Content uploaded by Craig Schneider
Author content
All content in this area was uploaded by Craig Schneider on Sep 16, 2024
Content may be subject to copyright.
2024 ● 45 ● 1
AlgologieAlgologie
Cryptogamie, Algologie est indexé dans / Cryptogamie, Algologie is indexed in:
– Aquatic Sciences & Fisheries Abstracts Part I.
– Biological Abstracts
– Chemical Abstracts
– Current Contents
– Marine Science Contents Tables (FAO)
– Science Citation Index
– Publications bibliographiques du CNRS (Pascal)
Cryptogamie, Algologie est distribué en version électronique par / Cryptogamie, Algologie is distributed electronically by:
– BioOne® (http://www.bioone.org/loi/crya)
Cryptogamie, Algologie est une revue en ux continu publiée par les Publications scientiques du Muséum, Paris
Cryptogamie, Algologie is a fast track journal published by the Museum Science Press, Paris
Les Publications scientiques du Muséum publient aussi / The Museum Science Press also publish: Adansonia, Geodiversitas, Zoosystema,
Anthropozoologica, European Journal of Taxonomy, Naturae, Comptes Rendus Palévol, Cryptogamie sous-sections Bryologie, Mycologie.
Diusion – Publications scientiques Muséum national d’Histoire naturelle
CP 41 – 57 rue Cuvier F-75231 Paris cedex 05 (France)
Tél. : 33 (0)1 40 79 48 05 / Fax : 33 (0)1 40 79 38 40
di.pub@mnhn.fr / http://sciencepress.mnhn.fr
© Publications scientiques du Muséum national d’Histoire naturelle, Paris, 2024
ISSN (imprimé / print) : 0181-1568 / ISSN (électronique / electronic) : 1776-0984
Directeur De la publication / Publication director: Gilles BLOCH
Président du Muséum national d’Histoire naturelle
réDactrice en chef / editor-in-chief: Line le Gall
Muséum national d’Histoire naturelle
assistant De réDaction / assistant editor: Chris LE COQUET-LE ROUX (algo@cryptogamie.com)
Mise en paGe / Page layout: Chris LE COQUET-LE ROUX
réDacteurs associés / associate editors
Ecoevolutionary dynamics of algae in a changing world
Stacy KRUEGER-HADFIELD
Department of Biology, University of Alabama, 1300 University Blvd, Birmingham, AL 35294 (United States)
Jana KULICHOVA
Department of Botany, Charles University, Prague (Czech Republic)
Cecilia TOTTI
Dipartimento di Scienze della Vita e dell’Ambiente, Università Politecnica delle Marche, Via Brecce Bianche, 60131 Ancona (Italy)
Phylogenetic systematics, species delimitation & genetics of speciation
Sylvain FAUGERON
UMI3614 Evolutionary Biology and Ecology of Algae, Departamento de Ecología, Facultad de Ciencias Biologicas,
Ponticia Universidad Catolica de Chile, Av. Bernardo O’Higgins 340, Santiago (Chile)
Marie-Laure GUILLEMIN
Instituto de Ciencias Ambientales y Evolutivas, Universidad Austral de Chile, Valdivia (Chile)
Diana SARNO
Department of Integrative Marine Ecology, Stazione Zoologica Anton Dohrn, Villa Comunale, 80121 Napoli (Italy)
Comparative evolutionary genomics of algae
Nicolas BLOUIN
Department of Molecular Biology, University of Wyoming, Dept. 3944, 1000 E University Ave, Laramie, WY 82071 (United States)
Heroen VERBRUGGEN
School of BioSciences, University of Melbourne, Victoria, 3010 (Australia)
Algal physiology & photosynthesis
Janet KÜBLER
California State University Northridge, Department of Biology, California State University, Northridge, CA 91330-8303 (United States)
Prokaryotic algae
Nico SALMASO
IASMA Research and Innovation Centre, Fondazione Mach-Istituto Agrario di S. Michele all’Adige, Limnology and River Ecology,
Via E. Mach, 1, 38010 San Michele all’Adige, Trento (Italy)
Vitor VASCONCELOS
Faculdade de Ciências da Universidade do Porto and CIIMAR, Rua do Campo Alegre, s/n, 4169-007 Porto (Portugal)
couverture / cover:
Extrait de la Figure 3 / Extract of the Figure 3
1
CRYPTOGAMIE, ALGOLOGIE • 2024 • 45 (1) © Publications scientiques du Muséum national d’Histoire naturelle, Paris. www.cryptogamie.com/algologie
Australasian Lophothamnion J.Agardh
aligns genetically with Pleonosporium Nägeli
(Wrangeliaceae, Spongoclonieae):
new species from the western Atlantic
Craig W. SCHNEIDER
Department of Biology, Trinity College, Hartford, Connecticut, 06106 (United States)
cschneid@trincoll.edu (corresponding author)
Gary W. SAUNDERS
Centre for Environmental & Molecular Algal Research, Department of Biology,
University of New Brunswick, Fredericton, NB E3B 5A3 (Canada)
Submitted on 22 August 2023 | Accepted on 27 October 2023 | Published on 17 January 2024
Schneider C. W. & Saunders G. W. 2024. — Australasian Lophothamnion J.Agardh aligns genetically with Pleonosporium
Nägeli (Wrangeliaceae, Spongoclonieae): new species from the western Atlantic. Cryptogamie, Algologie 45 (1): 1-10.
