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Systematics and Biodiversity
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Morphological and molecular assessment of Sargassum
(Fucales, Phaeophyceae) from Caribbean Colombia,
including the proposal of Sargassum giganteum sp.
nov. , Sargassum schnetteri comb. nov. and Sargassum
section Cladophyllum sect. nov.
ab
c
d
a
Olga Camacho , Lydiane Mat t io , St ef ano Draisma , Suzanne Fredericq & Guillermo DiazPulido
a
e
Depart ment of Biology, Universit y of Louisiana at Laf ayet t e, LA 70504–2451, USA
b
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Programa de Biología Marina, Universidad de Bogot á Jorge Tadeo Lozano, Carrera 4 #
22–61, Bogot á, Colombia
c
Depart ment of Biological Sciences and Marine Research Inst it ut e, Universit y of Cape Town,
7701 Rondebosch, Sout h Af rica
d
Inst it ut e of Ocean & Eart h Sciences, Universit y of Malaya, 50600, Kuala Lumpur, Malaysia
e
Grif f it h School of Environment , Aust ralian Rivers Inst it ut e – Coast & Est uaries, and ARC
Cent re of Excellence f or Coral Reef St udies, Nat han Campus, Grif f it h Universit y, 170 Kessels
Road, Brisbane, Nat han, Qld 4111, Aust ralia
Published online: 01 Dec 2014.
To cite this article: Olga Camacho, Lydiane Mat t io, St ef ano Draisma, Suzanne Fredericq & Guillermo Diaz-Pulido (2014):
Morphological and molecular assessment of Sargassum (Fucales, Phaeophyceae) f rom Caribbean Colombia, including t he
proposal of Sargassum gigant eum sp. nov. , Sargassum schnet t eri comb. nov. and Sargassum sect ion Cladophyllum sect . nov. ,
Syst emat ics and Biodiversit y, DOI: 10. 1080/ 14772000. 2014. 972478
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Systematics and Biodiversity (2014), 1 26
Research Article
Downloaded by [Univ of Louisiana at Lafayette] at 07:59 12 January 2015
Morphological and molecular assessment of Sargassum (Fucales,
Phaeophyceae) from Caribbean Colombia, including the proposal of
Sargassum giganteum sp. nov., Sargassum schnetteri comb. nov. and
Sargassum section Cladophyllum sect. nov.
OLGA CAMACHO1,2, LYDIANE MATTIO3, STEFANO DRAISMA4, SUZANNE FREDERICQ1 & GUILLERMO
DIAZ-PULIDO5
1
Department of Biology, University of Louisiana at Lafayette, LA 70504 2451, USA
Programa de Biologıa Marina, Universidad de Bogota Jorge Tadeo Lozano, Carrera 4 # 22 61, Bogota, Colombia
3
Department of Biological Sciences and Marine Research Institute, University of Cape Town, 7701 Rondebosch, South Africa
4
Institute of Ocean & Earth Sciences, University of Malaya, 50600, Kuala Lumpur, Malaysia
5
Griffith 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
2
(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 the
large variability of morphological traits among and within taxa. To date, most molecular studies of this group have focused
on the central Indo-Pacific region, even though the genus is also well represented in the Atlantic Ocean. In the present
study, we re-assessed the diversity and taxonomy of Sargassum and the monospecific genus Cladophyllum from Caribbean
Colombia (especially from the Santa Marta-Tayrona National Natural Park) and extended to the western tropical Atlantic
towards 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 revealed
its nesting inside Sargassum subgenus Sargassum as a close relative of S. pteropleuron, a broadly distributed species in the
Caribbean. Analysis of molecular divergence in this newly identified clade demonstrated a similar range of variation as that
present 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 within
the worldwide-distributed S. section Sargassum, thus providing no support for the other eight morphological species
currently recognized in the Caribbean Colombia and other western tropical Atlantic areas. Based on the morphological
analysis we further described a new species, S. giganteum Camacho & Diaz-Pulido sp. nov., endemic from TNNP. Detailed
morphological 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
Introduction
The 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 recognized species (Guiry & Guiry, 2014). The classification
system proposed by J. Agardh (1848, 1889) initially
Correspondence to: Olga Camacho. E-mail: olgacamacho76@
yahoo.com
ISSN 1477-2000 print / 1478-0933 online
Ó The Trustees of the Natural History Museum, London 2014. All Rights Reserved.
http://dx.doi.org/10.1080/14772000.2014.972478
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).
