morphological and molecular assessment of sargassum (fucales...

Research Article

Morphological and molecular assessment of Sargassum (Fucales,Phaeophyceae) from Caribbean Colombia, including the proposal ofSargassum giganteum sp. nov., Sargassum schnetteri comb. nov. andSargassum section Cladophyllum sect. nov.

OLGA CAMACHO1,2, LYDIANE MATTIO3, STEFANO DRAISMA4, SUZANNE FREDERICQ1 & GUILLERMO

DIAZ-PULIDO5

1Department of Biology, University of Louisiana at Lafayette, LA 70504�2451, USA2Programa de Biolog�ıa Marina, Universidad de Bogot�a Jorge Tadeo Lozano, Carrera 4 # 22�61, Bogot�a, Colombia3Department of Biological Sciences and Marine Research Institute, University of Cape Town, 7701 Rondebosch, South Africa4Institute of Ocean & Earth Sciences, University of Malaya, 50600, Kuala Lumpur, Malaysia5Griffith School of Environment, Australian Rivers Institute � Coast & Estuaries, and ARC Centre of Excellence for Coral Reef Studies,Nathan Campus, Griffith University, 170 Kessels Road, Brisbane, Nathan, Qld 4111, Australia

(Received 22 February 2014; accepted 12 August 2014)

The use of molecular markers to evaluate species delineation in the genus Sargasssum is of critical importance given thelarge variability of morphological traits among and within taxa. To date, most molecular studies of this group have focusedon the central Indo-Pacific region, even though the genus is also well represented in the Atlantic Ocean. In the presentstudy, we re-assessed the diversity and taxonomy of Sargassum and the monospecific genus Cladophyllum from CaribbeanColombia (especially from the Santa Marta-Tayrona National Natural Park) and extended to the western tropical Atlantictowards a comprehensive revision of the genus in this basin based on morphological and molecular analyses (ITS-2, rbcLS,cox3 and mtsp) on new and existing collections from the region. Sequences obtained from the genus Cladophyllum revealedits nesting inside Sargassum subgenus Sargassum as a close relative of S. pteropleuron, a broadly distributed species in theCaribbean. Analysis of molecular divergence in this newly identified clade demonstrated a similar range of variation as thatpresent in existing sections leading to the description of a new section, Sargassum sect. Cladophyllum (Bula-Meyer)Camacho, Mattio & Diaz-Pulido, sect. nov., that includes the two sister species mentioned above. Based on these results,we also merged Cladophyllum within Sargassum and renamed its unique species S. schnetteri (Bula-Meyer) Camacho,Mattio & Diaz-Pulido, comb. nov. The remaining Sargassum spp. included in the analyses clustered in a polytomy withinthe worldwide-distributed S. section Sargassum, thus providing no support for the other eight morphological speciescurrently recognized in the Caribbean Colombia and other western tropical Atlantic areas. Based on the morphologicalanalysis we further described a new species, S. giganteum Camacho & Diaz-Pulido sp. nov., endemic from TNNP. Detailedmorphological descriptions and illustrations, as well as an identification key, are provided for all studied taxa.

Key words: Caribbean Colombia, Cladophyllum, cox3, DNA, endemism, Fucales, ITS-2, phylogeny, rbcLS, Sargassum,taxonomy

IntroductionThe widespread tropical to temperate marine algal genus

Sargassum C. Agardh (Fucales, Phaeophyceae) is one of

the most taxonomically difficult and species-rich genera

in the brown algae, accounting for 336 currently recog-

nized species (Guiry & Guiry, 2014). The classification

system proposed by J. Agardh (1848, 1889) initially

included five subgenera, further subdivided into sections,

subsections and series. This traditional classification

scheme based on polymorphic morphological characters

(holdfast, axes, phylloids or ‘leaves’, air vesicles and

receptacles) had been accepted by most phycologists, in

some instances with minor modifications (e.g. Abbott,

Tseng, & Lu, 1988; Ajisaka, Noro, & Yoshida, 1995;

Grunow, 1915, 1916; Setchell, 1931, 1933, 1936; Tseng &

Lu, 1988, 1992a, 1992b; Womersley, 1954, 1987; Yoshida,

1983, 1988; Yoshida, Ajiksaka, Noro, & Horiguchi, 2004).Correspondence to: Olga Camacho. E-mail: [email protected]

ISSN 1477-2000 print / 1478-0933 online

This article was originally published with errors. This version has been amended. Please see Corrigendum (http://dx.doi.org/10.1080/14772000.2015.1009703).

� The Trustees of the Natural History Museum, London 2014. All Rights Reserved.

http://dx.doi.org/10.1080/14772000.2014.972478

Systematics and Biodiversity (2015), 13(2): 105�130

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mailto:[email protected]

mailto:[email protected]

http://dx.doi.org/10.1080/14772000.2015.1009703

http://dx.doi.org/10.1080/14772000.2014.972478

However, with the recent use of molecular markers, and

as more taxa from various regions became included in the

global phylogeny of Sargassum, the traditional classifica-

tion led to revisions and subsequent division of the genus

into two subgenera and nine sections with the abandon-

ment of the lower subdivisions (Dixon, Huisman,

Buchanan, Gurgel, & Spencer, 2012; Dixon Mattio,

Huisman, Payri, Bolton, & Gurgel, 2014; Mattio, 2013;

Mattio & Payri, 2011; Mattio, Payri, & Verlaque, 2009;

Mattio, Payri, Verlaque, & De Reviers, 2010; Phillips &

Fredericq, 2000; Phillips, Smith, & Morden, 2005; Stiger,

Horiguchi, Yoshida, Coleman, & Masuda, 2000; Stiger,

Horiguchi, Yoshida, Coleman, & Masuda, 2003; Yoshida,

Stiger, Ajisaka, & Noro, 2002).

It is now well recognized that the use of molecular

markers to assess species delineation in Sargassum is of

critical importance (Mattio & Payri, 2011), considering

the large variability of morphological traits among and

within taxa, particularly in response to environmental

conditions and ontogeny (e.g. Gillespie & Critchley,

2001; Kilar & Hanisak, 1988, 1989; Kilar, Hanisak, &

Yoshida 1992; Paula & Oliveira, 1982). In spite of tax-

onomic advances, most molecular studies on Sargassum

have focused mainly on the central Indo-Pacific region.

A single study has explored the diversity of the genus

in the Atlantic Ocean (Phillips & Fredericq, 2000)

suggesting the presence of only the Sargassum section

Sargassum in the Gulf of Mexico, with eight of the 21

species recorded for the western Atlantic (Wynne,

2011).

In the southern Caribbean, species of the family Sargas-

saceae form large seasonal beds along rocky shores, par-

ticularly along the coast of Colombia (e.g. Santa Marta

and Tayrona National Natural Park [TNNP]), Venezuela

and Curacao (Camacho & Hernandez-Carmona, 2012;

D�ıaz-Piferrer, 1967; Engelen, Aberg, Olsen, Stam, &

Breeman, 2005; Schnetter, 1981). These beds include

mostly Sargassum and Turbinaria species, but also the

endemic and mono-specific genus Cladophyllum (C.

schnetteri Bula-Meyer), reported growing only on an

18 km stretch of a rocky shore in the TNNP (Bula-Meyer,

1980). Considering its extremely narrow distribution, C.

schnetteri may therefore represent a potentially endan-

gered species as suggested for other species with similar

limited distribution (Brodie, Andersen, Kawachi, &

Millar, 2009). However, since its original description in

1980, no further studies related to the taxonomy, ecology

or phenology of this species have been undertaken. Simi-

larly, 11 species of Sargassum have been listed for the

entire Caribbean Colombia (Diaz-Pulido & Diaz-Ruiz,

2002), but none has yet been assessed molecularly. More

than half of these Colombian Sargassum species have

been reported inside the TNNP (Camacho, 2003) along its

short coastal stretch of approximately 80 km. This marine

natural park is characterized by high variability in envi-

ronmental conditions, such as annual upwelling events

and geomorphologic heterogeneity, which allow the

development of high marine floral and faunal

diversity (Bula-Meyer, 2001; Diaz, 1995). Furthermore,

the TNNP is of particular interest for its algal endemism

in that, in addition to Cladophyllum, other endemic spe-

cies have been discovered, for instance in the Phylum

Rhodophyta, i.e. Champiocolax sarae Bula-Meyer,

Grateloupiocolax colombiana Schnetter & Bula-Meyer,

and Jania sanctae-marthae Schnetter (Bula-Meyer,

1985; Schnetter, 1972; Schnetter, Richter, Schemer, &

Bula-Meyer, 1983).

The main goal of the present study was to reassess the

diversity and taxonomic positions of Sargassum spp. and

Cladophyllum in Caribbean Colombia, especially from

Santa Marta-TNNP, and extended to the western tropical

Atlantic towards a comprehensive revision of the genus in

this basin. For this purpose, we used a combination of

morphological and molecular analyses on recent and pre-

viously established collections from the region. Detailed

morphological descriptions and illustrations are provided,

as well as an identification key.

Materials and methods

Study area and sample collection

Specimens of Sargassum, intended for molecular and mor-

phological analyses, were collected along the Caribbean

coast and oceanic atolls of Colombia (off the continental

shelf of Nicaragua) from various depths and seasons, and

complemented with additional samples from Caribbean

Panama, the Gulf of Mexico, the Florida Keys, North Caro-

lina, and Puerto Rico. Samples were collected by scuba div-

ing or snorkelling for benthic Sargassum species and from

high tide wrack (i.e. beach wash) or from drift for pelagic

taxa. Because of the easy access and abundance

of Sargassum in the northern coast of Colombia,

specifically in Santa Marta-TNNP (11�060�11�210N and

74�030�74�200W), seasonal collection efforts for morpho-

logical examination were concentrated in this area between

2002 and 2009. Samples of Cladophyllum schnetteri were

collected from the type locality in Ensenada de Neguanje

(Colombia) in 2009 (Bula-Meyer, 1980). For morphological

observation of vegetative and reproductive structures, col-

lected material of Sargassum and Cladophyllum were dried

as herbarium specimens and sub-samples were preserved in

4% formalin-seawater. For DNA analysis, apical parts of

the thallus, or preferably receptacles when present, were

preserved in silica gel for later extraction. Vouchers from

the present study were deposited in the herbarium collection

at LAF (University of Louisiana at Lafayette) and UTMC

(Universidad del Magdalena, Santa Marta, Colombia).