https://doi.org/10.5252/cryptogamie-algologie2024v45a1. http://cryptogamie.com/algologie/45/1
ABSTRACT
During a genetic analysis of western Atlantic Wrangeliaceae J.Agardh, specimens closely related to
the generitype of Lophothamnion J.Agardh fell into a clade including the generitype of the earlier
described Pleonosporium Nägeli, causing us to subsume the former genus. Two new species are de-
scribed, P. novae-angliae G.W.Saunders & C.W.Schneider, sp. nov. for specimens from southern New
England and New York, United States, formerly identified there as P. borreri (Smith) Nägeli, and
P. ricksearlesii C.W.Schneider & G.W.Saunders, sp. nov. from Bermuda. e relationship of Pleono-
sporium with its sister genus Spongoclonium Sonder is discussed with the transfer of Spongoclonium
australicum Womersley to Pleonosporium.
RÉSUMÉ
Le genre australasien Lophothamnion J.Agardh se révèle génétiquement aligné avec Pleonosporium Nägeli
(Wrangeliaceae, Spongoclonieae) : nouvelles espèces de l’Atlantique occidental.
Au cours d’une analyse génétique des Wrangeliaceae J.Agardh de l’Atlantique occidental, des spécimens
étroitement liés au généritype de Lophothamnion J.Agardh sont tombés dans un clade comprenant le
généritype de Pleonosporium Nägeli décrit précédemment, nous obligeant à englober le premier genre.
Deux nouvelles espèces sont décrites, P. novae-angliae G.W.Saunders & C.W.Schneider, sp. nov. pour
les spécimens du sud de la Nouvelle-Angleterre et de New York, États-Unis, anciennement identifiés
là-bas sous le nom de P. borreri (Smith) Nägeli, et P. ricksearlesii C.W.Schneider & G.W.Saunders,
sp. nov. des Bermudes. La relation entre Pleonosporium et son genre frère Spongoclonium Sonder est
discutée avec le transfert de Spongoclonium australicum Womersley dans Pleonosporium.
KEY WORDS
Bermuda,
New England,
Lophothamnion,
Pleonosporium,
Spongoclonium,
new combination,
new species.
MOTS CLÉS
Bermudes,
Nouvelle-Angleterre,
Lophothamnion,
Pleonosporium,
Spongoclonium,
combinaison nouvelle,
espèces nouvelles.
2CRYPTOGAMIE, ALGOLOGIE • 2024 • 45 (1)
Schneider C. W. & Saunders G. W.
INTRODUCTION
Two genetic species have been discovered in regular barcoding
assessments of marine macroalgae in North American and Ber-
mudian waters, both clustering with species of the three genera
presently comprising the tribe Spongoclonieae of the family
Wrangeliaceae J.Agardh (Choi et al. 2008), vis. Lophothamnion
J.Agardh (1892), Pleonosporium Nägeli (1862), and Spongo-
clonium Sonder (1855). ese genera have had complicated
and intertwined nomenclatural histories over the past more
than 150 years based upon branching patterns, cortication
of axes, and presence or absence of post-meiotic divisions in
tetrasporangia (Wynne 2005: note 104). Pleonosporium is a
widespread genus in the Wrangeliaceae presently consisting
of 31 species from tropical to polar waters (Guiry & Guiry
2023). It is characterized by uniseriate, filamentous axes often
with alternate distichous branching in distal regions, and with
most species corticated by rhizoidal investments over lower axes
but some ecorticate, and adaxial sporangia on upper branches
(Schneider & Searles 1991; Maggs & Hommersand 1993).
e monotypic Australasian genus Lophothamnion is based
upon L. comatum J.Agardh (1892), a species that was found
a century later to be a heterotypic synonym of L. hirtum
(Hooker f. & Harvey) Womersley from Australia, New Zea-
land and the subantarctic islands (Womersley & Wollaston
1998: 297). Lophothamnion has had a long nomenclatural
connection to the genus Pleonosporium, and both genera share
the production of polysporangia. De Toni (1903: 1309) was
the first to consider, although with some hesitation, that the
generitype L. comatum might better be placed in Pleonosporium
as P. ?comatum (J.Agardh) De Toni, while Laing (1905: 393)
moved Callithamnion hirtum Hooker f. & Harvey (Harvey &
Hooker 1845: 192) to Pleonosporium (as P. hirtum (Hooker
f. & Harvey) Laing) before Womersley & Wollaston (1998)
created the new combination in Lophothamnion. In effect,
Womersley & Wollaston (1998) resurrected the genus Lopho-
thamnion when they moved C. hirtum to the genus stating
that “there was no apparent difference between the Australian
L. comatum and the earlier named C. hirtum from the Auckland
Is…”. Lophothamnion is defined by basally branched lateral
branchlets with long unbranched termini, rhizoidal cortica-
tion proximally, and polysporangia sessile on lower cells of
lateral branches (Kylin 1956; Womersley & Wollaston 1998).
