Reassessment of Tristan da Cunha Gelidium (Gelidiales, Rhodophyta) species - De Gruyter
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Botanica Marina 2020; 63(5): 455–462
Short communication
D. Wilson Freshwater*, Sue Scott, Enrico M. Tronchin and Gary W. Saunders
Reassessment of Tristan da Cunha Gelidium
(Gelidiales, Rhodophyta) species
https://doi.org/10.1515/bot-2020-0036 islands of the archipelago as part of a Norwegian scientific
Received May 14, 2020; accepted June 24, 2020; published online expedition to the islands in 1937–1938. More recently, Scott
August 21, 2020 and colleagues have included observations of marine algae
as part of surveys of the marine environment, flora and
Abstract: Three endemic species of Gelidium have been
fauna (Scott and Tyler 2008; Scott 2010a, 2010b, 2017), and
described from the remote Tristan da Cunha archipelago. A
Saunders et al. (2019) published DNA barcode sequences
recent barcode survey of Tristan da Cunha red algae in
for red algae from the islands.
combination with the clarification of vouchers for previously
Baardseth (1941) reported four Gelidiales in his study,
sequenced specimens has prompted a molecular and
all of which he described as new species. These included
morphological reassessment of these species. Analyses of
one Gelidiella, G. feldmannii Baardseth, and three species
rbcL and COI-5P data indicated that all sequenced Tristan da
of Gelidium, Gelidium concinnum Baardseth, Gelidium
Cunha specimens represented a single taxon, and further-
inflexum Baardseth, and Gelidium regulare Baardseth. The
more that this genetic group was conspecific with Gelidium
three Gelidium species were described as differing in height
micropterum from southern Africa. Morphologically the
and the shape of main axes (Table 1). G. regulare was also
Tristan da Cunha specimens represented either Gelidium
distinguished by specimens having single distinctive main
concinnum or Gelidium regulare, and there was a grade of
axes that were noticeably lanceolate, a regular decrease in
character states between both of these species, as well as
size with each branch order, and internal rhizoidal fila-
G. micropterum. Based on these results the synonymy of
ments that were concentrated in the inner cortex and outer
G. concinnum and G. regulare under G. micropterum is pro-
medulla. G. inflexum was described as forming extended
posed and an expanded description of G. micropterum pro-
mats, had more irregular branching with branch bases
vided. None of the studied Tristan da Cunha specimens
varying in level of constriction, and fertile branches that
clearly fit the description of the third endemic species,
resembled lobes off the main axes.
Gelidium inflexum, and its status could not be determined.
Tronchin and Freshwater generated rbcL sequences
Keywords: COI-5P; DNA barcode; Gelidium concinnum; from Tristan da Cunha Gelidium specimens collected by
Gelidium inflexum; Gelidium micropterum; Gelidium regu- Scott in 2004, but these data were never published. The
lare; rbcL. recently generated sequences from Saunders et al. (2019),
as well as clarification of vouchers for the Tronchin and
Tristan da Cunha is a remote British Overseas Territory of Freshwater sequences, have now facilitated a reassess-
four islands located roughly midway between South Africa ment of Baardseth’s Gelidium species.
and South America and accessible only by sea. Baardseth Specimens included in this study were collected from
(1941) studied the marine algae of the three northernmost Tristan and Nightingale islands during 2004 and 2010, and
South Africa during 1992 (Table S1, Figures 1–3, S1).
Morphological examinations were made of herbarium
*Corresponding author: D. Wilson Freshwater, Center for Marine
specimens and permanent microscope slides. Transverse
Science, University of North Carolina at Wilmington, 5600 Marvin K.
Moss Lane, Wilmington, NC, 28409, USA, and longitudinal sections were made by hand and stained
E-mail: freshwaterw@uncw.edu. using 1% aniline blue (Millar and Wynne 1992). The rbcL
https://orcid.org/0000-0003-0125-3133 sequences of specimens collected in 2004 were generated
Sue Scott, Cana, North Strome, Lochcarron, Ross-shire, IV54 8YJ, UK as described in Tronchin and Freshwater (2007). COI-5P
Enrico M. Tronchin, Callaghan Innovation, 55 Featherston St. Level 14,
and rbcL sequences from specimens collected in 2010 were
Mount Victoria, New Zealand
Gary W. Saunders, Centre for Environmental & Molecular Algal
generated and published by Saunders et al. (2019). New
Research, Biology, University of New Brunswick, Fredericton, New sequences in this study were determined following the
Brunswick, E3B 5A3, Canada methods of Taylor et al. (2017) and using primers GWSFn;
456
Table : Characteristics of Tristan da Cunha Gelidium species described by Baardseth (), Gelidium micropterum from South Africa, and Tristan da Cunha specimens sequenced in this study.