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2
O. Camacho et al.
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 classification led to revisions and subsequent division of the genus
into two subgenera and nine sections with the abandonment 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 taxonomic 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 Sargassaceae form large seasonal beds along rocky shores, particularly along the coast of Colombia (e.g. Santa Marta
and Tayrona National Natural Park [TNNP]), Venezuela
and Curaçao (Camacho & Hernandez-Carmona, 2012;
Dıaz-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 endangered 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. Similarly, 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 environmental 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 species 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 previously 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 morphological 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 Carolina, and Puerto Rico. Samples were collected by scuba diving 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 11 210 N and
74 030 74 200 W), seasonal collection efforts for morphological 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, collected 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).
Morphological and molecular assessment of Sargassum
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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 specimens (scans) from the collection of Agardh at LD (Lund,
Sweden), Børgesen at C (Copenhagen, Denmark), Grunow at W (Vienna, Austria), Linnaeus at LINN (London,
UK), and Montagne at PC (Paris, France) were also compared. 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 following the widely accepted terminology in Sargassum.
To analyse the shape and size of the cryptostomata, specimens were observed under a dissecting microscope.
Hand-made cross-sections of receptacles were observed
under a light microscope to determine their sex. Morphological 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 following 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
utzing (1849, 1861), Martius (1833), Montagne
(1957), K€
(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 Developpement) in Noumea, New Caledonia, and
at the Seaweeds Lab at the University of Louisiana at
Lafayette, USA. Silica gel-dried material (Table 1) was
3
ground in liquid nitrogen and total DNA extracted using
the DNeasy Plant mini Kit (Qiagen GmbH., Hilden, Germany). All extracts were purified using the Geneclean kit
III (Qbiogen Inc., Carlsbad, CA, USA) prior to PCR
amplification. DNA extraction from old herbarium specimens (e.g. BM, GD-P) was attempted using a modified
Dellaporta, Wood, and Hicks (1983) protocol described
by Hughey, Silva, and Hommersand (2001) without success, probably due to previous formalin fixation of the
material. We chose to amplify the nuclear Internal Transcribed 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 Sargassum 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 primers 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 mM
of forward and reverse primers, 0.2 mM of each dNTP,
1.5 mM of MgCl2, 5 mL of reaction buffer, 1 mL of purified 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 denaturation 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 extension step at 72 C for 7 min. PCR products were purified
and sequenced in both directions using the BigDyeTM terminator 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 consequence, 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
4
O. Camacho et al.
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Table 1. Taxa included in molecular analyses with the vaucher reference, collection sites, collectors, collection dates and GenBank
accessions. Accessions numbers in bold correspond to sequences newly obtained in this study.
Taxon name revised
Vaucher
number
Collection site; Collector;
Collection date
Sargassum schnetteri
LAF06612
Sargassum schnetteri
LAF04287A
Sargassum aquifolium
IRD1531
Sargassum aquifolium
IRD1681
Sargassum aquifolium
IRD1582
Sargassum aquifolium
IRD1660
Sargassum aquifolium
Sh01466
Sargassum carpophyllum
IRD1511
Sargassum cf. cymosum
LAF06602
Sargassum cf. cymosum
LAF06614
Sargassum cymosum
LAF04290
Sargassum cymosum
LAF06609
Sargassum cymosum
LAF06610
Sargassum cymosum
LAF06613
Sargassum filipendula
LAF04288
Sargassum filipendula
LAF04106
Sargassum filipendula
LAF04256
Sargassum filipendula
LAF04275
Sargassum fluitans
LAF04276
Sargassum fluitans
LAF06920
Sargassum giganteum
LAF06605
Colombia, Magdalena, Neguanje
(TNNP); O. Camacho; May
2009
Colombia, Magdalena, Neguanje
(TNNP); O. Camacho; Nov
2009
New Caledonia, Ile des Pins; L.
Mattio; Dec 2005
Vanuatu, Santo; L. Mattio; Aug
2006
Fiji, Navutulevu rf.; L. Mattio;
May 2007
Solomon, Malaita Is. ST850; C.
Payri; Jul 2004
Hawaiian Is., Ohau; T. Sauvage;
Oct 2006
New Caledonia, Feycinet Is.; L.