At present, Spongoclonium consists of ten species (Guiry &
Guiry 2023) confined to the Indo-Pacific except for one,
S. caribaeum (Børgesen) M.J.Wynne, known from the tropical
western Atlantic (Wynne 2022). e genus was described by
Sonder (1855) and based upon S. conspicuum Sonder from
Victoria, Australia, “presumably in reference to the spongy
texture of the thallus” (Huisman 2018). Since the protologue,
several species have been added to Spongoclonium, most from
Australia and New Zealand (Guiry & Guiry 2023), and all
lacking “spongy” habits. Spongoclonium is characterized by
dense, irregular branching, thick rhizoidal cortication proxi-
mally, and tetrasporangia, rarely octosporangia (Itono 1977;
Womersley & Wollaston 1998). It is noteworthy that Wom-
ersley & Wollaston (1998) loosely differentiated two groups
of species in southern Australia, those that strictly produce
tetrasporangia, and those that also produce octosporangia.
In the present study, we assess the two genetic species groups
from southern New England, United States, and Bermuda
that align in a clade comprised of the Spongoclonieae (Fig. 1).
Historically, one species of Pleonosporium has been reported
from southern New England, P. borreri (Smith) Nägeli, a
species with a European type locality, also known from the
Mediterranean Sea, many eastern Atlantic islands, and vari-
ous Indo-Pacific locations (Guiry & Guiry 2023). In North
America, it is reportedly distributed from Long Island Sound
to the southern side of Cape Cod, Massachusetts. No other
member of the Spongoclonieae has previously been reported
in this region (Mathieson & Dawes 2017), nor any in the
Bermuda flora (Schneider 2003). Along with the genetic
species that we have discovered from these two areas, we also
consider genus-level relationships within the tribe.
MATERIAL AND METHODS
Fragments of individual specimens chosen for DNA analysis
were dried on silica gel and also preserved with 4-5% formal-
dehyde in sea water for anatomical study. e remainder of
each specimen was pressed fresh and dried on herbarium paper
as archival vouchers. Wet specimen fragments were mounted
permanently on microscope slides in a 20:1 solution of 30%
Karo® corn syrup (ACH Food Company, Inc., Memphis,
TN, United States) and 1% aniline blue. Dried specimens
were scanned on an Epson ET-2650 scanner (Seiko Epson
Corporation, Suwa, Nagano, Japan), and photomicrographs
were taken using a Zeiss Axioskop 40 microscope (Carl Zeiss,
Oberkochen, Germany) equipped with a Spot Idea 28.2-5MP
digital camera (Diagnostic Instrument, Sterling Heights,
MI, United States). Voucher specimens are deposited in the
herbaria under each species (herbarium abbreviations follow
the online Index Herbariorum (iers 2023) and standard
author initials follow the online International Plant Names
Index (IPNI, https://www.ipni.org/index.html). e Phycotheca
Boreali-Americana (P.B.-A.) exsiccata cited here (Collins et al.
1897) is part of the personal herbarium of CWS.
DNA extractions of our silica-dried samples followed
Saunders & McDevit (2012), and PCR amplification and
sequencing of COI-5P, rbcL and SSU were as detailed in
Saunders & Moore (2013). Amplification products were sent
to Genome Quebec for sequencing, and all successfully gen-
erated sequences for all specimens and markers are included
in Appendix 1. In addition, rbcL data for Pleonosporium
borreri were downloaded from GenBank for our analyses
(Appendix 1). ree single-gene alignments were generated:
COI-5P (11 sequences, 664 bp [base pairs]); rbcL (13 sequences,
1358 bp); and SSU (7 sequences, 1750 bp). ese alignments
were analyzed separately in Geneious 2023.1.1 with maximum
likelihood (general time reversible with invariant sites and
gamma-distributed rates for the variable sites, GTR + I + G;
Soares et al. 2019) using RAxML (Stamatakis 2014) with
partitioning by codon (for the two protein coding genes) and
3
New Pleonosporium species from the western Atlantic
CRYPTOGAMIE, ALGOLOGIE • 2024 • 45 (1)
500 bootstrap replicates. Because no strong conflicts were
detected, concatenated COI-5P + rbcL + SSU (13 sequences,
3742 bp) and COI-5P + rbcL (13 sequences, 1992 bp) align-
ments were constructed with analyses as described for the
single-gene alignments, but with partitioning by gene and
codon and with 1000 bootstrap replicates (Fig. 1). Phyloge-
netic trees were rooted with an outgroup of allied genera in
the Wrangeliaceae (Choi et al. 2008).
RESULTS
Newly generated rbcL sequences for what had previously been
reported as Pleonosporium borreri from New England differed
by 81 substitutions from a European collection of this species
(Appendix 1). Indeed, our North American specimens were
closer to an entry in GenBank for Lophothamnion hirtum
(diverging by only 48 substitutions). us, more species of
these genera were sequenced precipitating the current study.