G. concinnuma G. regularea G. inflexuma G. micropterumb TdC specimensc
Habitat Intertidal pools and subtidal Shaded rock pools On rocks or CCA in inter- Lower intertidal and pools Intertidal, tide pools and subtidal to > m depth
to ca. m depth tidal of exposed shore
Height – cm – cm
D.W. Freshwater et al.: Tristan da Cunha Gelidium species 457
Figures 1–3: Specimens of Tristan da Cunha Gelidium and G. micropterum from South Africa. (1) 2004 collected, upper intertidal Tristan
specimen field identified as G. inflexum. Scale = 1 cm. (2) 2010 collected, subtidal Nightingale specimen field identified as G. concinnum.
Scale = 2 cm. (3) Gelidium micropterum intertidal specimen collected from the Cape Peninsula, South Africa. Scale = 0.5 cm.
GWSRx for COI-5P (Le Gall and Saunders 2010; Saunders confirmed that G. micropterum and the specimens from
and McDevit 2012) and F57; F753; R1144 (5′-CCRCARTG- Tristan da Cunha are nearly identical (99.7–99.9% simi-
TATACCACCAGA-3′) or R1150; RrbcSstart for rbcL (Fresh- larity, Table S2).
water and Rueness 1994; Freshwater et al. 2017). Sequence Saunders et al. (2019) also generated COI-5P se-
data were aligned with Muscle (Edgar 2004) and phyloge- quences for three Tristan da Cunha Gelidium specimens
netic analyses conducted using RAxML (Stamatakis et al. (GenBank#s MK202363; MK202369; MK202424) and
2005) as implemented in Geneious (v. R9; Biomatters, these were identical. These sequences were 98.6%
Auckland, New Zealand). similar to the COI-5P of a newly sequenced South African
Saunders et al. (2019) generated rbcL sequences for G. micropterum specimen (GenBank# MT577583). Two
two Tristan da Cunha Gelidium specimens, one field iden- unpublished COI-5P sequences were available in Gen-
tified as G. concinnum (GenBank# MK185755) and the other Bank from other laboratories for specimens identified as
as G. inflexum (GenBank# MK185763). The sequences were G. micropterum. The provenance of these specimens was
identical, and BLAST searches returned a greatest homol- not included in their GenBank records, but it was likely
ogy with Gelidium vittatum (Linnaeus) Kützing at 98% southern Asia – these sequences were458 D.W. Freshwater et al.: Tristan da Cunha Gelidium species
minimum K.M. Kim, I.K. Hwang, H.S. Yoon et S.M. Boo, 2010 008] varied in the latter character. Internal
Gelidium microdonticum W.R. Taylor, and species rhizoidal filaments were heavily concentrated within
included in the Gelidium millariana species complex - the inner cortex and outer medulla of its main axes, but
G. millariana G.H. Boo, Hughey, K.A. Miller et S.M. Boo, there was a more even distribution of these cells
Gelidium pakistanicum (Afaq-Husain et Shameel) Shah- throughout the inner cortex and medulla in lateral
naz et Freshwater, and Gelidium palmatum G.H. Boo et branches (Figures 5 and 6).
K.M. Kim. One each of the specimens collected in 2004 and 2010
Baardseth (1941, p. 52) questioned the morphological were field identified tentatively as G. inflexum. These
characters he used to distinguish his new species stating collections were both turfs from the upper intertidal zone
that their systematic value was uncertain. Morphological matching Baardseth’s description of the species being
examination of the sequenced Tristan da Cunha speci- mat-forming in exposed parts of the intertidal. However,
mens (Figures 1 and 2, S1, Table S3) revealed a wide range the specimens were larger, and did not have lobe-like
of character states that encompassed Baardseth’s con- reproductive branches as described and illustrated by
cepts of G. concinnum and G. regulare. The majority of Baardseth (1941, p. 54, figure 24d, 24e). The specimen
these specimens matched the size and gross morphology collected in 2004 (Figure 1) was a better fit to the
of Baardseth G. concinnum specimens in the LD, BM, and G. regulare specimen shown in Baardseth (1941, p. 52,
UC herbaria. As described, G. regulare differs from figure 23). Although Baardseth (1941, p. 52) postulated
G. concinnum by being shorter; having lanceolate, single that G. inflexum could be a habitat-induced stunted form
main axes; producing branches that regularly diminish of a larger species, none of the specimens re-examined in
in size with each branch order, and demonstrating in- this study fits his description of this species and its status
ternal rhizoidal filaments concentrated within the inner remains in question.