106 O. Camacho et al.

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Morphological examination

Morphological analyses were conducted on both recently

collected and herbarium-preserved specimens. Examined

herbaria included UTMC (10 specimens), the personal

herbarium of Bula-Meyer (BM, 70 specimens) deposited

at UTMC, LAF (35 specimens), MICH herbarium (127

specimens) and the personal herbarium of Guillermo

Diaz-Pulido (GD-P, 10 specimens). Relevant type speci-

mens (scans) from the collection of Agardh at LD (Lund,

Sweden), Børgesen at C (Copenhagen, Denmark), Gru-

now at W (Vienna, Austria), Linnaeus at LINN (London,

UK), and Montagne at PC (Paris, France) were also com-

pared. Cladophyllum schnetteri was identified following

the diagnosis by Bula-Meyer (1980) and the examination

of the isotype specimens located at UTMC (no. 07510)

and MICH (no. 1306267). Macroscopic analysis for all

specimens included examination of the shape, size and

characteristics of the holdfast, stem (or main axis),

branches, leaves (or phylloids), vesicles and receptacles.

In the present paper, we refer to phylloids as leaves fol-

lowing the widely accepted terminology in Sargassum.

To analyse the shape and size of the cryptostomata, speci-

mens were observed under a dissecting microscope.

Hand-made cross-sections of receptacles were observed

under a light microscope to determine their sex. Morpho-

logical measurements included length and width of leaves,

vesicles, cryptostomata and receptacles (15�20 leaves/

thallus, 15 vesicles/thallus, 75�100 cryptostomata/thallus

and 15 receptacles/thallus). The number of vesicles was

counted separately for each thallus in benthic taxa (e.g. S.

filipendula) and on short branches (up to 15 cm long) in

pelagic taxa (i.e. S. fluitans and S. natans) (see range of

measurements in the Taxonomy section). According to

the corresponding observations and measurements, the

samples were sorted into morphotypes, considered as

groups of morphologically similar specimens showing

characters within a specific range of variation. The follow-

ing literature was used for species identification: C.

Agardh (1820, 1824), J. Agardh (1848, 1889), Bertossi

and Ganesan (1973), Børgesen (1914a,1914b), Chapman

(1963), Dawes and Mathieson (2008), Earle (1969),

Grunow (1916), Harvey (1852), Howe (1920), Joly

(1957), K€utzing (1849, 1861), Martius (1833), Montagne

(1837), Paula (1988), Schnetter (1976) and Taylor (1928,

1942, 1960).

DNA processing and phylogenetic analyses

DNA extractions and PCR amplifications were conducted

at the Plateforme du Vivant, IRD (Institut de Recherche

pour le D�eveloppement) in Noum�ea, New Caledonia, and

at the Seaweeds Lab at the University of Louisiana at

Lafayette, USA. Silica gel-dried material (Table 1) was

ground in liquid nitrogen and total DNA extracted using

the DNeasy Plant mini Kit (Qiagen GmbH., Hilden, Ger-

many). All extracts were purified using the Geneclean kit

III (Qbiogen Inc., Carlsbad, CA, USA) prior to PCR

amplification. DNA extraction from old herbarium speci-

mens (e.g. BM, GD-P) was attempted using a modified

Dellaporta, Wood, and Hicks (1983) protocol described

by Hughey, Silva, and Hommersand (2001) without suc-

cess, probably due to previous formalin fixation of the

material. We chose to amplify the nuclear Internal Tran-

scribed Spacer 2 (ITS-2), the chloroplast-encoded partial

rbcL C spacer C partial rbcS (hereafter mentioned as

rbcLS), and the mitochondrial Cytochrome c Oxydase

subunit 3 (cox3) regions because of their wide use in Sar-

gassum phylogenetics (e.g. Dixon et al., 2012; Mattio &

Payri, 2011) therefore ensuring sequences availability on

GenBank for molecular context. We also amplified a

mitochondrial spacer region (mt 23S-tRNA-Val intergenic

spacer referred to in the text as mtsp), whose potential

value for the study of closely related species of Sargassum

was suggested by Draisma, Ballesteros, Rousseau, and

Thibaut (2010). PCR products were obtained using pri-

mers listed in Coyer, Hoarau, Oudot-Le Secq, Stam, and

Olsen (2006) and Mattio, Payri, and Stifer-Pouvreau

(2008). The 25 mL PCR reaction mix contained 0.2 mMof forward and reverse primers, 0.2 mM of each dNTP,

1.5 mM of MgCl2, 5 mL of reaction buffer, 1 mL of puri-

fied template DNA, 1.25 units of Taq DNA polymerase

(Sigma, St. Louis, MI, USA) and pure water. The reaction

profile included: (i) an initial 1 min long step of denatur-

ation at 94 �C, (ii) 40 cycles of denaturation at 94 �C for

40 s, (iii) primer annealing (respectively 55 �C, 44 �C,42 �C, and 50 �C for each of the above listed markers) for

30 s, (iv) extension at 72 �C for 45 s, and (v) a final exten-

sion step at 72 �C for 7 min. PCR products were purified

and sequenced in both directions using the BigDyeTM ter-

minator v 3.1 method by Macrogen (Seoul, Korea) and

Beckman Coulter Genomics (Danvers, MA).

Sequences were aligned with ClustalW in BioEdit

(Hall, 1999). Cox3 and rbcLS aligned unambiguously

while the ITS-2 alignment required adjustment by eye

using the alignments of Mattio et al. (2010) and Stiger

et al. (2003) as guides. Mtsp sequences were very variable

and their alignment was only possible between closely

related species of S. section Sargassum. As a conse-

quence, mtsp sequences could not be included in the

concatenated alignment. Following concatenation of

cox3, rbcLS and ITS-2, the best-fit model and partitioning

strategy for the dataset was estimated using Partitionfinder

(Lanfear, Calcott, Ho, & Guindon, 2012). This analysis

resulted in the selection of the General Time Reversible

plus Gamma model applied separately for each marker,

and per codon position for the protein-encoding regions

(i.e. cox3, rbcL and rbcS). The best-fit model found for

Morphological and molecular assessment of Sargassum 107

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Table 1. Taxa included in molecular analyses with the vaucher reference, collection sites, collectors, collection dates and GenBankaccessions. Accessions numbers in bold correspond to sequences newly obtained in this study.

VaucherGenBank accessions

Taxon name revised number

Collection site; Collector;Collection date ITS-2 rbcLS cox3

Sargassum schnetteri LAF06612 Colombia, Magdalena, Neguanje(TNNP); O. Camacho; May2009

KF437949 KF437962 KF437931

Sargassum schnetteri LAF04287A Colombia, Magdalena, Neguanje(TNNP); O. Camacho; Nov2009

KF437950 KF437963 KF437932

Sargassum aquifolium IRD1531 New Caledonia, Ile des Pins; L.Mattio; Dec 2005

EU100800 EU100808 EU882243

Sargassum aquifolium IRD1681 Vanuatu, Santo; L. Mattio; Aug2006

EU833456 EU833476 EU833412

Sargassum aquifolium IRD1582 Fiji, Navutulevu rf.; L. Mattio;May 2007

EU833432 EU833464 EU833406

Sargassum aquifolium IRD1660 Solomon, Malaita Is. ST850; C.Payri; Jul 2004

EU833447 EU833462 EU833397

Sargassum aquifolium Sh01466 Hawaiian Is., Ohau; T. Sauvage;Oct 2006

EU100796 EU100821 EU100835

Sargassum carpophyllum IRD1511 New Caledonia, Feycinet Is.; L.Mattio; Jul 2005

EU100797 EU100804 EU833415

Sargassum cf. cymosum LAF06602 Colombia, Magdalena, Granate(TNNP); O. Camacho; May2009

KF437935 � KF437919

Sargassum cf. cymosum LAF06614 Colombia, Magdalena, PlayaBlanca; O. Camacho; May2009

KF437944 KF437961 KF437928

Sargassum cymosum LAF04290 Colombia, Magdalena, Granate(TNNP); O. Camacho; Apr2009

KF437936 KF437953 KF437920

Sargassum cymosum LAF06609 Colombia, Magdalena, Concha(TNNP); O. Camacho; Apr2009

KF437939 KF437956 KF437923

Sargassum cymosum LAF06610 Colombia, Magdalena, Concha(TNNP); O. Camacho; Apr2009

KF437940 KF437957 KF437924

Sargassum cymosum LAF06613 Colombia, Magdalena, Neguanje(TNNP); O. Camacho; May2009

KF437943 KF437960 KF437927

Sargassum filipendula LAF04288 Colombia, Magdalena, Punta LaLoma; O. Camacho; Apr 2009

KF437938 KF437955 KF437922

Sargassum filipendula LAF04106 Panama, Zapatilla Cay; O.Camacho; Aug 2010

KM461671 KP064347 KP064332

Sargassum filipendula LAF04256 Panama, Bocas del Toro, FlatRock Beach; S. Fredericq;Aug 2010

KM461672 KP064348 KP064333

Sargassum filipendula LAF04275 United States, North Carolina,Masonboro; O, Camacho;May 2011

KM461673 KP064349 KP064334

Sargassum fluitans LAF04276 United States, North Carolina,Fort Fisher, drift; O,Camacho; May 2011

KM461674 KP064350 KP064335

Sargassum fluitans LAF06920 United States, Gulf of Mexico,Holly Beach; O. Camacho;Jun 2014

KM461675 KP064351 KP064336

Sargassum giganteum LAF06605 Colombia, Magdalena, Granate(TNNP); O. Camacho; Mar2009

KF437945 � KF437929

(continued)


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Table 1. (Continued )




Sargassum giganteum LAF06607 Colombia, Magdalena, Granate(TNNP); O. Camacho; Apr2009

KF437946 � KF437930

Sargassum giganteum LAF04289 Colombia, Magdalena, Granate(TNNP); O. Camacho; Apr2009