Our phylogenetic analyses resolved collections from southern
New England and Bermuda as sister species (Fig. 1), these
in turn allied to Lophothamnion (L. hirtum specimen from
Tasmania, type locality: Auckland Island, New Zealand) and
Spongoclonium australicum (specimen from Tasmania, type
locality: Kangaroo Island, SA, Australia). e previous were
sister to the type species of Pleonosporium (P. borreri specimen
from Galicia in northwestern Spain, type locality: Yarmouth,
England), with the type of Spongoclonium (S. conspicuum
specimen from Warrnambool, VIC, Australia, type locality:
Victoria, Australia) a distant sister to all the previous (Fig. 1).
ese presently represent all of the genera in the Spongoclo-
nieae (Guiry & Guiry 2023), but a further complication was
the distant and variously unsupported alliance to the Pacific
species (P. cf. squarrosum and sp. 3GWS; as well as other
species not included in the current study) currently assigned
to Pleonosporium (Fig. 1). As a result of our analyses, we
return L. hirtum to Pleonosporium where it had been earlier
moved by Laing (1905), designate here a new combination
for S. australicum in the same genus, and recognize two new
species for the western Atlantic.
Family Wrangeliaceae J.Agardh
Genus Pleonosporium Nägeli
Pleonosporium hirtum (Hooker f. & Harvey)
Transactions and Proceedings of the New Zealand Institute 37: 393,
pl. 27, fig. 1 (Laing 1905). — Callithamnion hirtum Hooker f. &
Harvey, Flora Antarctica pl fig arvey ooker
Type localiTy. — New Zealand, Auckland Island.
Pleonosporium australicum (Womersley)
G.W.Saunders & C.W.Schneider, comb. nov.
Spongoclonium australicum Womersley in Womersley & Wollas-
ton, e Marine Benthic Flora of Southern Australia: 293, 296, 297,
figs 139, 141A, B (Womersley & Wollaston 1998).
Type localiTy. — Australia, South Australia, Kangaroo Island.
98/91/94
93/84/92
97/97/97
90/74/84
99/98/97
78/na/na
46/63/53
na/61/55
*
*
*
97
0.07
Spermothamnion repens
Plumaria plumosa
Ptilota asplenioides
Haloplegma sp. 2WA
Dasythamniella dasyura
Pleonosporium cf. squarrosum
Pleonosporium sp. 3GWS
Spongoclonium conspicuum
Pleonosporium borreri
Pleonosporium novae-angliae sp. nov.
Pleonosporium ricksearlesii sp. nov.
Pleonosporium (Spongoclonium) australicum comb. nov.
Pleonosporium (Lophotamnion) hirtum
Pleonosporium
fiG. 1. — Maximum likelihood analyses of the SSU + rbcL + COI-5P alignment with bootstrap values for SSU + rbcL + COI-5P / rbcL + COI-5P / rbcL only, respec-
tively, included. Pacic Pleonosporium spp. join that lineage in rbcL + COI-5P / rbcL only analyses. Asterisks (*) indicate 100% support in all three analyses. Taxa
in bold type are new species described here, as well as those transferred to dierent genera. Scale: substitutions per site.
4CRYPTOGAMIE, ALGOLOGIE • 2024 • 45 (1)
Schneider C. W. & Saunders G. W.
Pleonosporium novae-angliae
G.W.Saunders & C.W.Schneider, sp. nov.
(Fig. 2)
HoloType (designaTed Here). — United States. Rhode Island, Fort
Wetherill, 41°28’44.8”N, 71°21’36.2”W, subtidal (6 m) on other
algae, 10.VIII.2007, G.W. Saunders & B. Clarkston, GWS005733
(holo-, UNB), GenBank: OQ561797 (COI-5P), OQ561894 (rbcL),
OQ561850 (SSU).
paraType. — United States. Massachusetts, Woods Hole, Garbage
Beach Breakwater, 41°31’30.7”N, 70°40’21.2”W, subtidal (3 m)
on Sargassum C.Agardh, 14.IV.2010, B. Clarkston, D. McDevit,
M. Bruce, A. Savoie & C. Longtin, GWS017847 (para-, UNB),
GenBank: OR336111 (rbcL-3P).
a
ddiTional
maTerial
sTudied
. — United States. Massachu-
setts, Martha’s Vineyard, Edgartown, 5.VII.1897, M. Jernegan,
P.B.-A. 342b (Herb. CWS); Connecticut, Bridgeport, Black Rock
Beach (Seabright Beach), 26.VIII.1894, I. Holden 1031 (Herb.
CWS); Fairfield, Penfield Reef, 19.VII.1896, I. Holden 1203 (Herb.
CWS); Penfield Reef near Bridgeport, VII-VIII.1897, I. Holden,
P.B.-A. 342a (Herb. CWS); Waterford, Millstone Point, Fox Island
South, 12.X.1976, C. Schneider 1310 (Herb. CWS); Waterford, Gos
-
hen Point, 5.XI.1977, C. Schneider 1874 (Herb. CWS); Groton, Bluff
Point State Park, 12.IX.1978, C. Schneider 78-16-3 (Herb. CWS).
eTymology. — Novae-angliae (Latin, genitive), for “of New Eng-
land”, its present distribution in northeastern North America.
d
isTribuTion
. — From southern Cape Cod, Massachusetts to
Connecticut and New York in Long Island Sound, United States.