Mattio; Jul 2005
Colombia, Magdalena, Granate
(TNNP); O. Camacho; May
2009
Colombia, Magdalena, Playa
Blanca; O. Camacho; May
2009
Colombia, Magdalena, Granate
(TNNP); O. Camacho; Apr
2009
Colombia, Magdalena, Concha
(TNNP); O. Camacho; Apr
2009
Colombia, Magdalena, Concha
(TNNP); O. Camacho; Apr
2009
Colombia, Magdalena, Neguanje
(TNNP); O. Camacho; May
2009
Colombia, Magdalena, Punta La
Loma; O. Camacho; Apr 2009
Panama, Zapatilla Cay; O.
Camacho; Aug 2010
Panama, Bocas del Toro, Flat
Rock Beach; S. Fredericq;
Aug 2010
United States, North Carolina,
Masonboro; O, Camacho;
May 2011
United States, North Carolina,
Fort Fisher, drift; O,
Camacho; May 2011
United States, Gulf of Mexico,
Holly Beach; O. Camacho;
Jun 2014
Colombia, Magdalena, Granate
(TNNP); O. Camacho; Mar
2009
GenBank accessions
ITS-2
rbcLS
cox3
KF437949
KF437962
KF437931
KF437950
KF437963
KF437932
EU100800
EU100808
EU882243
EU833456
EU833476
EU833412
EU833432
EU833464
EU833406
EU833447
EU833462
EU833397
EU100796
EU100821
EU100835
EU100797
EU100804
EU833415
KF437935
KF437919
KF437944
KF437961
KF437928
KF437936
KF437953
KF437920
KF437939
KF437956
KF437923
KF437940
KF437957
KF437924
KF437943
KF437960
KF437927
KF437938
KF437955
KF437922
KM461671
KP064347
KP064332
KM461672
KP064348
KP064333
KM461673
KP064349
KP064334
KM461674
KP064350
KP064335
KM461675
KP064351
KP064336
KF437945
KF437929
(continued)
Morphological and molecular assessment of Sargassum
5
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Table 1. (Continued )
Taxon name revised
Vaucher
number
Collection site; Collector;
Collection date
Sargassum giganteum
LAF06607
Sargassum giganteum
LAF04289
Sargassum hystrix
LAF04292
Sargassum hystrix
LAF04131
Sargassum ilicifolium
IRD1589
Sargassum ilicifolium
IRD3931
Sargassum ilicifolium
GENT-TZ0852
Sargassum natans
LAF06919
Sargassum natans
LAF06437
Sargassum micracanthum
IRD5222
Sargassum obtusifolium
UPF2651
Sargassum pacificum
UPF2754
Sargassum polyceratium
LAF04291
Sargassum polyceratium
LAF04105
Sargassum polyceratium
LAF03947
Sargassum cf. polyceratium
LAF04185
Sargassum polycystum
ARV144
Sargassum polycystum
IRD1571
Sargassum polyphyllum
IRD1613
Sargassum portierianum
BOL44348
Sargassum pteropleuron
LAF06913
Sargassum pteropleuron
LAF06917
Colombia, Magdalena, Granate
(TNNP); O. Camacho; Apr
2009
Colombia, Magdalena, Granate
(TNNP); O. Camacho; Apr
2009
United States, Gulf of Mexico,
Geyer Bank; Emma
Hickerson; Sep 2011
United States, Gulf of Mexico,
Geyer Bank; Emma
Hickerson; Sep 2011
Fiji, Kiuva reef; L. Mattio, May
2007
New Caledonia, Crouy; L.
Mattio; Jun 2006
Tanzania, n.a.; H. Verbruggen;
Jan 2008
United States, Gulf of Mexico,
Holly Beach; O. Camacho;
Jun 2014
United States, Gulf of Mexico,
offshore LA, drift; O.
Camacho; Jun 2014
Japan, Mitohama, Misaki; F.
Mineur; Oct 2010
French polynesia, Rapa,
Australs; C. Payri; Nov 2002
French polynesia, Bora Bora; C.
Payri & V. Stiger; Mar 2003
Colombia, Magdalena, Neguanje
(TNNP); O. Camacho; May
2009
Panama, Big Plantain Cay; O.
Camacho; Aug 2010
Panama, East Rio Ca~
naveral; O.
Camacho; Aug 2010
Puerto Rico, Ponce, Caleta de
Cabullones; O. Camacho; Sep
2002
Reunion Is., Cap la Houssaye;
M. Zubia; Jul 2010
Fiji, Makuluva Is.; L. Mattio;
Apr 2007
New Caledonia, Ma^ıtre Is.; L.