KF437947 � KP064337

Sargassum hystrix LAF04292 United States, Gulf of Mexico,Geyer Bank; EmmaHickerson; Sep 2011

KM461676 KP064352 KP064338

Sargassum hystrix LAF04131 United States, Gulf of Mexico,Geyer Bank; EmmaHickerson; Sep 2011

KM461677 KP064353 KP064339

Sargassum ilicifolium IRD1589 Fiji, Kiuva reef; L. Mattio, May2007

EU833439 EU833470 �

Sargassum ilicifolium IRD3931 New Caledonia, Crouy; L.Mattio; Jun 2006

FJ170443 FJ170387 FJ170416

Sargassum ilicifolium GENT-TZ0852 Tanzania, n.a.; H. Verbruggen;Jan 2008

HQ416061 HQ416022 HQ416133

Sargassum natans LAF06919 United States, Gulf of Mexico,Holly Beach; O. Camacho;Jun 2014

KM461678 KP064354 KP064340

Sargassum natans LAF06437 United States, Gulf of Mexico,offshore LA, drift; O.Camacho; Jun 2014

KM461679 KP064355 KP064341

Sargassum micracanthum IRD5222 Japan, Mitohama, Misaki; F.Mineur; Oct 2010

KF281945 � KF281993

Sargassum obtusifolium UPF2651 French polynesia, Rapa,Australs; C. Payri; Nov 2002

EU100785 EU100819 EU100830

Sargassum pacificum UPF2754 French polynesia, Bora Bora; C.Payri & V. Stiger; Mar 2003

EU100783 EU100812 EU100824

Sargassum polyceratium LAF04291 Colombia, Magdalena, Neguanje(TNNP); O. Camacho; May2009

KF437942 KF437959 KF437926

Sargassum polyceratium LAF04105 Panama, Big Plantain Cay; O.Camacho; Aug 2010

KM461680 � KP064342

Sargassum polyceratium LAF03947 Panama, East Rio Ca~naveral; O.Camacho; Aug 2010

KM461681 KP064356 KP064343

Sargassum cf. polyceratium LAF04185 Puerto Rico, Ponce, Caleta deCabullones; O. Camacho; Sep2002

KM461682 KP064357 KP064344

Sargassum polycystum ARV144 Reunion Is., Cap la Houssaye;M. Zubia; Jul 2010

KF413701 KF413688 KF413707

Sargassum polycystum IRD1571 Fiji, Makuluva Is.; L. Mattio;Apr 2007

EU833422 EU833471 EU833405

Sargassum polyphyllum IRD1613 New Caledonia, Maıtre Is.; L.Mattio; Sep 2005

EU833424 EU833458 EU833385

Sargassum portierianum BOL44348 Mauritius, Flic en Flac; L.Mattio; Jun 2011

KF413704 KF413685 KF413715

Sargassum pteropleuron LAF06913 United States, Florida,Newfound Harbor Key; O.Camacho; April 2014

KM461683 KP064358 KP064345

Sargassum pteropleuron LAF06917 United States, Florida,Summerland Key; O.Camacho; April 2014

KM461684 KP064359 KP064346

(continued)


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mtsp was Felsenstein 1981 plus Gamma. The Maximum

likelihood (ML) tree reconstruction was performed in

RAxML (Stamatakis, 2006) on the partitioned (ITS-2 CrbcLS C cox3) dataset as above with 1000 restarts to find

the best tree (lowest likelihood score) and 1000 bootstrap

(BS) replications. Bayesian MCMC (Monte Carlo Markov

Chain) was also applied to the concatenated dataset using

MrBayes v.3.2.1£64 (Huelsenbeck & Ronquist, 2001;

Ronquist & Huelsenbeck, 2003). Bayesian analysis con-

sisted of two independent runs of three heated chains and

one cold chain, run for seven million generations and sam-

pled every 100 generations (total of 140 002 trees). Con-

vergence was visualized in Tracer v1.5, and the first

17 500 trees were discarded as burn-in. The Bayesian con-

sensus tree and best ML tree were rooted with species of

Sargassum subgenus Bactrophycus, representing the clos-

est phylogenetic group to S. subgenus Sargassum (e.g.

Dixon et al., 2014). Results were visualized in FigTree

v1.3.1 (Drummond & Rambaut, 2007). The resulting ML

tree obtained from the concatenated alignment also shows

posterior probabilities (PP) taken from Bayesian consen-

sus tree (Fig. 1). Analysis of the mtsp marker was carried

out in MrBayes v.3.1.2£64 (as above but for 3 million

generations, a total of 60 002 trees and 10% trees

discarded as burn-in) and rooted with a sequence of S.

carpophyllum J. Agardh.

Pairwise genetic distances were calculated from the

branch lengths of the best RAxML tree with the Package

APE in R (Paradis, Claude, & Strimmer, 2004). The

resulting distance matrix was used to extract the maxi-

mum genetic distance of representative clusters of sequen-

ces representing sections in subgenus Sargassum and

reported in the margin of the phylogenetic tree (Fig. 1).

Results

Morphological analysis

The examination of the 370 specimens of Sargassum and

Cladophyllum specimens collected in the present study

and the 252 specimens from existing herbarium material

examined led to the determination of 10 morphotypes in

the western tropical Atlantic region. The most distinctive

morphotype is that of Cladophyllum, distinguished from

the others by the presence of a rhizomatous base (or hold-

fast) and absence of vesicles (Figs 2�5). Eight of those 10

morphotypes were congruent with descriptions previously

reported in the literature for the western Atlantic (e.g.

Table 1. (Continued )




Sargassum scabridum WELT-A028417 New Zealand, Auckland; W.Nelson; 2005

FJ170456 FJ170393 FJ170423

Sargassum stenophyllum LAF06611 Colombia, Magdalena, Concha(TNNP); O. Camacho; Apr2009

KF437941 KF437958 KF437925

Sargassum spinuligerum f. crispata IRD3978 New Caledonia, ılot Signal; L.Mattio; 2005

FJ170462 FJ170401 FJ170428

Sargassum cf. spinuligerum GENT-TZ0400 Tanzania, Mtwara, MikindaniBay; K. Pauly; Jan 2008

HQ416072 HQ416019 HQ416131

Sargassum swartzii IRD3912 New Caledonia, ılot Maıtre; L.Mattio; Sep 2005

EU882255 EU882264 �

Sargassum swartzii IRD1532 New Caledonia, Thio, C.Bertaut; Apr 2006

EU882254 EU100807 KF413706

Sargassum thunbergii IRD5223 Japan, Mitohama, Misaki; F.Mineur; Oct 2010

KF281946 � KF281994

Sargassum thunbergii IRD5241 Japan, Mitohama, Misaki; F.Mineur; Oct 2010

KF281927 KF281785 KF281980

Sargassum turbinarioides IRD1604 New Caledonia, Ile des Pins; C.Payri; Dec 2005

EU882256 EU882265 EU882245

Sargassum vulgare SZNPattiS-Ca3 Italy; A. Chiarore & F.P. Patti;2012

KJ572482 � KJ572496

Sargassum vulgare SZNPattiS-Ca4 Italy; A. Chiarore & F.P. Patti;2012

KJ572483 � KJ572494

Sargassum sp. IRD1609 New Caledonia, Rocher �a lavoile; L. Mattio; May 2005

EU882248 EU882259 EU882237


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Earle, 1969; Paula, 1988; Schnetter, 1976; Taylor, 1960),

namely Sargassum cymosum C. Agardh, S. filipendula C.

Agardh, S. fluitans (Børgesen) Børgesen, S. hystrix J.

Agardh, S. natans (Linnaeus) Gaillon, S. polyceratium

Montagne, S. pteropleuron Grunow and S. stenophyllum

Martius (Figs 6�27). Six of these morphotypes exhibit

solid holdfasts and vesicles, except for S. fluitans and S.

natans that do not possess holdfasts. The morphological

identification was further confirmed by examination of the

original diagnoses and relevant type specimens. The

remaining morphotype, found only in TNNP, could not be

assigned to any of the morphological species previously

reported for the western Atlantic or other regions

(Figs 28�31). We describe it here as a new species under

Fig. 1. Maximum likelihood (RAxML) tree of the combined ITS-2, rbcLS and cox3 dataset showing the position of Cladophyllum sect.nov. within Sargassum subgenus Sargassum. Values at the nodes indicate Bootstrap support (left) and Posterior Probability (right); val-ues below 50 are not shown or represented by ‘�’. Infra-sectional genetic distances are indicated in parentheses below each section,except for S. sect. Polycystae. Area abbreviations: C, Colombia; FJ, Fiji; FL, Florida Keys; FP, French Polynesia; GoMX, Gulf of Mex-ico; HI, Hawaii; IT, Italy; JP, Japan; MAUR, Mauritius; NC, New Caledonia; NCar, North Carolina; NZ, New Zealand; PanCar, Pan-ama; PR, Puerto Rico; RUN, Reunion Is.; S, The Solomon Islands; TZ, Tanzania; Va, Vanuatu.


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the name Sargassum giganteum sp. nov. (see Taxonomy

and Discussion sections).

Phylogenetic analyses

A total of 28 ITS-2, 24 rbcLS and 28 cox3 sequences were

newly obtained for specimens from Colombia and other

western tropical Atlantic localities (see Table 1) for the 10

morphotypes listed above. A number of sequences were

downloaded from GenBank to include subgenera and sec-

tions of Sargassum from worldwide collections. The final

alignment included a total of 54 taxa and a total of

1759 nt positions corresponding to the concatenation of

601 nt ITS-2, 724 nt rbcLS and 434 nt cox3.

