassum. However, its usefulness has yet to be tested.

  3. (iii)

    A comparison of morphological and DNA data. The aim is to test the monophyly of morphotypes defined above, the taxonomic value of morphological characters used to define them, and the subjectivity linked to the interpretation of these characters’ variability. Two results may arise: either morphotypes are congruent with clades or not. In the latter case, the morphotype may be poly- or paraphyletic, or several morphotypes may be found within the same clade. If the morphotype is poly- or paraphyletic, going back to the morphological observations may help to identify new morphological characters which taxonomic informativeness was not suspected, or morphological variations were misinterpreted as intra-specific polymorphism. If several morphotypes are found within the same clade, either the morphological variations were wrongly interpreted as inter-specific differences or the DNA marker(s) used is (are) not variable enough to discriminate the morphologically well differentiated morphotypes. The main limit encountered when using above listed markers is the lack, even the absence, of variability in sequences obtained for S. sect. Sargassum taxa yet discriminated based on well established morphological differences. This lack of variability has been interpreted as the mark of recent radiation (Mattio et al., 2008; Mattio & Payri, 2009), but more variable markers have to be explored to test this hypothesis. It is important to note that if the DNA analysis cannot a priori replace a traditional taxonomic study, it may put forward inconsistencies in the interpretation of morphological characters and thus represents a supplementary taxonomic character to be considered for species delineation.

  4. (iv)

    Finally, a first identification of morphotypes may be done with data from local literature (identification keys, Floras, and phylogenies) which would have to be confirmed through the careful study of original diagnoses and types (loan or visit to herbaria) for the suspected species. A comparison of morphology and DNA sequences with specimens from the type locality is recommended. If several names can be applied to the same morphotype, and only after effective examination of types, the taxon earliest published would be considered as the current name while the other epithet(s) may be proposed as heterotypic synonym(s) (Art. 11.4, ICBN).

The classification may be re-evaluated by testing the following nul hypothesis: “the traditional classification is similar to the phylogenetic classification”. If the nul hypothesis is accepted it is then possible to be confident with the traditional classification. If the nul hypothesis is rejected, it is necessary to understand why the traditional classification is different from the phylogenetic classification and how to adapt it (or revise it) to find consistency between the two. One of the main source of inconsistency is of topologic order, ie. the arrangement of taxa in the traditional and phylogenetic classifications are different. The most frequent case is that of non-monophyly of traditional taxa: a taxon may be either polyphyletic or paraphyletic.

  1. (i)

    If a section (or another infrageneric entity) is paraphyletic (ie. it doesn’t include all taxonomic entities found in the relevant clade), the relevant taxa may be transferred from the section, within which they are traditionally classified, to that indicated by phylogenetic analyses. A second option may be to merge the sections which taxonomic entities form a single clade.

  2. (ii)

    If a section is polyphyletic, ie. taxonomic entities traditionally attributed to this section are found in two (or more) distinct clades, only taxa grouped in the same clade as the type for the section should be considered as part of the section. Taxa found in a different clade may be either transferred to the section corresponding to the relevant clade or attributed to a new section.

In both instances, when amending or describing a section, it is necessary to know (i) the position of the section’s type which will ascertain the clade corresponding to the section(s) of interest (Art. 7 & 10 ICBN), (ii) the anteriority of taxa which will determine the epithet to be conserved when merging two taxonomic groups (Art. 11.4 & 11.5 ICBN), and (iii) the diagnostic characters of the group.