Mattio; Sep 2005
Mauritius, Flic en Flac; L.
Mattio; Jun 2011
United States, Florida,
Newfound Harbor Key; O.
Camacho; April 2014
United States, Florida,
Summerland Key; O.
Camacho; April 2014
GenBank accessions
ITS-2
rbcLS
cox3
KF437946
KF437930
KF437947
KP064337
KM461676
KP064352
KP064338
KM461677
KP064353
KP064339
EU833439
EU833470
FJ170443
FJ170387
FJ170416
HQ416061
HQ416022
HQ416133
KM461678
KP064354
KP064340
KM461679
KP064355
KP064341
KF281945
KF281993
EU100785
EU100819
EU100830
EU100783
EU100812
EU100824
KF437942
KF437959
KF437926
KM461680
KP064342
KM461681
KP064356
KP064343
KM461682
KP064357
KP064344
KF413701
KF413688
KF413707
EU833422
EU833471
EU833405
EU833424
EU833458
EU833385
KF413704
KF413685
KF413715
KM461683
KP064358
KP064345
KM461684
KP064359
KP064346
(continued)
6
O. Camacho et al.
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Table 1. (Continued )
Taxon name revised
Vaucher
number
Collection site; Collector;
Collection date
Sargassum scabridum
WELT-A028417
Sargassum stenophyllum
LAF06611
Sargassum spinuligerum f. crispata
IRD3978
Sargassum cf. spinuligerum
GENT-TZ0400
Sargassum swartzii
IRD3912
Sargassum swartzii
IRD1532
Sargassum thunbergii
IRD5223
Sargassum thunbergii
IRD5241
Sargassum turbinarioides
IRD1604
Sargassum vulgare
SZNPattiS-Ca3
Sargassum vulgare
SZNPattiS-Ca4
Sargassum sp.
IRD1609
New Zealand, Auckland; W.
Nelson; 2005
Colombia, Magdalena, Concha
(TNNP); O. Camacho; Apr
2009
New Caledonia, ^ılot Signal; L.
Mattio; 2005
Tanzania, Mtwara, Mikindani
Bay; K. Pauly; Jan 2008
New Caledonia, ^ılot Ma^ıtre; L.
Mattio; Sep 2005
New Caledonia, Thio, C.
Bertaut; Apr 2006
Japan, Mitohama, Misaki; F.
Mineur; Oct 2010
Japan, Mitohama, Misaki; F.
Mineur; Oct 2010
New Caledonia, Ile des Pins; C.
Payri; Dec 2005
Italy; A. Chiarore & F.P. Patti;
2012
Italy; A. Chiarore & F.P. Patti;
2012
New Caledonia, Rocher a la
voile; L. Mattio; May 2005
mtsp was Felsenstein 1981 plus Gamma. The Maximum
likelihood (ML) tree reconstruction was performed in
RAxML (Stamatakis, 2006) on the partitioned (ITS-2 C
rbcLS 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 consisted of two independent runs of three heated chains and
one cold chain, run for seven million generations and sampled every 100 generations (total of 140 002 trees). Convergence was visualized in Tracer v1.5, and the first
17 500 trees were discarded as burn-in. The Bayesian consensus tree and best ML tree were rooted with species of
Sargassum subgenus Bactrophycus, representing the closest 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 consensus 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
GenBank accessions
ITS-2
rbcLS
cox3
FJ170456
FJ170393
FJ170423
KF437941
KF437958
KF437925
FJ170462
FJ170401
FJ170428
HQ416072
HQ416019
HQ416131
EU882255
EU882264
EU882254
EU100807
KF281946
KF413706
KF281994
KF281927
KF281785
KF281980
EU882256
EU882265
EU882245
KJ572482
KJ572496
KJ572483
KJ572494
EU882248
EU882259
EU882237
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 maximum genetic distance of representative clusters of sequences 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 holdfast) 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.
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Morphological and molecular assessment of Sargassum
7
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); values 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 Mexico; HI, Hawaii; IT, Italy; JP, Japan; MAUR, Mauritius; NC, New Caledonia; NCar, North Carolina; NZ, New Zealand; PanCar, Panama; PR, Puerto Rico; RUN, Reunion Is.; S, The Solomon Islands; TZ, Tanzania; Va, Vanuatu.