The overall topology of the tree showed six strongly

supported lineages (BS � 87, PP � 0.98) within Sargas-

sum subgenus Sargassum, five of which correspond to

the currently recognized sections, Binderiana, Ilicifolia,

Polycystae, Sargassum and Zygocarpiceae (Mattio,

2013; Mattio & Payri, 2011) and the newly identified

cluster of sister species including Cladophyllum schnet-

teri and S. pteropleuron. Examination of molecular

divergence within the C. schnetteri�S. pteropleuron

clade revealed a maximum divergence (0.012) that falls

within the range of variation of S. subgenus Sargassum

sections (between 0.008�0.021, Fig. 1). Infra-sectional

molecular divergence could not be assessed meaning-

fully in S. sect. Polycystae since it is represented in our

phylogeny by a single species (i.e. S. polycystum) with

very low sequence variation (3.58E¡06). The sequences

of the eight remaining Caribbean morphotypes clustered

within S. section Sargassum in a polytomy with other

species, such as S. scabridum J.D. Hooker & Harvey

from New Zealand and S. vulgare C. Agardh from Italy

(Fig. 1), overall showing little intraspecific divergence.

Section Sargassum also includes species sequenced

from the south Pacific (French Polynesia, New

Caledonia) and the western Indian Ocean (Mauritius,

Tanzania) which branch prior to the polytomy with low

support (Fig. 1, Appendix 1, see online supplemental

material, which is available from the article’s Taylor &

Francis Online page at http://dx.doi.org/10.1080/

14772000.2014.972478).

The mtsp alignment (172 nt long) including newly

obtained and previously published sequences was proc-

essed independently as resulting sequences appeared to be

very variable and were aligned only by batch of closely

related species such as those of the S. section Sargassum.

However, results of this analysis with mtsp (available

upon request to the authors) did not show any further sig-

nificant resolution when compared with the concatenated

alignment analysis.

Figs 2�5. Sargassum schnetteri comb. nov. (2) Immature specimen. (3) Isotype herbarium specimen (UTMC-07510); female thallus fromEnsenada Neguanje (TNNP), Colombia. (4) Holdfast rhizomatous with vegetative re-growth or new thallus (arrow). (5) Fertile branch withgroups of short receptacles growing in axils of thin leaves. Scales bars represent: Fig. 2, 5 cm; Fig. 3, 5 cm; Fig. 4, 1 cm; Fig 5, 1 cm.


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http://dx.doi.org/10.1080/14772000.2014.972478

http://dx.doi.org/10.1080/14772000.2014.972478

Taxonomy

Morphological description of Sargassum taxa from

Caribbean Colombia and the western tropical Atlantic

Morphological descriptions provided here are based on

material collected by the authors for the purpose of the

present study and confirmed records at different herbaria.

Information on the geographic distribution for Caribbean

Colombia and Panama and Gulf of Mexico follows newly

collected material and records examined in the UTMC,

BM and GD-P herbaria. Distribution in the western Atlan-

tic follows Bertossi and Ganesan (1973), Chapman

(1963), Dawes and Mathieson (2008), Earle (1969),

Fredericq et al. (2009), Ganesan (1989), Littler and Littler

(2000), Moreira and Cabrera (2007), Menezes-Sz�echyand Paula (2010), Ortega, Godinez, and Garduno-Solo-

rzano (2001), Paula (1988) and Taylor (1960).

Sargassum subgenus Sargassum

Sargassum sect. Cladophyllum (Bula-Meyer) Camacho,

Mattio & Diaz-Pulido, stat. nov. � Cladophyllum

Bula-Meyer, Bot. Mar. 23: 555�562. 1980 � Type:

Sargassum schnetteri (Bula-Meyer) Camacho, Mattio &

Diaz-Pulido, this publication (� Cladophyllum schnetteri

Bula-Meyer, Bot. Mar. 23: 556. 1980).

Diagnosis. Thalli composed of either a rhizomatous or a

discoid base (holdfast) and a main axis (or main axes)

from whose apex arise numerous, primary laterals

(branches), with secondary ramifications, bearing leaves

and receptacles with wart-like surface.

Sargassum schnetteri (Bula-Meyer) Camacho, Mattio &

Diaz-Pulido, comb. nov.

(Figs 2�5)

� Cladophyllum schnetteri Bula-Meyer, Bot. Mar. 23:

556. 1980

Type specimen. Holotype: COL000006319. Isotypes:

UTMC-007510 (BM-P76B); COL000006320;

MICH1306267.

Type locality. Ensenada Neguanje (TNNP) Colombia,

Atlantic Ocean (Bula-Meyer, 1980).

Representative material. LAF04287, LAF06612,

LAF06615, UTMC-011404 (BM-198B), UTMC-011405

(BM-96B).

Morphology. Plants up to 70 cm high, dark yellow-

brown. Holdfast rhizomatous, with terete ramifications (or

stolon-like branches) irregularly disposed, up to 1.5 mm

diam., attached to the substratum by small discs and giv-

ing rise to short main axes up to 30 mm high and 2.6 mm

diam. Primary and secondary branches smooth, terete or

slightly compressed, up to 1.5 mm diam. Leaves forked

several times, flat, linear, up to 60 mm long and 1 mm

wide with smooth margins and acute apices. Vesicles

absent. Cryptostomata few or absent.

Plants dioecious. Receptacles terete, dichotomously

branched; female receptacles with wart-like surface up to

8 mm long and 1 mm diam.; male receptacles with bumpy

surface up to 14 mm long and 1.2 mm diam. (For detailed

morphological description, reproduction and embryo

development of this species, see Bula-Meyer, 1980).

Distribution. Endemic to Colombia: Magdalena (TNNP:

Neguanje and Gayraca bays). This species has been

reported and observed growing only along 18 km-long

stretch of coast in this area.

Habitat. On rocky substratum from the upper intertidal

zone, down to 9 m depth, in wave-exposed habitats.

Sargassum pteropleuron Grunow (1868)

(Figs 6�8)

Type specimen. Grunow Herbarium (Krypto-Grunow)

no. 0002204 (W) � Holotype. Grunow (1868 p. 55).

Type locality. Nassau, New Providence Island, Bahamas

Islands, Atlantic Ocean [as ‘Nassau, Neu-Providence.

(Herb. Grunow)’ in Grunow 1868 ‘1867’ p. 55].

Synonymy. Not known.

Representative material. LAF06913, LAF06917.

Morphology. Plants up to 1 (�4) m high, yellow-brown.

Discoid holdfast up to 30 mm diam. Main axis up to

25 cm high and 8 mm diam. with scars of fallen branches

and with or without spine-like projections. Primary

branches cylindrical, up to 5 mm diam. in proximal parts

and up to 2 mm diam. in apical parts, with spine-like pro-

jections more abundant in proximal parts. Secondary

branches not observed. Leaves linear, simple, thick, flat or

triquetrous, 25�100 mm long and 2�4 (�6) mm wide;

margins deeply and irregular serrate, symmetrical bases,

acute apices and conspicuous raised-serrate midrib.

Vesicles 30�150 per thallus; elliptical or spherical, reach-

ing up to 10 mm long and 8 mm diam., mostly smooth,

few with an apical spine-like projection up to 10 mm long

with small teeth, sub-sessile or on a very short stalk. Cryp-

tostomata elliptical or spherical, central pore 75�150 mmlong and 50�100 mm wide. Cryptostomata numerous and

scattered over the surface of leaves, few on vesicles.

Receptacles dichotomously branched, arranged in loose

axillary clusters.

Distribution. Western Atlantic: Bermuda, Gulf of Mex-

ico (Texas, Louisiana), Florida, Bahamas, Caicos Is.,

Greater Antilles (Cuba), Lesser Antilles (Dominica, Vene-

zuela) and Western Caribbean.


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Habitat. Frequent on rocky substrata and coral rubble up

to 4 m depth. Found in protected to moderately exposed

habitats.

Notes. The specimens collected in this study did not

exhibit receptacles; however, their vegetative morphology

was characteristic of the species’ descriptions from the

western tropical Atlantic (e.g. Dawes & Mathieson, 2008;

Earle, 1969; Taylor, 1960). This species was the dominant

taxon at Southwest Newfound Harbor Key along with

Lobophora sp. The latter was observed growing conspicu-

ously on the basal branches of S. pteropleuron as well as

on the substratum.

Sargassum sect. Sargassum

Sargassum cymosum C. Agardh (1820)

(Figs 9�11)

Type specimen. Agardh Herbarium no. 2979 (LD) �Holotype. C. Agardh (1820 p. 20) designated the type

locality as: ‘In mari Atlantico, ad littora Brasiliae’.

Because only one herbarium sheet for S. cymosum in the

Agardh collection at LD is indicated ‘ad littora Brasilia’

(LD2979), we believe it represents the holotype.

Type locality. Brazil, Atlantic Ocean [as ‘In mari Atlan-

tico, ad littora Brasiliae’ in C. Agardh, 1820 p. 20].

Synonymy. S. rigidulum K€utzing 1849, p. 615.


LAF06610; LAF06613, LAF06614, BM-9, BM-45A,

BM-54.

Morphology. Plants up to 70 (�100) cm high, tough and

dark brown. Holdfast discoid up to 40 mm in diam. with

few to several short main axes 2.2�17.5 mm high and

1.7�2.6 mm in diam.; main axes smooth or with scars of

fallen branches. Primary branches coriaceous, smooth,

terete or sometimes compressed, 1�1.8 mm diam., with

secondary and sometimes, tertiary axes. Leaves simple,

flat, thick, oblong to lanceolate (few linear), 15�40 mm

long and 2�4 (�6) mm wide; smooth, crenulate or rarely

serrate margins, symmetrical cuneate to rounded bases,

acute to obtuse apices and conspicuous percurrent midrib;

stipe up to 2 mm long, sometimes with few spines-like

protuberances. Vesicles elliptical or spherical, (0�)

100�180 (�870) per thallus; 1.7�5.7 mm long and

1.5�4.5 mm diam., some with an apical spine-like mucro

up to 3 mm long; stipe 1.6�3.2 (�7.3) mm long and

1 mm diam., often terete, few compressed or alated. Cryp-

tostomata small, elliptical or spherical, central pore

40�130 mm long and 33�100 mm wide; scattered on

leaves and vesicles.