cortex and outer medulla. The smaller studied specimens Just as the range of morphological variation
exhibited varying grades of these states except for the exhibited by the sequenced Tristan da Cunha specimens
distribution of internal rhizoidal filaments, which was encompasses the concept of both G. concinnum and
relatively even throughout the medulla and inner cortex. G. regulare, it also overlapped with that described for
Only the largest Tristan da Cunha specimen [Nightingale G. micropterum (Table 1). A key character of
G. micropterum is the production of bisporangia instead
of tetrasporangia by the sporophyte life history stage
(Stegenga et al. 1997). Bisporangia are produced by a
single periclinal division of the sporangial mother cell
in the Gelidiales (Carter 1985; Fan 1961), an attribute
that is not easily recognized in surface view. Baardseth
(1941) described the shape of the sporangial sori, but
evidently did not make sections of them to observe
characteristics of the sporangia. However, the produc-
tion of bisporangia was verified in all the fertile sporo-
phyte specimens from Tristan da Cunha included in this
study (Figures 7 and 8, Table S3). Bisporangia are un-
common in the Gelidiales and are currently only re-
ported in G. foliaceum, G. micropterum, G. pristoides,
and G. vittatum (Carter 1985; Fan 1961; Norris 1992;
Stegenga et al. 1997). All four species have southern
African distributions and are consistently resolved
within the same strongly supported clade by phyloge-
netic analyses (e.g. Boo et al. 2014; Freshwater et al.
1995; Tronchin et al. 2002).
Based on these new molecular analyses and the
Figure 4: Maximum likelihood (ML) tree resulting from analysis of
observed overlap in morphological character states the
rbcL sequences for 19 Gelidium specimens. Bootstrap support
values (1000 replications) ≥ 70% are displayed along branches. The
synonymy of G. concinnum and G. regulare under
ML analysis applied the GTR CAT I model and rapid hill-climbing G. micropterum is proposed, and an expanded description
algorithm with the data partitioned by codon position. of the species provided.D.W. Freshwater et al.: Tristan da Cunha Gelidium species 459
Gelidium micropterum Kützing (1868, p. 29, pl.
59c–g)
Heterotypic synonyms
Gelidium concinnum Baardseth (1941, p. 50, figs. 22, 24B, C)
Gelidium regulare Baardseth (1941, p. 52, figs. 23, 24A)
Description
Thallus cartilaginous, consisting of bushy to more lax
erect fronds to 15 cm tall, arising from a prostrate system
of terete to compressed stoloniferous axes extending
from the base of main axes and attached to the substra-
tum by brush-like haptera (Figure 9). Erect axes are
compressed to flattened, and alternately to oppositely
pinnately branched to four (five) orders (Figures 1–3, S1).
Branching sometimes irregular, especially where clusters
of branches develop at wound sites. Erect axes observed
to sometimes develop haptera from blade surfaces (Fig-
ures 10 and 11) and also develop into stoloniferous axes.
Main axes linear, lanceolate or elongately clavate and
often curved or bent. Lateral branches mostly tapered to
constricted at their bases and with obtuse to widely acute
apices. Ultimate and penultimate laterals often short and
issuing at short intervals, with emarginate apices when
fertile (Figure 12).
Axes composed of 3–4 layers of pigmented, globose to
polygonal cortical cells surrounding a medulla of thick-
walled, oblong to elongate cells. The distribution of inter-
nal rhizoidal filaments is variable from relatively evenly
distributed throughout, to being concentrated in either the
inner cortex and outer medulla, or inner medulla (Fig-
ures 5, 6, and 13).