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
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8
O. Camacho et al.
Figs 2 5. Sargassum schnetteri comb. nov. (2) Immature specimen. (3) Isotype herbarium specimen (UTMC-07510); female thallus from
Ensenada Neguanje (TNNP), Colombia. (4) Holdfast rhizomatous with vegetative re-growth or new thallus (arrow). (5) Fertile branch with
groups 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.
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 sections 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 Sargassum 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 schnetteri 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 meaningfully 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 processed 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 significant resolution when compared with the concatenated
alignment analysis.
Morphological and molecular assessment of Sargassum
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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 Atlantic 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-Szechy
and Paula (2010), Ortega, Godinez, and Garduno-Solorzano (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 yellowbrown. 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 giving 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
9
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 projections 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, reaching 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. Cryptostomata elliptical or spherical, central pore 75 150 mm
long 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 Mexico (Texas, Louisiana), Florida, Bahamas, Caicos Is.,
Greater Antilles (Cuba), Lesser Antilles (Dominica, Venezuela) and Western Caribbean.
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10
O. Camacho et al.
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 first
branches with spine-like protuberances. Scales bars represent: Fig. 6, 5 cm; Fig. 7, 2 cm; Fig. 8, 2 cm.
Habitat. Frequent on rocky substrata and coral rubble up
to 4 m depth. Found in protected to moderately exposed
habitats.
Representative
material. LAF04290,
LAF06609,
LAF06610; LAF06613, LAF06614, BM-9, BM-45A,
BM-54.
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 conspicuously on the basal branches of S. pteropleuron as well as
on the substratum.
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. Cryptostomata 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-
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 Atlantico, ad littora Brasiliae’ in C. Agardh, 1820 p. 20].
utzing 1849, p. 615.
Synonymy. S. rigidulum K€
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Morphological and molecular assessment of Sargassum
11
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.
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 prominent 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), Magdalena (Punta Betın, Taganga, TNNP: Granate, Concha,
Gayraca, Neguanje). Western Atlantic: Bermuda, Gulf of
Mexico, Florida, Bahamas, Greater Antilles (Cuba, Hispaniola), 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 morphological 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.
Representative
material. LAF04106,
LAF04275, LAF04288, BM-164.
LAF04256,
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 conspicuous 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 spinelike protuberances up to 7 mm long, some with an apical
leaf up to 2 cm long and 2 mm wide with serrate margin;
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O. Camacho et al.
Figs 12 15. Sargassum filipendula. (12) Fertile herbarium specimen LAF04288A. (13) Fertile branch with receptacles intermixed with
vesicles 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.
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, Massachusetts, North Carolina, Gulf of Mexico (Mexico,
Texas, Louisiana, Mississippi, Alabama), Florida, Bahamas, Greater Antilles (Cuba, Hispaniola, Jamaica, Puerto
Rico), Lesser Antilles (Virgin Islands, St. Barthelemy,
Nevis, Guadeloupe, Dominica, Venezuela), Western
Caribbean (Mexico), Southern Caribbean (Colombia, Panama) and Brazil.
Habitat. Intertidal and subtidal zones to 3 m depth, in
protected or exposed habitats.
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Morphological and molecular assessment of Sargassum
13
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.
Notes. Additional morphological and molecular work
need to be done at the infraspecific level in order to accurately designate varieties and forms of S. filipendula
housed in various herbarium collections. For instance,
Wynne (2011) recognized four named varieties, in addition to the nominate variety for the tropical and subtropical 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-A92174) 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.
Representative
LAF06929.
material. LAF04276,
LAF06920,
Morphology. Plants pelagic, without a holdfast or a distinct main axis. Branches smooth or with few spiny projections, terete or sometimes compressed, 1 1.8 mm
diam., ramified several times. Leaves simple, flat, lanceolate 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 MartaTNNP area.
Sargassum hystrix J. Agardh 1847
(Figs 18 19)
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O. Camacho et al.
Figs 18 19. Sargassum hystrix. (18) Fertile herbarium specimen LAF04131. (19) Receptacle with spine-like protuberances and
extruded oogonia. Scales bars represent: Fig. 18, 5 cm; Fig. 19, 1 mm.
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].
utzing 1861, p. 15.
Synonym. Carpacanthus spinulosus K€
Representative material. LAF04131, LAF04292, D-P
550, D-P 556, D-P 608, D-P 421.