Plants dioecious, occasionally monoecious. Receptacles

arranged in the axils of leaves on secondary or tertiary

branches forming sparsely to densely ramified groups

(cymose) up to 15 mm long, with a short stipe that can

become a sterile axis with lateral receptacles. In mature-

Figs 6�8. Sargassum pteropleuron. (6) Fertile herbarium specimen LAF06913, with Lobophora sp. as epiphyte in proximal parts. (7)Apical part of a branch with leaves and large vesicles. (8) Proximal part of the thallus with discoid holdfast, and main axis and firstbranches with spine-like protuberances. Scales bars represent: Fig. 6, 5 cm; Fig. 7, 2 cm; Fig. 8, 2 cm.


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senescent plants (with few or no leaves and vesicles) the

receptacles form large and dense clusters on the secondary

and tertiary branches. Receptacles terete, 2 to 4 times

dichotomously branched; female receptacles with promi-

nent wart-like surface up to 6 mm long and 0.7 mm diam.;

male receptacles with wart-like surface up to 10 mm long

and 0.5 mm in diam.

Distribution. Colombia: Guajira (Punta Gallinas), Mag-

dalena (Punta Bet�ın, Taganga, TNNP: Granate, Concha,Gayraca, Neguanje). Western Atlantic: Bermuda, Gulf of

Mexico, Florida, Bahamas, Greater Antilles (Cuba, Hispa-

niola), Lesser Antilles (Barbados, Guadaloupe, Trinidad,

Venezuela), Western Caribbean (Mexico), and Brazil.

Habitat. Common on rocky intertidal and subtidal zones

to 3 m deep. Frequent in different places from protected,

moderately exposed to high wave action habitats.

Notes. In agreement with Schnetter (1976), this species was

found to be highly polymorphic along the Caribbean coast

of Colombia, with important intra- and inter-individual mor-

phological variability in the shape of leaves and receptacles.

Sargassum filipendula C. Agardh (1824)

(Figs 12�15)

Type specimen. Agardh Herbarium no. 3253 (LD) �Lectotype, designated from the syntype collection by

Hanisak and Kilar (1990).

Type locality. West Indies ‘India Occidentalis, Aspegren’

[as ‘In sinu mexicano?’ in C. Agardh 1824 p. 300].

Synonymy. Sargassum affine J. Agardh 1848, p. 343;

Sargassum filipendula f. subcirerea Grunow 1916, p. 171.


LAF04275, LAF04288, BM-164.

Morphology. Plants up to 1.25 m high, pyramid-shaped

and dark brown. Holdfast discoid up to 22 mm diam.

Main axis up to 4 cm high and 3 mm diam., with scars of

fallen branches. Primary branches smooth, terete,

1�1.5 mm diam. Leaves linear, simple or occasionally

forked, thick, flat, (30�) 40�90 (100) mm long and

3�7 mm wide; serrate margins, mostly symmetrical but

with some asymmetrical bases, acute apices and conspicu-

ous percurrent midrib; stipe up to 3 mm long, sometimes

with few spine-like protuberances. Vesicles100�630 per

thallus; elliptical or spherical, reaching up to 5 mm long

and 4 mm diam. or smaller, often with an apical spine-

like protuberances up to 7 mm long, some with an apical

leaf up to 2 cm long and 2 mm wide with serrate margin;

Figs 9�11. Sargassum cymosum. (9) Fertile herbarium specimen LAF06613. (10) Fertile branch with receptacles, vesicles and leaves.(11) Main axes with scars of fallen branches and new primary branches at the apex. Scales bars represent: Fig. 9, 5 cm; Fig. 10, 5 mm;Fig. 11, 1 cm.


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long stipe, smooth, up to 7 mm long and 0.6 mm wide,

terete or compressed. Cryptostomata spherical, central

pore of apical leaves 150�200 m diam., central pore of

proximal leaves 75�90 m diam.; numerous and scattered

over the surface of leaves and vesicles.

Plants dioecious. Receptacles arranged on secondary or

tertiary branches, forming loose racemes or cymes up to

30 mm long, sometimes mixed with small leaves and

vesicles. Receptacles terete, simple or sparsely branched;

female receptacles with wart-like surface and up to

20 mm long and 1.2 mm wide; male receptacles with

bumpy surface, up to 25 mm long and 1.0 mm wide.

Distribution. Colombia: Magdalena (Punta La Loma).

Panama: Zapatilla Cay. Western Atlantic: Bermuda, Mas-

sachusetts, North Carolina, Gulf of Mexico (Mexico,

Texas, Louisiana, Mississippi, Alabama), Florida, Baha-

mas, Greater Antilles (Cuba, Hispaniola, Jamaica, Puerto

Rico), Lesser Antilles (Virgin Islands, St. Barth�elemy,

Nevis, Guadeloupe, Dominica, Venezuela), Western

Caribbean (Mexico), Southern Caribbean (Colombia, Pan-

ama) and Brazil.

Habitat. Intertidal and subtidal zones to 3 m depth, in

protected or exposed habitats.

Figs 12�15. Sargassum filipendula. (12) Fertile herbarium specimen LAF04288A. (13) Fertile branch with receptacles intermixed withvesicles and leaves. (14) Apical part of the thallus. (15) Discoid holdfast with two growing thalli. Scales bars represent: Fig. 12, 5 cm;Fig. 13, 2cm; Fig. 14, 2 cm; Fig. 15, 1 cm.


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Notes. Additional morphological and molecular work

need to be done at the infraspecific level in order to accu-

rately designate varieties and forms of S. filipendula

housed in various herbarium collections. For instance,

Wynne (2011) recognized four named varieties, in addi-

tion to the nominate variety for the tropical and subtropi-

cal western Atlantic.

Sargassum fluitans (Børgesen) Børgesen 1914

(Figs 16�17)

Type specimen. Børgesen Herbarium at C (C-A-92173)

collected in the Danish West Indies by F. Børgesen in

1895�1896 � Lectotype. Other specimen at C (C-A-

92174) from the same collection � Isolectotype.

Type locality. Sargasso Sea [as ‘Sargasso-Sea’ in

Børgesen, 1914b, p. 11] (Silva, Basson, & Moe, 1996:

673).

Synonymy. Sargassum hystrix var. fluitans Børgesen

1914b, p. 11; Fucus baccifer var. oblongifolius Turner

1807 pp. 103�106.


LAF06929.

Morphology. Plants pelagic, without a holdfast or a dis-

tinct main axis. Branches smooth or with few spiny pro-

jections, terete or sometimes compressed, 1�1.8 mm

diam., ramified several times. Leaves simple, flat, lanceo-

late or linear, 20�50 (�60) mm long and 3�8 mm wide;

serrate margins, symmetrical or asymmetrical bases, acute

apices and percurrent midrib. Vesicles 10�55 per short

branch; elliptical or spherical, reaching up to 6 mm long

and 5 mm diam., usually smooth; stipe of vesicles up to

8 mm long, terete (some with spines), or compressed.

Cryptostomata and receptacles not observed.

Distribution. Colombia: San Andres and Providence

Islands. Western Atlantic: Massachusetts, North Carolina,

Bermuda, Gulf of Mexico (Mexico, Texas, Louisiana,

Mississippi, Alabama, Florida), Florida, Bahamas,

Greater Antilles (Cuba, Hispaniola, Jamaica), Lesser

Antilles (Virgin Islands, Guadeloupe), Western Caribbean

(British Honduras, Costa Rica, Mexico), and Southern

Caribbean (Panama).

Habitat. Pelagic. It is one of the species of the Sargasso

Sea (Børgesen, 1914b).

Notes. In the present study, this taxon was less frequently

found than S. natans, the other floating species found in

the Sargasso Sea. Both S. natans and S. fluitans have

never been observed in the drift around the Santa Marta-

TNNP area.

Sargassum hystrix J. Agardh 1847

(Figs 18�19)

Figs 16�17. Sargassum fluitans. (16) Thallus habit. (21) Branch with leaves and vesicles. Scales bars represent: Fig. 16, 5 cm; Fig. 21,1 cm.


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Type specimen. Agardh Herbarium no. C AT1353

(LD) � Lectotype (designated from a Liebmann collection

by Mattio et al. 2010: 6).

Type locality. Campeche Bank, Mexico [as ‘Campeche

bankarne’ J. Agardh 1847 p. 7].

Synonym. Carpacanthus spinulosus K€utzing 1861, p. 15.

Representative material. LAF04131, LAF04292, D-P

550, D-P 556, D-P 608, D-P 421.

Morphology. Plants up to 30 cm high, olive green-

brown. Holdfast discoid up to 10 mm diam. Main axis up

to 10 mm high and 2 mm diam. Primary branches smooth,

terete or compressed, up to 1.2 mm in diam., with alter-

nate secondary branches. Leaves simple, flat, oblong-

elliptical to lanceolate, 15�35 mm long and 4�8 mm

wide; serrate margins, asymmetrical bases, obtuse to acute

apices and percurrent midrib; stipe up to 2 mm long.

Vesicles 65�400 per thallus, spherical, reaching up 3

(�4) mm diam.; stipe up to 3 mm, terete, compressed, or

alated with 1 or 2 spine-projections. Cryptostomata spher-

ical, central pore 50�75 m diam.; numerous and scattered

over the surface of leaves.

Plants monoecious (androgynous). Receptacles axillary

from leaves or vesicles, forming loose clusters up to

20 mm long. Receptacles terete or some compressed

mostly at the tips, often with spine-like protuberances,

simple or branched mostly at the base, wart-like surface

and up to 12 mm long and 1.2 mm wide.

Distribution. Colombia: Oceanic atolls (Cays: Serrana,

Roncador, Courtown), Western Atlantic: Bermuda, Gulf

of Mexico (Geyer Bank, Campeche Banks), Florida,

Bahamas, Greater Antilles (Cuba, Puerto Rico, Jamaica),

Lesser Antilles (Virgin Islands, Guadeloupe, Granada,

Trinidad), Western Caribbean (Mexico, Costa Rica), and

southern Caribbean (Panama, Venezuela) and Brazil.

Habitat. On rocky substrata and coral reefs, more fre-

quently found below 10 m depth. Found in both protected

and moderately exposed habitats.

Notes. Specimens of this morphotype were found at

36 m depth in Geyer Bank (Gulf of Mexico) and from 9

to 19.5 m depth in the oceanic atolls of Colombia.