descripTion
Plants epiphytic, bushy, erect to 2-6 cm tall (Fig. 2A), Redwood
red (Graf1x 2023) to purplish-red in colour, attached by basal
cells and rhizoids; relatively common descending rhizoids simple
or branched and variously adherent to, or free of, main axes and
typically produced from basal cells of branches (Fig. 2B); axes
throughout uniseriate and essentially ecorticate, indeterminate
axes with slightly overtopping branches in a weak sigmoidal
pattern, branching regularly alternate in a single plane in upper
portions, appearing pyramidal in outline (Fig. 2C); upper axial
cells of indeterminate axes 16-20 µm diam. and 18-25 µm long,
middle portions with relatively regular and alternate (slightly
spiralled) branches, mid-axial cells prominent, 35-50 µm
diam. and 112-154 µm long; indeterminate axial cells in
lower portions 125-260 µm diam. and 550-860 µm long, the
axes held together by a tangle of free rhizoids; non-sequenced
plants with tetrasporangia and octosporangia adaxially sessile
on upper branches (Fig. 2D, E), borne singly or on a series of
successive cells (Fig. 2F); subglobose to obovoidal, 35-50 µm
diam. and 50-60 µm long, including a thick wall; spermatangia
in oblong masses (Taylor 1957), cystocarps unknown.
Pleonosporium ricksearlesii
C.W.Schneider & G.W.Saunders, sp. nov.
(Fig. 3)
H
oloType
(
designaTed
Here
). — Bermuda. Somerset Island,
32°16.783’N, 64°52.788’W, on wooden dock in Ely’s Harbour,
depth 0-1 m, 30.VI.2015, C.W. Schneider & T.R. Popolizio 15-21-3
(holo-, MICH[1210917]), dried silica sample: BDA1944, GenBank:
OR336107 (COI-5P), OR336112 (rbcL).
isoTypes. — Same data as holotype (iso-, NY, UNB, Herb. CWS).
e
Tymology
. — Named for Prof. Richard Brownlee Searles, the
first author’s graduate mentor, collaborator and friend, on the occa-
sion of his 87th birthday. Joint cruises with the first author to study
mesophotic seaweeds off Bermuda aboard the R/V Seahawk in the
early 1980s initiated four decades of investigation on the macroalgal
flora of this Atlantic archipelago.
disTribuTion. — Endemic to Bermuda as currently known.
descripTion
Delicate plants lignicolous or on mud-saturated wood, bushy,
erect to 5.0 cm tall, Persian red in colour (Graf1x 2023) and
ecorticate (Fig. 3A); indeterminate axes fine with alternately
irregular branching above with corymbose and narrowly-angled
branches at apices, some with some branches overtopping the
apex (Fig. 3B); most branches simple of 15 with fewer cells or
once branched, indeterminate branches irregularly replacing
these branches; in lower portions of indeterminate axes, the
lateral branches markedly smaller than the axis that produced
them (Fig. 3C), and with most lateral branches losing all but
a few of their most proximal cells; in distal portions the axes
only slightly larger in diam. than the branches they produce;
indeterminate axial cells cylindrical and usually flared at their
proximal ends in basal portions of main axes (Fig. 3C, F, G),
95-150 µm diam. and 370-530 µm long, gradually tapering
distally to cells 20-30 µm diam. and 85-250 µm long several
segments below the apices; upper branches incurved, apical
cells slightly tapering but obtuse (Fig. 3D); tetrasporangia
adaxially sessile on upper incurved branches, borne singly or in
a series of successive cells or every other branch cell (Fig. 3E),
subglobose to obovoidal, 33-36 µm diam. and 36-48 µm
long, including a thick wall, sporangia also forming laterally
or terminally, at times clustered or in secund series, on broken
lower and regenerating lateral branches (Fig. 3F, G), some
appearing to have single-celled stalks; gametangia unknown.
DISCUSSION
When Harvey (1853: 233) first reported the “variable”
Callithamnion borreri for North America, he stated that his
specimens were “more slender and softer than the European
form…”, and he could “possibly have described them as a
new distinct species”. ree decades later, Farlow (1881: 125)
also noted that New England specimens were “always more
slender than European forms of the species”, but wrote that
“there can be almost no doubt that we have true C. borreri.”
Following suit, Taylor (1957) reported that the American
material of Pleonosporium borreri was “much more slender
than that from Europe”. Two recent collections made in
southern New England, one each from Massachusetts and
Rhode Island, morphologically appeared to be the species
identified by these and other earlier workers in the region
as P. borreri. Using rbcL, we unequivocally establish that the
5
New Pleonosporium species from the western Atlantic
CRYPTOGAMIE, ALGOLOGIE • 2024 • 45 (1)
AC
BD
E
F
fiG. 2
. — Pleonosporium novae-angliae G.W.Saunders & C.W.Schneider, sp. nov., holotype specimen (GWS005733): A, habit of type specimen; B, origins of
rhizoids (arrowheads) that will eventually loosely envelop proximal axial cells (CWS 78-16-3); C, apices of axes and branches with distichous, triangular pat-
terns (CWS 1310); D, tetrasporangium (CWS 78-16-3); E, octosporangium (CWS 78-16-3); F, adaxial tetrasporangium (arrowhead) and octosporangium (double
arrowheads) developing singly and in a series on upper lateral branches (CWS 78-16-3). Scale bars: A, 2 cm; B, C, 250 µm; D-F, 50 µm.
6CRYPTOGAMIE, ALGOLOGIE • 2024 • 45 (1)
Schneider C. W. & Saunders G. W.