Bisporangial sori develop in the apical part of
branches and are ellipsoidal to elongate with relatively
wide, ill-defined sterile margins (Figure 12). Bisporangia
are generally obovate, 20 × 30 µm to 30 × 40 µm, and are
present in various stages of development throughout
the sori (Figures 7 and 8). Cystocarps are bilocular with a
placental tissue of nutritive filament and gonimoblast
cells giving rise to elongate elliptical to obovate
illumination; Scale = 50 μm. (6) Transverse section showing even
distribution of internal rhizoidal filaments (arrows) in specimen
Figures 5–8: Distribution of internal rhizoidal filaments and Nightingale 2010 008 lateral branch. Scale = 50 μm. (7) Longitudinal
bisporangia in Tristan da Cunha Gelidium specimens. Specimen section of specimen TDC20 bisporangial sorus showing sporangial
codes from Table S1. (5) Transverse section showing concentration mother cells (arrowheads) and bisporangia (arrows) at various
of internal rhizoidal filaments (arrows) in the outer medulla and stages of development. Scale = 20 μm. (8) Bisporangia formed from
inner cortex of specimen Nightingale 2010 008 main axis. DIC single periclinal divisions. Specimen ‘inflex’; Scale = 20 µm.460 D.W. Freshwater et al.: Tristan da Cunha Gelidium species
Figures 9–15: Gelidium micropterum morphological features. (9) Transverse section through sub-terete stoloniferous axis and brush-like
hapteron. Specimen ‘inflex’; Scale = 50 μm. (10) Brush-like hapteron (arrow) and hapteron initial (arrowhead) developing on blade
surface. Specimen “Nightingale 2010 023”; scale = 100 μm. (11) Hapteron initial developing from blade surface. Specimen “Nightingale
2010 008”; scale = 50 μm. (12) Ultimate and penultimate laterals with bisporangial sori. Specimen “TDC20”; scale = 500 μm. (13)
Transverse section showing 3-4 layers of pigmented cortical cells surrounding thick-walled medullary cells and evenly distributed
internal rhizoidal filaments (arrows). Specimen “microp RSA 3”; scale = 30 μm. (14) Transverse section of bilocular cystocarp. Specimen
“microp RSA 2”; scale = 100 μm. (15) Longitudinal section of bilocular cystocarp with simple openings without peristomes (arrows).
Specimen “microp RSA 2”; scale = 500 µm.
carposporangia (Figures 14 and 15). Third-order cell Initiative, RSPB and the people of Tristan da Cunha;
filaments frequently extend from the central placental GWS - This research was supported through NSERC
tissue to the six to nine cell thick pericarp through which Discovery funding, and by the Canada Foundation for
simple openings without peristomes develop (Figures 14 Innovation and the New Brunswick Innovation
and 15). Spermatangia have not been observed. Foundation.
Conflict of interest statement: The authors declare no
conflicts of interest regarding this article.
Acknowledgements: The authors wish to acknowledge the
people of Tristan da Cunha for their support during
fieldwork.
Author contribution: All the authors have accepted
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Saunders, G.W. and McDevit, D.C. (2012). Methods for DNA barcoding interests include molecular phylogeny and taxonomy of marine algae,
photosynthetic protists emphasizing the macroalgae and marine floristics, Scomberomorus maculatus artificial bait
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Sue Scott
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p. 40. Sue Scott is a retired freelance marine biologist and consultant based
Scott, S. (2017). A biophysical profile of the Tristan da Cunha in the highlands of Scotland. She has particular interests in subtidal
archipelago. Commissioned and reviewed by The Pew Charitable community structure in colder seas, macroalgal identification and
Trusts, p. 187. impacts on the marine environment. Since 2004 she has made
Scott, S. and Tyler, P. (2008). Underwater life of Tristan da Cunha. numerous trips to Tristan da Cunha for intertidal and subtidal surveys,
Report For Darwin Initiative Project No: 162/12/010. macroalgal collections and impact assessment of marine accidents.462 D.W. Freshwater et al.: Tristan da Cunha Gelidium species
Enrico M. Tronchin Gary W. Saunders
Callaghan Innovation, 55 Featherston St. Level Centre for Environmental & Molecular Algal
14, Mount Victoria, New Zealand Research, Biology, University of New
Brunswick, Fredericton, New Brunswick, E3B
5A3, Canada
Enrico M. Tronchin worked on this project while a visiting researcher Gary W. Saunders is a researcher at the Centre for Environmental &
at the Center for Marine Science, University of North Carolina Molecular Algal Research, Biology, University of New Brunswick
Wilmington and Claude Leon Harris Postdoctoral Fellow at the Fredericton. His current research interests include biodiversity and
University of Cape Town. He currently is the manager of biogeography of seaweeds with an emphasis on origins of the Arctic
Commercialisation Development at Callaghan Innovation in New flora, as well as shifts in species ranges owing to climate change and
Zealand. kelp forest restoration.You can also read