Taylor (1960) included a report of S. hystrix from a

depth of 57 m and referred to this species as a potential

deep-water taxon. Littler and Littler (2000) also men-

tioned this species in deep-water habitats up to 137 m

deep. In the present study, receptacles with spine-pro-

jections (a diagnostic character of this species, Agardh,

1847) were observed only in the Geyer Bank specimens.

Agardh’s original description also defined the recep-

tacles as forming dense axillary groups; however, the

specimens collected, and observed from different herba-

ria, are arranged in loose axillary clusters. The presence

of spines on the receptacles has generally not been

described in previous descriptions of S. hystrix from the

tropical western Atlantic (e.g. Dawes & Mathieson,

2008; Earle, 1969; Little & Littler, 2000) except in

Taylor (1960). See also comments about this character

in Børgesen (1914a, 1914b).

Sargassum natans (Linnaeus) Gaillon 1828

(Figs 20�21)

Figs 18�19. Sargassum hystrix. (18) Fertile herbarium specimen LAF04131. (19) Receptacle with spine-like protuberances andextruded oogonia. Scales bars represent: Fig. 18, 5 cm; Fig. 19, 1 mm.


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Type specimen. Linnaean Herbarium no. 1274.35

(LINN) � Lectotype (designated by Børgesen, 1914b: 7).

Type locality. ‘Indica’ (probably Jamaica) (Silva et al.,

1996: 687).

Synonym. Fucus natans Linnaeus 1753, p. 1160; Bacca-

laria natans (Linnaeus) S.F. Gray 1821, p. 393; Fucus

sargasso S.G. Gmelin 1768 pp. 92�96; Fucus baccifer

Turner 1802 pp. 55�60; Sargassum bacciferum (Turner)

C.Agardh 1820 pp. 6�7; Baccalaria teres S.F. Gray

1821, p. 393.


LAF06437, LAF06919.

Morphology. Plants pelagic, without a holdfast or a dis-

tinct main axis. Branches smooth, terete or sometimes

compressed, 1�1.5 mm diam., ramified several times.

Leaves simple, flat, linear, 20�80 (�100) mm long and

1�4 mm wide, serrate margins, symmetrical bases, acute

apices and percurrent midrib. Vesicles 25�80 per short

branch; elliptical or spherical, reaching up to 6 mm long

and 5 mm diam., often with an apical spine-like projection

up to 10 mm long, some with a reduced apical leaf; stipe

up to 8 mm long, terete (some with spines), few com-

pressed. Cryptostomata and receptacles not observed.

Distribution. Colombia: Bolivar (Cartagena), San

Andres and Providence Islands. Western Atlantic: Canada

(Newfoundland), Massachusetts, North Carolina, Ber-

muda, Gulf of Mexico (Mexico, Texas, Louisiana,

Alabama), Florida, Bahamas, Caicos Is., Greater Antilles

(Cuba, Hispaniola, Jamaica), Lesser Antilles (Guade-

loupe, Barbados, Granada), Western Caribbean (British

Honduras), Southern Caribbean (Colombia, Panama) and

Brazil.

Habitat. Pelagic. It is one of the species present in the

Sargasso Sea (Børgesen, 1914b).

Notes. This species was found as drift and in the beach

wash, sometimes in large masses in different areas of the

Caribbean (e.g. San Andres Island) and Gulf of Mexico

(e.g. Galveston, Texas; Holly Beach and Isle Derni�eres,Louisiana). Refer to Silva et al. (1996) for details on the

complex taxonomic and nomenclatural history of this

species.

Sargassum polyceratiumMontagne (1837)

(Figs 22�24)

Type specimens. Montagne Herbarium at PC

(PC0045052, MA 9217) collected by M.R. de la Sagra in

1936, La Habana, Cuba (may represent the Lectotype).

NY no. 00922444 collected by M.R. de la Sagra in 1936,

La Habana, Cuba � Isotype.

Type locality. La Habana, Cuba, Atlantic Ocean [as ‘In

portu La Havane’ in Montagne 1837 p. 356].

Synonymy. Carpacanthus polyceratius (Montagne)

K€utzing, 1849.

Figs 20�21. Sargassum natans. (20) Thallus habit. (21) Branch with leaves and vesicles. Scales bars represent: Fig. 16, 5 cm; Fig. 21,2 cm.


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Representative material. LAF04105, LAF04291, BM-

15, BM-39, BM-61, BM-85, BM-172, D-P 344, D-P 383,

D-P 445, D-P 578.

Morphology. Plants up to 80 cm high, tough and dense

in appearance, olive green in colour, often with brown

and white stains or veins on leaves. Holdfast conical or

discoidal up to 30 mm diam. Main axis 4.2�12 mm high

and 1.7�5 mm diam. Primary branches terete or

compressed, 1.3�2.2 mm largest diam., with alternate

secondary and sometimes short tertiary branches; often

with spine-like protuberances which are more abundant

in apical parts. Leaves simple, crisped or undulate, thick,

ovate or lanceolate, 15�35 (�40) mm long and (3�)

4�10 mm wide; serrate margins, asymmetrical and re-

curved bases, obtuse to rounded apices and percurrent

midrib; short stipe or absent with none to a few spines.

Vesicles spherical or elliptical, (0�) 50�600 along the

thallus, 3.3�5.6 (�6.4) mm long and 3�5.2 mm diam.,

some with an apical spine-like mucro or small leaf; stipe

0.8�3.5 (�5) mm long, terete (some with spines), com-

pressed or alated. Cryptostomata elliptical or spherical,

central pore (40�) 67�167 (�200) mm long and (40�)

67�134 mm wide, numerous and scattered on leaves,

stipes and vesicles.

Plants dioecious or monoecious (androgynous). Recep-

tacles terete, dichotomously branched disposed in stipitate

clusters on secondary or tertiary branches, some in

racemes with differentiated sterile axis, up to 20 mm

long; female receptacles with prominent wart-like surface

up to 7 (�10) mm long and 0.8 mm wide; male recep-

tacles with wart-like surface up to 10 mm long and

0.6 mm diam.; androgynous receptacles with prominent

wart-like surface up to 5 mm long and 0.7 mm diam.,

without stipe.

Distribution. Colombia: Magdalena (TNNP: Neguanje,

Cinto, Cabo San Juan de Gu�ıa and Arrecifes), Bolivar

(Islas del Rosario), Providence Island (Cayo Cangrejo),

Choco (Sapzurro), Oceanic atolls (Cays: Albuquerque,

Courtown, Serrana). Panama: Big Plantain Cay. Western

Atlantic: Bermuda, Gulf of Mexico (Mexico), Florida,

Bahamas, Caicos Is., Greater Antilles (Cuba, Islas Cay-

man, Jamaica, Hispaniola, Puerto Rico), Lesser Antilles

(Virgin Islands, Guadeloupe, St. Lucia, Barbados, Cura-

cao, Venezuela), Western Caribbean (Mexico), Southern

Caribbean (Colombia, Panama) and Brazil.

Habitat. Frequent on rocky substrata and coral reefs in

intertidal and subtidal zones to 4 m depth. Found in both

protected and exposed habitats.

Notes. Specimens from sheltered localities inside

Neguanje and Cinto bays resemble those of S. polycera-

tium var. ovatum (Collins) W.R. Taylor. Specimens found

in other localities without crisped leaves, narrower

Figs 22�24. Sargassum polyceratium. (22) Habit of fertile thallus. (23) Spine-like protuberances on tertiary branches. (24) Tertiarybranch with receptacles, vesicles and undulate leaves. Scales bars represent: Fig. 20, 5 cm; Fig. 21, 4 mm; Fig. 22, 1 cm.


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(3�5 mm wide) than in S. polyceratium, with few or lack-

ing spines-like protuberances and without a dense thallus

appearance, may resemble S. vulgare C. Agardh. How-

ever, we found it very difficult to distinguish S. vulgare

from S. polyceratium in Colombia. Kilar and Hanisak

(1988, 1989) found 47 different morphotypes, and signifi-

cant seasonal variability in blade morphology in S. poly-

ceratium from the Content Keys in Florida. Although S.

vulgare was reported by Schnetter (1976) in Guajira

(north coast of the Caribbean Colombia), as well as for

other areas in the western Atlantic (Wynne, 2011), the

presence of this taxon in the western Atlantic needs to be

re-considered in the light of an accepted type. The neo-

type proposed by Ramon and Gil-Ad (2007) from the

Mediterranean Sea was rejected by the Committee on

Algae (Prud’homme van Reine, 2011).

Sargassum stenophyllumMartius (1828)

(Figs 25�27)

Type specimen. Types not seen.

Type locality. Sa~o Paulo, Brazil, Atlantic Ocean [as

‘Crescit in Oceano atlantico ad oras Provinciarum

Bahiensis, Sebastianopolitanae et S. Pauli’ in Martius

1828, p. 8].

Synonymy. Sargassum cymosum var. stenophyllum

(Martius) Grunow 1916, p. 138.

Representative material. LAF06611, LAF06654, BM-

62, BM-48.

Morphology. Plants up to 1 m high, olive green-brown.

Holdfast conical or discoidal, 5.2�9.3 mm diam. Main

axis up to 7.3 mm high and 2.8 mm in diam. Primary

branches smooth, terete, 1�1.7 mm in diam. with second-

ary and rarely tertiary branches. Leaves simple, linear, flat

in lateral view, thick, 25�50 (�80) mm long and

0.6�1.5 mm wide (some up to 3 mm wide in proximal

parts); smooth margins, symmetrical bases, acute

apices and not often percurrent midrib. Vesicles abundant,

200�3200 per thallus, elliptical, 2.1�4.5 (�5.6) mm long

and 1.4�3.3 (�3.8) mm diam., often with an apical spine-

like expansion of 1�3 (�8) mm long; stipe terete,

1.5�5 mm long and to 1 mm diam. Cryptostomata scarce

or absent, small, mostly elliptical, central pore 50�130 mmlong and 33�100 mm wide; on leaves disposed in one row

on each side of the midrib or next to the margin.