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 frequently found below 10 m depth. Found in both protected
and moderately exposed habitats.
Morphology. Plants up to 30 cm high, olive greenbrown. 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 alternate secondary branches. Leaves simple, flat, oblongelliptical 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 spherical, 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.
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 mentioned this species in deep-water habitats up to 137 m
deep. In the present study, receptacles with spine-projections (a diagnostic character of this species, Agardh,
1847) were observed only in the Geyer Bank specimens.
Agardh’s original description also defined the receptacles as forming dense axillary groups; however, the
specimens collected, and observed from different herbaria, 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).
Distribution. Colombia: Oceanic atolls (Cays: Serrana,
Roncador, Courtown), Western Atlantic: Bermuda, Gulf
Sargassum natans (Linnaeus) Gaillon 1828
(Figs 20 21)
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Morphological and molecular assessment of Sargassum
15
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.
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; Baccalaria 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.
Representative
material. LAF04257,
LAF06437, LAF06919.
LAF05425,
Morphology. Plants pelagic, without a holdfast or a distinct 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 compressed. Cryptostomata and receptacles not observed.
Distribution. Colombia: Bolivar (Cartagena), San
Andres and Providence Islands. Western Atlantic: Canada
(Newfoundland), Massachusetts, North Carolina, Bermuda, Gulf of Mexico (Mexico, Texas, Louisiana,
Alabama), Florida, Bahamas, Caicos Is., Greater Antilles
(Cuba, Hispaniola, Jamaica), Lesser Antilles (Guadeloupe, 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 Dernieres,
Louisiana). Refer to Silva et al. (1996) for details on the
complex taxonomic and nomenclatural history of this
species.
Sargassum polyceratium Montagne (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
K€utzing, 1849.
polyceratius
(Montagne)
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16
O. Camacho et al.
Figs 22 24. Sargassum polyceratium. (22) Habit of fertile thallus. (23) Spine-like protuberances on tertiary branches. (24) Tertiary
branch with receptacles, vesicles and undulate leaves. Scales bars represent: Fig. 20, 5 cm; Fig. 21, 4 mm; Fig. 22, 1 cm.
Representative material. LAF04105, LAF04291, BM15, 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 recurved 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), compressed 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). Receptacles 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 receptacles 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 Guıa 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 Cayman, Jamaica, Hispaniola, Puerto Rico), Lesser Antilles
(Virgin Islands, Guadeloupe, St. Lucia, Barbados, Curacao, 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. polyceratium var. ovatum (Collins) W.R. Taylor. Specimens found
in other localities without crisped leaves, narrower
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Morphological and molecular assessment of Sargassum
17
Figs 25 27. Sargassum stenophyllum. (25) Fertile herbarium specimen LAF06611. (26) Non-fertile branch. (27) Apical part of a branch
with leaves and small vesicles. Scales bars represent: Fig. 25, 5 cm; Fig. 26, 1 cm; Fig. 27, 2 cm.
(3 5 mm wide) than in S. polyceratium, with few or lacking spines-like protuberances and without a dense thallus
appearance, may resemble S. vulgare C. Agardh. However, we found it very difficult to distinguish S. vulgare
from S. polyceratium in Colombia. Kilar and Hanisak
(1988, 1989) found 47 different morphotypes, and significant seasonal variability in blade morphology in S. polyceratium 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 neotype proposed by Ramon and Gil-Ad (2007) from the
Mediterranean Sea was rejected by the Committee on
Algae (Prud’homme van Reine, 2011).
Sargassum stenophyllum Martius (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
(Martius) Grunow 1916, p. 138.
var.
stenophyllum
Representative material. LAF06611, LAF06654, BM62, 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 secondary 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 spinelike 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 mm
long 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
18
O. Camacho et al.
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.
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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. MICH 1210567.
racemes have alternated, distanced, simple to 4 times
dichotomously branched receptacles, on stipes 1 2 mm
long, not mixed with leaves or vesicles. Female receptacles 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 substrate and entangle together with other individuals forming underwater forests of up to 8 m high.
Isotype. LAF04289.
Type locality. Granate Bay, Tayrona (Tayrona National
Natural Park), Caribbean Colombia.
Etymology. This species is named for its exceptionally
large size.