North American populations are distinct from a collection
of P. borreri from Europe for which this marker has been
sequenced (Fig. 1). Indeed, the two New England specimens
were identical in their rbcL sequences but were much closer to
Bermudian P. ricksearlesii C.W.Schneider & G.W.Saunders,
sp. nov. (15 substitution, thus representing distinct species)
than they were to the European P. borreri (81 substitutions).
e New England and Bermudian populations also differed
by 62 substitutions in the COI-5P gene, again indicating
their unique status. Both species were closer to Australian
species in our phylogenetic analyses than they were to the
generitype, P. borreri, the name formerly used for the southern
New England/New York taxon (Fig. 1). erefore, on the basis
of its genetic sequences and morphological comparisons, we
describe P. novae-angliae G.W.Saunders & C.W.Schneider,
sp. nov. for our cold-temperate North American collections,
as well as those specimens historically known as P. borreri in
the western Atlantic (Harvey 1853, as Callithamnion borreri
(Smith) C.Agardh; Farlow 1881, as C. borreri; Taylor 1957;
Mathieson & Dawes 2017).
Indeterminate axes of both Pleonosporium borreri and
P. novae-angliae G.W.Saunders & C.W.Schneider, sp. nov.
produce alternately distichous branches from the distal ends
of axial cells. Near their apices, the alternately pinnate branch-
ing pattern suggests a pyramidal outline (Fig. 2C), a pattern
that can be found in other members of the Wrangeliaceae (e.g.
Compsothamnion), as well as some in the related Callitham-
niaceae (e.g. Aglaothamnion, Callithamnion, Gaillona). Both
P. borreri and P. novae-angliae G.W.Saunders & C.W.Schneider,
sp. nov. produce entangling rhizoids issued from basal cells
of lower branches that attach to other axes as well as other
plants and substrata. As noted by early workers on the New
England flora, the axes of P. novae-angliae G.W.Saunders &
C.W.Schneider, sp. nov. are on average much finer than those
of European P. borreri. Maggs & Hommersand (1993) reported
that the rhizoids of P. borreri descend and intertwine loosely
around the lowermost axial cells causing the lower axes to be
as large as 500 µm in diameter, whereas in P. novae-angliae
G.W.Saunders & C.W.Schneider, sp. nov. only a few loose
rhizoids are produced exposing the axial cells that are maxi-
mally c. 260 µm wide (Fig. 2B).
Measurements collected from the two genetic specimens of
Pleonosporium novae-angliae G.W.Saunders & C.W.Schneider,
sp. nov. reported here are consistent with those retrieved from
archival New England/New York specimens from the 1800s
to 2000 identified at the time as P. borreri. ese specimens
include P.B.-A. no. 342 listed as P. borreri with 1897 collec-
tions from both Connecticut and Massachusetts (Collins et al.
1897). As we have yet to sequence recent tetrasporangial or
octosporangial specimens, these all being collected prior to
our regular specimen processing for molecular analysis, we
tentatively assigned sporangial measurements from archival
specimens to the above description. Plenosporium borreri was
reported from the warmer, more southern waters of North
Carolina (Williams 1951), but Schneider & Searles (1991) were
unable to locate Williams’ vouchers of this species. Because of
its similarity to P. boergesenii (A.B.Joly) R.E.Norris (Schneider
1975, as Mesothamnion boergesenii Joly), Schneider & Searles
(1991) excluded P. borreri from the southeastern U.S. flora,
although Mateo-Cid et al. (2018) recently reported it from
the Atlantic coast of Mexico.
Sequences from collections of a fine, bushy filamentous
species from a wooden dock in Bermuda (field identified as
Aglaothamnion sp.) also nested the clade with P. borreri and
congeners. Prior to this study, the genus Pleonosporium was
unknown in Bermuda, but comparison with known spe-
cies in the genus showed these isolates to represent P. rick-
searlesii C.W.Schneider & G.W.Saunders, sp. nov. from
the warm temperate western Atlantic. e specimens from
Somerset, Bermuda, aligned with P. borreri, P. hirtum and
P. australicum (Womersley) G.W.Saunders & C.W.Schneider,
comb. nov., and directly with its sister species, P. novae-angliae
G.W.Saunders & C.W.Schneider, sp. nov. (Fig. 1). Pleonospo-
rium ricksearlesii C.W.Schneider & G.W.Saunders, sp. nov.
differs from P. novae-angliae G.W.Saunders & C.W.Schneider,
sp. nov. by not developing a pronounced alternately pinnate
branching pattern with a pyramidal outline in distal por-
tions. e apices of P. ricksearlesii C.W.Schneider & G.W.