Plants dioecious. Receptacles on secondary or tertiary

branches forming dense racemes up to 10 mm long, sessile

or arising from a short stipe. Receptacles terete, 2�3 times

dichotomously branched with wart-like surface; male

Figs 25�27. Sargassum stenophyllum. (25) Fertile herbarium specimen LAF06611. (26) Non-fertile branch. (27) Apical part of a branchwith leaves and small vesicles. Scales bars represent: Fig. 25, 5 cm; Fig. 26, 1 cm; Fig. 27, 2 cm.


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receptacles 2�5 mm long and 0.4�0.6 mm wide; female

receptacles more densely arranged and to 4 mm long.

Distribution. Colombia: Magdalena (TNNP: Concha).

Western Atlantic: Venezuela, Brazil.

Habitat. On rocky substratum in the intertidal to 2 m

depth, occurring in a wave exposed habitat.

Notes. The specimens studied here were morphologically

similar to those described from Brazil by Paula (1998),

although the leaves from the Colombian material were not

as distant from each other and the vesicles were smaller.

Sargassum giganteum Camacho & Diaz-Pulido sp. nov.

(Figs 28�31)

Holotype. CBUMAG:ALG:00529

Collecting permit No. DTC-T-30 10/07 and DTCA-Ty036

02/05 by Colombian National Natural Park System

Administrative Unit.

Isotype. LAF04289.

Type locality. Granate Bay, Tayrona (Tayrona National

Natural Park), Caribbean Colombia.

Etymology. This species is named for its exceptionally

large size.

Representative material. LAF04289, LAF06605, LAF06607.

Description. Plants up to 5 m high, loose in appearance,

light brown. Holdfast discoid up to 2.5 mm in diam. Main

axis (1.3) �4.5�8.5 (�10.3) mm high and 1.5�3 mm

diam. Branches smooth, terete in proximal parts and com-

pressed in distal parts, 0.9�2.8 mm diam. Primary and

secondary branches sparsely alternately branched. Leaves

simple or forked up to 4 times, flat or undulate, thin, lan-

ceolate or linear, (20�) 30�50 (�60) mm long and

(1�)�2�4 (�6) mm wide; margins deeply and irregular

serrate, asymmetrical or symmetrical bases, acute apices

and percurrent midrib more evident in proximal leaves;

stipe up to 3 mm long, sometimes with few spine-like pro-

tuberances. Vesicles (63�) 130�620 (�920) per thallus;

spherical, 3�9 mm long and 3�9.4 diam.; stipe 3�8 mm

long and to 1 mm wide, terete and smooth. Cryptostomata

elliptical or spherical, central pore of 83�250 m long and

83�133 m wide, dark in colour contrasting with the pale

tonality of the entire plant; numerous and scattered over

the surface of leaves, branches, vesicles and stipes, raised

particularly in distal parts of the plant.

Plants dioecious. Receptacles axillary from leaves or

vesicles on tertiary branches forming loose racemes up to

35 mm long with a well-differentiated sterile central axis;

racemes have alternated, distanced, simple to 4 times

dichotomously branched receptacles, on stipes 1�2 mm

long, not mixed with leaves or vesicles. Female recep-

tacles terete with wartlike surface, 5�10 mm long and

0.6�1.2 mm wide; male receptacles terete, with bumpy

surface, 5�15 mm long and 0.4�0.8 mm wide.

Distribution. Colombia: This morphotype has been

observed only from the TNNP (Granate, Concha, and

Gayraca bays).

Habitat. On rocky substratum in the subtidal zone

between 2 and 8 (�12) m depth. Prefers protected small

bays where wave and current exposure is moderate. The

most conspicuous populations are found in Granate and

Concha bays during April to May when it forms dense

fringed beds of >1 km long and 8 m high. Branches of

mature individuals of up to 5 m tall detach from the sub-

strate and entangle together with other individuals form-

ing underwater forests of up to 8 m high.

Notes. The frequency of simple or forked leaves varied

between plants. Most thalli displayed simple leaves, some

showed both simple and forked leaves, while some other

plants had only forked leaves. After a rigorous analysis

made on this morpho-species, we could not assign it to

any of the morphological species previously reported for

the western Atlantic or other regions. Sargassum gigan-

teum sp. nov. resembles S. filipendula in some aspects;

however, S. giganteum sp. nov. can be distinguished by:

(1) leaves with margins more deeply and irregularly ser-

rate; (2) vesicles less numerous, bigger and without

spines-like or leaf-like protuberances; (3) receptacles in

racemes with a well-differentiated sterile axis bearing

spaced receptacles, without leaves and vesicles; (4) cryp-

tostomata are bigger, very conspicuous and raised particu-

larly in distal parts of the plant; and (5) S. giganteum

thalli are much taller and have a laxer aspect than S. fili-

pendula. Additionally, none of the varieties and forms of

S. filipendula previously reported for the western Atlantic

(Bertossi & Ganesan, 1973; Dawes & Mathieson, 2008;

Earle, 1969; Guiry & Guiry, 2014; Hanisak & Kilar,

1990; Moreira & Su�arez, 2002; Paula, 1988; Schnetter,1976; Taylor, 1960) appeared morphologically similar to

S. giganteum sp. nov. One specimen from W.R. Taylor’s

collection (MICH 39�248) identified as S. filipendula,

and collected as drift in Cienaga (Magdalena, Colombia)

in 1939, looks identical to S. giganteum sp. nov.; however,

the MICH specimen lacks the basal parts of the thallus.

Sargassum pteropleuron Grunow, reported to reach 4 m

tall in the Caribbean (Dawes & Mathieson, 2008; Littler

& Littler, 2000), was considered as a potential name

because of its size. However, detailed morphological anal-

ysis and molecular results from this study provided


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Figs 28�31. Sargassum giganteum sp. nov. (28) Holotype: Fertile herbarium specimen, CBUMAG:ALG:00529. (29) Branched femalereceptacle with extruded oogonia on a sterile stipe. (30) Fertile branch with leaves and axillary receptacles. (31) Secondary branch of afertile specimen. Scales bars represent: Fig. 28, 20 cm; Fig. 29, 1 mm; Fig. 30, 1 cm; Fig. 31, 2 cm].


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enough evidence to confirm it is not the case. Sargassum

giganteum sp. nov. was recognized and cited as Sargas-

sum sp. in Camacho and Hern�andez-Carmona (2012).

Key for the identification of Sargassum spe-

cies from the Caribbean Colombia and other

western tropical Atlantic areas

A key is provided for the identification of all 10 Sargas-

sum morpho-species reported in this study for the Colom-

bian Caribbean, as well as for other areas in the western

tropical Atlantic. The key was built based on rigorous

morphological examination of newly collected samples,

and extensive herbarium and type specimens.

1a. Plants floating, without holdfast; cryptostomata and

receptacles absent .............................................................2

1b. Plants attached by a solid or a rhizomatous holdfast;

cryptostomata and receptacles present..............................3

2a. Leaves linear, 1�4 mm wide; vesicles with an api-

cal spine-like projection or a reduced leaf ........... S. natans

2b. Leaves lanceolate, 3�8 mm wide; vesicles usually

smooth................................................................. S. fluitans

3a. Plants attached by rhizomatous holdfast, vesicles

absent .............................................................. S. schnetteri

3b. Plants attached by discoid or conical holdfast,

vesicles present .................................................................4

4a. Spine-like protuberances often present on

branches ............................................................................5

4b. Spine-like protuberances absent on branches .........6

5a. Leaves crisped or undulate, ovate or lanceolate,

15�35 mm long and 4�10 mm wide; spine-like protuber-

ances more abundant in apical parts ..........S. polyceratium

5b. Leaves flat, linear, 25�100 mm long and 2�4 (�6)

mm wide; spine-like protuberances more abundant in

proximal parts ............................................S. pteropleuron

6a. Leaves oblong or lanceolate, few linear..................7

6b. Leaves linear or lanceolate .....................................8

7a. Plants to 70 (�100) m tall, common in the intertidal

to 2 m; leaves oblong-lanceolate few linear, 2�4 (�6)

mm wide, with smooth, crenulate or rarely serrated

margins.............................................................S. cymosum

7b. Plants to 30 cm tall, common in deep waters (to

36 m depth); leaves oblong-elliptical to lanceolate,

4�10 mm wide, serrate margin ...........................S. hystrix

8a. Leaves with smooth margin, cryptostomata scarce

or absent. Receptacles to 5 mm long forming dense race-

mes to 10 mm long.....................................S. stenophyllum

8b. Leaves with serrate margins, cryptostomata abun-

dant. Receptacles to 5 mm long forming loose racemes to

30 or more mm long..........................................................9

9a. Leaves (30�) 40�90 (�100) mm long and 3�7 mm

wide, flat, with serrate margin. Vesicles to 4 mm diam.,

often with an apical spine-like protuberance. Thalli to 1 m

tall ..................................................................S. filipendula

9b. Leaves (20�) 30�50 (�60) mm long and (1�) 2�4

(�6) mm wide, flat or undulate, with deeply and irregular

serrate margins. Vesicles to 9.4 mm diam. Thalli to 5 m

tall .....................................................S. giganteum sp. nov.

DiscussionIn the present study we assessed the molecular identity

and morphological comparison of the monotypic genus

Cladophyllum and nine Sargassum morphotypes from the

western tropical Atlantic with a focus on representatives

found in Caribbean Colombia, especially along the coast

of Santa Marta-TNNP. Our phylogenetic analysis grouped

all the sequences newly obtained into two well-supported

clades within the S. subgenus Sargassum. The majority

(eight) of the identified morphotypes grouped into a

polytomy in S. section Sargassum clade, while a second

group contained only sequences of C. schnetteri and S.

pteropleuron.

Based on the molecular results of the present study, we

propose to: (1) subsume Cladophyllum into Sargassum,

and thus rename its single species as Sargassum schnetteri

(Bula-Meyer) Camacho, Mattio & Diaz-Pulido comb.

nov., and (2) describe a new section within S. subgenus

Sargassum, i.e. S. section Cladophyllum (Bula-Meyer)

Camacho, Mattio & Diaz-Pulido, to house the species S.

schnetteri and its closest relative from Atlantic, S. ptero-

pleuron (see the Taxonomy section).