Representative
LAF06607.
material. LAF04289,
LAF06605,
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 compressed 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, lanceolate 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 protuberances. 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;
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 giganteum 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 serrate; (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) cryptostomata are bigger, very conspicuous and raised particularly in distal parts of the plant; and (5) S. giganteum
thalli are much taller and have a laxer aspect than S. filipendula. 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 & Suarez, 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 analysis and molecular results from this study provided
19
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Morphological and molecular assessment of Sargassum
Figs 28 31. Sargassum giganteum sp. nov. (28) Holotype: fertile herbarium specimen in MICH 1210567. (29) Branched female receptacle with extruded oogonia on a sterile stipe. (30) Fertile branch with leaves and axillary receptacles. (31) Secondary branch of a fertile
specimen. Scales bars represent: Fig. 28, 20 cm; Fig. 29, 1 mm; Fig. 30, 1 cm; Fig. 31, 2 cm.
20
O. Camacho et al.
enough evidence to confirm it is not the case. Sargassum
giganteum sp. nov. was recognized and cited as Sargassum sp. in Camacho and Hernandez-Carmona (2012).
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Key for the identification of Sargassum species from the Caribbean Colombia and other
western tropical Atlantic areas
A key is provided for the identification of all 10 Sargassum morpho-species reported in this study for the Colombian 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 apical 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 protuberances 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 racemes to 10 mm long.....................................S. stenophyllum
8b. Leaves with serrate margins, cryptostomata abundant. 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.
Discussion
In 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. pteropleuron (see the Taxonomy section).
Both molecular and morphological analyses demonstrated the nesting of C. schnetteri within Sargassum.
This species was originally described based exclusively
on morphological characters (Bula-Meyer, 1980), and recognized mainly by its rhizomatous holdfast (instead of a
discoid or conical holdfast as in the other Sargassum morphotypes in the region), the absence of vesicles and the
shape of its leaves. Our molecular results clearly demonstrate that these characters do not warrant generic level
and that Cladophyllum should instead be considered a
Sargassum species within subgenus Sargassum. BulaMeyer (1980) himself had discussed the considerable
morphological affinity between these two genera. For
example, other species classified in S. subgenus Sargassum 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 sections have recently been proposed to accommodate species 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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Morphological and molecular assessment of Sargassum
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 fusing with one another (Tseng & Baoren, 2002), or S. cornutifructum 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. hemiphyllum (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. schnetteri 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 morphologically 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 Sargassum (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 species 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 Atlantic morphospecies identified in the present study belong to
the polytomic and widely distributed (worldwide) S. section Sargassum clade, providing limited molecular differentiation 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
21
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, Tatarenkov, 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, and
Pearson (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 uncovered 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 present 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; Ganesan, 1989; Guiry & Guiry, 2014; Menezes-Szechy &
Paula, 2010; Moreira & Cabrera, 2007; Paula, 1988; Taylor, 1960; Wynne, 2011). Among them, the pelagic species 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 Virginia 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. borbonicum in Reunion (Mattio et al., 2013) and S. albemarlense 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-dispersal 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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22
O. Camacho et al.
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 Scytothalia dorycarpa (Turner) Greville in western Australia
where its distribution was narrowed down by approximately 100 km following a marine heatwave (Smale &
Wernberg, 2013). Likewise, the endemic Bifurcaria galapagensis (Piccone & Grunow) Womersley from the Galapagos 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 population 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.
Acknowledgements
We acknowledge Claude Payri, Nathalie Duong and the
Plateforme du Vivant at IRD in Noumea 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 additional specimens from Panama, Florida and the Gulf of
Mexico. We thank Dr Patrik Fr€
oden, 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 anonymous reviewers for their valuable criticism of the manuscript, to William Schmidt for his help with the
molecular analyses, and to Carlos Alberto Trujillo for
assistance in field collections.
Supplemental data
Supplemental data for this article can be accessed here.
Appendix 1. Close up of Sargassum section Sargassum clade
taken from the Maximum likelihood (RAxML) tree of the combined ITS-2, rbcLS and cox3. Values at the nodes indicate Bootstrap support (left) and Posterior Probability (right); values
below 50 are not shown or represented by ‘ ’. Area abbreviations: C, Colombia; FP, French Polynesia; GoMX, Gulf of Mexico; IT, Italy; MAUR, Mauritius; NC, New Caledonia; NCar,
North Carolina; NZ, New Zealand; PanCar, Panama; PR, Puerto
Rico; TZ, Tanzania.
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Associate Editor: Elliot Shubert
Stefano Draisma