Saunders, sp. nov. develop alternate branches, but these are
issued irregularly, appearing congested and not pinnately
displayed (Fig. 3B, D). e Bermuda species also has much
smaller axial cells in lower portions of the indeterminate
axes than P. novae-angliae G.W.Saunders & C.W.Schneider,
sp. nov. (95-150 µm diam. × 370-530 µm long vs 125-260 µm
diam. × 550-860 µm long) and longer upper axial cells (85-
250 µm vs 18-25 µm long). Among the known members of
the genus, P. ricksearlesii C.W.Schneider & G.W.Saunders,
sp. nov. is morphologically most similar to P. boergesenii from
North Carolina to Brazil through the Caribbean Sea (Guiry &
Guiry 2023), a species yet to be sequenced. Pleonosporium
ricksearlesii C.W.Schneider & G.W.Saunders, sp. nov. differs
in having finer cells near their bases, 95-150 µm diam. and
370-530 µm long, as compared to those of P. boergesenii,
210-325 µm diam. and 600-900 µm long (Schneider &
Searles 1991; Littler et al. 2008). Tetrasporangia of both spe-
cies develop in similar positions, but those of P. ricksearlesii
C.W.Schneider & G.W.Saunders, sp. nov. are smaller than
those of P. boergesenii, 33-36 µm diam. by 36-48 µm long vs
40-75 µm diam. by 85-160 µm long (Joly 1957, as Mesotham-
nion boergesenii A.B.Joly; Littler et al. 2008). Pleonosporium
ricksearlesii C.W.Schneider & G.W.Saunders, sp. nov. has
some similarity to the habit of P. mexicana E.Y.Dawson from
Pacific Mexico and Brazil (Dawson 1962; Oliveira Filho 1969),
but that species is strictly distichous and also has much larger
axial cells and sporangial dimensions than the new species.
e genus Pleonosporium is characterized as producing
mitotic divisions beyond the normal meiotic division in
sporangia (Maggs & Hommersand 1993). Species of the
Spongoclonieae producing sporangia would first produce
meiotic tetrasporangia before dividing sequentially again
to eight (octosporangia), 16 or 32 spores (polysporangia).
Unlike the great majority of species presently in the genus,
P. ricksearlesii C.W.Schneider & G.W.Saunders, sp. nov. is one
of just three species found to produce only tetrasporangia,
7
New Pleonosporium species from the western Atlantic
CRYPTOGAMIE, ALGOLOGIE • 2024 • 45 (1)
AB
CD
E
FG
fiG. 3. — Pleonosporium ricksearlesii C.W.Schneider & G.W.Saunders, sp. nov., holotype specimen (CWS/TRP 15-21-3, BDA1944): A, habit of type specimen;
B, apex of indeterminate axis; C, lateral branch origin from basal portion of axis; D, apex of lateral branch; E, apical portion of axis with adaxial tetrasporangia;
F, terminal tetrasporangium on lateral o lower main axis with subtending branchlet or sporangial initials; G, regenerating lateral on lower axis producing a series
of tetrasporangia. Scale bars: A, 2 cm; B, D, E, 100 µm; C, F, G, 50 µm.
8CRYPTOGAMIE, ALGOLOGIE • 2024 • 45 (1)
Schneider C. W. & Saunders G. W.
not octosporangia or polysporangia. Pleonosporium intricatum
R.E.Norris (Norris 1994) from Hawaii and P. mageshimense
(Itono) R.E.Norris from Japan (Itono 1977) are also known
to produce only tetrasporangia among the 31 currently rec-
ognized species prior to this report (Guiry & Guiry 2023).
e lack of polysporangia in P. ricksearlesii C.W.Schneider &
G.W.Saunders, sp. nov. could, however, be a collecting arti-
fact; thus, additional collections are needed to substantiate
this claim. Some species such as P. borreri (Newton 1931),
P. kobayashii Okamura (Okamura 1933) and P. novae-angliae
G.W.Saunders & C.W.Schneider, sp. nov. have plants bear-
ing both tetrasporangia as well as octoporangia on the same
individuals. Although the recent sequenced specimens used
to genetically separate P. novae-angliae G.W.Saunders &
C.W.Schneider, sp. nov. from P. borreri lacked sporangia
on their branches, archival specimens from southern New
England showed both tetrasporangia and octosporangia on
the same individuals (Fig. 2F). As early collectors cited poly-
sporangia for this species (Harvey 1853, as C. borreri; Farlow
1881, as C. borreri; Taylor 1957, as P. borreri; Mathieson &
Dawes 2017, as P. borreri), it is possible that they used the
term polysporangia for sporangia with any divisions post
meiosis. Furthermore, it could be that specimens other than
those we have seen may indeed produce them as well. Further
collections of both of the new western Atlantic species will
hopefully clarify whether these species produce any mitotic
divisions beyond meiosis, and how many spores are found
in the sporangia.
e generitype of Spongoclonium, S. conspicuum, produces
only tetrasporangia on sporophytes (Wollaston 1990). Like-
wise, some other species remaining in the genus produce only
tetrasporangia (e.g. S. fasciculatum J.Agardh, S. pastorale Laing),
while others develop tetrasporangia as well as occasional to
rare octosporangia (e.g. S. brownianum (Harvey) J.Agardh,
S. caribaeum, S. yagii (Yamada) H.-S.Kim & I.K.Lee). Each
of the species varies as to the presence of (and levels of) cor-
tication on axial cells in lower portions of indeterminate axes.
Whether the number of cell divisions in sporangia becomes a
useful generic distinction for Pleonoporium and Spongoclonium
remains to be seen after additional samples of both become
available and more species are genetically tested and phyloge-
netically sorted. We are thus reluctant at this time to declare
that Pleonosporium (Nägeli 1862) is a junior synonym of Spon-
goclonium (Sonder 1855). Despite their sister association in
our phylogenies (Fig. 1), they are relatively distantly related,
and the possibility that these should remain as distinct gen-
era in Spongoclonieae requires analysis of other Australasian
species in Spongoclonium, as well as Pleonosporium spp. that
exclusively produce tetrasporangia. Nevertheless, we are assured
that L. hirtum is solidly aligned in the clade with Pleonosporium
and thus subsume Lophothamnion (Agardh 1892) under it.