Both molecular and morphological analyses demon-

strated the nesting of C. schnetteri within Sargassum.

This species was originally described based exclusively

on morphological characters (Bula-Meyer, 1980), and rec-

ognized mainly by its rhizomatous holdfast (instead of a

discoid or conical holdfast as in the other Sargassum mor-

photypes in the region), the absence of vesicles and the

shape of its leaves. Our molecular results clearly demon-

strate that these characters do not warrant generic level

and that Cladophyllum should instead be considered a

Sargassum species within subgenus Sargassum. Bula-

Meyer (1980) himself had discussed the considerable

morphological affinity between these two genera. For

example, other species classified in S. subgenus Sargas-

sum exhibit a basal part formed by a mix of holdfast and

rhizoidal branches (stolon-like), with the latter issued

from the upper part of the main axis (e.g. S. herporhizum

Setchell & N.L. Gardner, S. brandegeei Setchell & N.L.

Gardner, S. polycystum C. Agardh). Two distinct new sec-

tions have recently been proposed to accommodate spe-

cies showing this trait: S. sect. Polycystae (Mattio et al.,

2009) and S. sect. Herporhizum (Norris, 2010). Sargassum

stolonifolium S.M. Phang & T. Yoshida was described as

having a holdfast and rhizoidal stolon-like branches, the

latter issued from cauline leaves on the lower part of the

axis (Phang & Yoshida, 1997). Other types of basal


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structures have been reported in S. subgenus Sargassum,

such as those observed in S. rhizophorum Tseng & Lu, S.

integerrimum Tseng & Lu, S. symphyorhizoideum Tseng

& Lu and S. yinggehaiense Tseng & Lu with rhizoids fus-

ing with one another (Tseng & Baoren, 2002), or S. cornu-

tifructum H.D. Nguyen & Q.N. Huynh with attachment

via small discoid haptera with many filamentous rhizoids

(Dinh & Nang, 1999). Other examples have been reported

in S. subgenus Bactrophycus where the base also consists

of a holdfast and rhizoidal outgrowths, e.g. S. hemiphyl-

lum (Turner) C.Agardh, S. ammophilum Yoshida & T.

Konno, S. nipponicum Yendo and S. miyabei Yendo

(Tseng et al., 1985). None of these structures resemble the

basal part observed in Cladophyllum.

Interestingly, the present study also revealed C. schnet-

teri as a sister species to S. pteropleuron, together forming

the sixth section of subgenus Sargassum that is supported

molecularly. Intra-sectional genetic distances calculated

in this study suggested that these two highly morphologi-

cally distinct taxa belong to the same section (Fig. 1).

Unlike C. schnetteri, S. pteropleuron exhibits a discoid

holdfast, presence of vesicles, spine-like protuberances on

the branches, and serrate leaves with an elevated midrib.

Other molecularly recognized sections in S. subgenus Sar-

gassum (e.g. S. sect. Binderiana, S. sect. Ilicifolia, Mattio

et al., 2010) also contain morphologically well distinct

taxa, but none appear to be as morphologically distinct as

the section including C. schnetteri and S. pteropleuron

(S. section Cladophyllum).

Besides the morphological distinction observed in

these two species, S. section Cladophyllum represents

the first identified section to occur only in the western

Atlantic. Intriguingly, Sargassum pteropleuron is a spe-

cies broadly distributed in the Caribbean (Dawes &

Mathieson, 2008; Earle, 1969; Littler & Littler, 2000;

Moreira & Cabrera, 2007; Taylor, 1960), with no reports

yet for Colombia, while C. schnetteri is endemic to a

short coastal area in TNNP. As more sequences from

various regions around the world are included in a

global Sargassum’s phylogeny, additional sections may

be identified or confirmed, together providing further

insights into the evolution of Sargassum. For instance,

the relationships of four endemic sections described by

Norris (2010) for the Gulf of California with the other

sections in S. subgenus Sargassum still remains to be

assessed molecularly.

The other eight Colombian and western tropical Atlan-

tic morphospecies identified in the present study belong to

the polytomic and widely distributed (worldwide) S. sec-

tion Sargassum clade, providing limited molecular differ-

entiation between them. The low molecular diversity

observed between morphological species of this section

has been previously recorded and interpreted as possible

sign of a recent and rapid diversification (Mattio et al.,

2008). Low genetic diversity was also reported between

species of S. subgenus Bactrophycus section Halochloa

(Cho, Lee, Ko, Mattio, & Boo, 2012; Dixon et al., 2014)

and within the fucalean genus Fucus (Bergstr€om, Tataren-

kov, Johannesson, Jonsson, & Kautsky, 2005; Coyer

et al., 2006; Leclerc, Barriel, Lecointre, & Reviers, 1998;

Serr~ao, Alice, & Brawley, 1999). For instance, Pereyra,

Bergstr€om, Kautsky, and Johannesson (2009), relying on

microsatellite markers, hypothesized that the evolution of

the Baltic Sea endemic Fucus radicans L. Bergstr€om & L.

Kautsky may have occurred in the last 400 years, while

based on a molecular clock, Canovas, Mota, Serr~ao, andPearson (2011) estimated that Fucus radiated only about

2.5 Mya ago. In the present study, besides the analysis of

ITS-2, rbcLS and cox3, we assessed the variability of a

mitochondrial spacer region (mtsp); however, it did not

allow for a better molecular resolution at the species level

in S. section Sargassum. Considering the low molecular

divergence among S. section Sargassum species, and

whether or not a suitable molecular marker will be uncov-

ered to molecularly confirm the species in this section, we

view the morphological variability observed in the present

study to be evidence of species-level boundaries. At pres-

ent we recognize eight Sargassum morphospecies for the

Caribbean coast of Colombia, one of those considered

new and here described as Sargassum giganteum sp. nov.

(see the Taxonomy section).

All of the S. section Sargassum species documented in

the present study are relatively widely distributed and

have been recorded for other localities in the western

Atlantic (Dawes & Mathieson, 2008; Earle, 1969; Gane-

san, 1989; Guiry & Guiry, 2014; Menezes-Sz�echy &

Paula, 2010; Moreira & Cabrera, 2007; Paula, 1988; Tay-

lor, 1960; Wynne, 2011). Among them, the pelagic spe-

cies S. natans appears the most widely distributed,

reported from Newfoundland (Canada) throughout the

Caribbean and Gulf of Mexico to Brazil. Considering the

benthic taxa, S. filipendula corresponds to the most

broadly dispersed species, reported from the coast of Vir-

ginia in North America (also through the Caribbean and

Gulf of Mexico) to Santa Catarina in Brazil. In contrast,

Sargassum giganteum sp. nov. and S. schnetteri appear to

be endemic to TNNP on the Caribbean coast of Colombia.

Endemism in Sargassum has seldom been recorded in the

literature but examples include S. turbinarioides Grunow

in New Caledonia (Mattio et al., 2009), S. cymosum f. bor-

bonicum in R�eunion (Mattio et al., 2013) and S. albemar-

lense W.R. Taylor in the Galapagos Islands (Taylor,

1945). The restricted distribution of S. schnetteri could be

explained by the absence of vesicles limiting long-dis-

persal of individuals since zygotes of Sargassum usually

settle about 1�2 m from the parental thallus (Deysher &

Norton, 1982; Kendrick & Walter, 1991). Because of its

narrow endemism and phylogenetic position, S. schnetteri

qualifies as a probable relict and may be, along with S.

pteropleuron, of great interest for understanding the


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evolution of the genus in the Atlantic. Extreme warming

events have been reported to extirpate marginal populations

of similar habitat-forming seaweeds, as is the case of Scy-

tothalia dorycarpa (Turner) Greville in western Australia

where its distribution was narrowed down by approxi-

mately 100 km following a marine heatwave (Smale &

Wernberg, 2013). Likewise, the endemic Bifurcaria gala-

pagensis (Piccone & Grunow) Womersley from the Gala-

pagos Islands is presumably extinct following the 1982 El

Ni~no event (Miller, Garske, & Edgar, 2007). Considering

the narrow endemism of S. schnetteri in the Caribbean

coast of Colombia, extreme climatic events could place the

S. schnetteri population in danger. We suggest this popula-

tion should be considered for detailed ecological study in

order to be properly assessed as a potential vulnerable or

endangered species on the IUCN Red List.

AcknowledgementsWe acknowledge Claude Payri, Nathalie Duong and the

Plateforme du Vivant at IRD in Noum�ea for their help

and financial support in sequencing the Colombian

specimens, and to NSF (DEB-0315995, DEB-0937978),

GoMRI-I, and SGA-ULL (#DC319110-G8530-2650U)

for financial support in collecting and processing addi-

tional specimens from Panama, Florida and the Gulf of

Mexico. We thank Dr Patrik Fr€od�en, curator of the

Agardh’s collection at LD in Lund (Sweden), Dr Bruno

de Reviers, curator of the Montagne’s collection at PC

in Paris (France), Dr Anton Igersheim curator of

Grunow’s collection at W in Wien (Austria), Dr Mark

Spencer, curator of the Linnean collection at LINN in

London (England) and Dr Nina Lundholm, curator of

Børgesen’s collection at C in Copenhagen (Denmark)

for scans of type herbaria material. We are also grateful

to Dr Michael Wynne, Thomas Sauvage and two anony-

mous reviewers for their valuable criticism of the manu-

script, to William Schmidt for his help with the

molecular analyses, and to Carlos Alberto Trujillo for

assistance in field collections.

Supplemental dataSupplemental data for this article can be accessed here.

Appendix 1. Close up of Sargassum section Sargassum cladetaken from the Maximum likelihood (RAxML) tree of the com-bined ITS-2, rbcLS and cox3. Values at the nodes indicate Boot-strap support (left) and Posterior Probability (right); valuesbelow 50 are not shown or represented by ‘�’. Area abbrevia-tions: C, Colombia; FP, French Polynesia; GoMX, Gulf of Mex-ico; IT, Italy; MAUR, Mauritius; NC, New Caledonia; NCar,North Carolina; NZ, New Zealand; PanCar, Panama; PR, PuertoRico; TZ, Tanzania.

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