We have uncovered six species of Pleonosporium in the
Northeast Pacific, two included in our phylogeny here (Fig. 1),
which fall well outside the nested Pleonosporium/Spongoclo-
nium clade. ey require further taxonomic work to clarify
their current ‘orphaned’ status, as well as to assign specific
epithets to the genetic groups.
Acknowledgements
We acknowledge Discovery Grants from the Natural Sci-
ences and Engineering Research Council of Canada with
infrastructure support from the Canada Foundation for
Innovation and the New Brunswick Innovation Foundation
that funded the molecular work at UNB. Field support for
GWS was provided in part through the Australian Biological
Resources Study. GWS thanks the many individuals in his
lab for field assistance, and Cody Brooks, Dan McDevit and
Tanya Moore for generating the new sequence data used in
this study. For the field work in Bermuda, we acknowledge
National Science Foundation DEB grant 1120688 to CWS,
and thank ea Popolizio for her assistance in collecting and
Roger Simmons of the Bermuda Aquarium who provided
logistical support in Bermuda. is is contribution no. 296
to the Bermuda Biodiversity Project (BBP) of the Bermuda
Natural History Museum, Department of Environment and
Natural Resources.
REFERENCES
agardH J. g. — nalecta algologica Lunds Universitets Års-
Skrift
c
Hoi
H.-g., K
rafT
g. T., K
im
H.-s., g
uiry
m. d. & s
aun
-
ders
g. W. — hylogenetic relationships among lineages
of the eramiaceae eramiales hodophyta based on nuclear
small subunit r sequence data Journal of Phycology
httpsdoiorgjx
collins f. s., Holden i. & seTcHell W. a. — Phycotheca
Boreali-Americana (Exsiccata), Algae of North America ascicle
os alden assachusetts
d
aWson
e. y. — arine red algae of acific exico art
eramiales eramiaceae elesseriaceae Allan Hancock Pacific
Expeditions
de Toni g. b. — Sylloge algarum omnium hucusque cogni-
tarum ol Florideae ectio umptibus auctoris atavii
adua httpswwwbiodiversitylibrary
orgpage
farloW W. g. — Marine Algae from New England and
Adjacent Coast eport of the ish ommission for
overnment rinting ffice ashington p httpswww
biodiversitylibraryorgpage
grafx — shades of red color palette vailable from
httpsgrafxcomshadesofredcolorpalettehexrgbcode
searched on anuary
g
uiry
m. d. & g
uiry
g. m. — lgaease worldwide
electronic publication ational niversity of reland alway
vailable from httpwwwalgaebaseorg accessed on anu
ary
Harvey W. H. — Nereis boreali-americana art ho
dospermeae Smithsonian Contributions to Knowledge
H
arvey
W. H. & H
ooKer
J. d. — lgae in
H
ooKer
ed e botany of the Antarctic voyage of H.M. dis-
covery ships Erebus and Terror in the Years 1839-1843: under the
command of Captain Sir James Clark Ross ol Flora Antarctica
art otany of ord ucklands roup and ampbells sland
eeve ondon
Huisman J. m. — Algae of Australia. Marine Benthic Algae
of North-Western Australia ol Red Algae
ublishing anberra elbourne p
iTono H. — Studies on the ceramiaceous algae (Rhodophyta)
from southern parts of Japan ramer aduz p ibliotheca
hycologia
9
New Pleonosporium species from the western Atlantic
CRYPTOGAMIE, ALGOLOGIE • 2024 • 45 (1)
J
oly
a. b. — ontribuição ao conhecimento da flora ficológica
marinha da aía de antos e arredores Boletim de Faculdade de
Filosofia, Ciências e Letras, Universidade de São Paulo, Botânica
K
ylin
H. — Die Gattungen der Rhodophyceen leerups
und p
l
aing
r. m. — n the ew ealand species of erami
aceae Transactions and Proceedings of the New Zealand Institute
l
iTTler
d. s., l
iTTler
m. m. & H
anisaK
m. d. — Submersed
Plants of the Indian River Lagoon: A Floristic Inventory and Field
Guide ffhore raphics nc ashington p
m
aggs
c. a. & H
ommersand
m. H. — Seaweeds of the
British Isles ol Rhodophyta art eramiales e atural
istory useum ublications ondon p
maTeo-cid l. e., mendoza-gonzález a. c., norris J. n. &
g
arcía
-l
ópez
d. y. — taxonomic account of species in
the tribe pongoclonieae eramiaceae eramiales hodophyta
reported from tlantic and acific exico Phytotaxa
httpsdoiorgphytotaxa
maTHieson a. c. & daWes c. J. — Seaweeds of the North-
west Atlantic niversity of assachusetts ress mherst p
n
ägeli
c. — eiträge zur morphologie und systema
tik des eramiaceae Sitzungsberichte der Königlichen Bayerischen
Akademie der Wissenschaften zu München
neWTon l. — A Handbook of British Seaweeds rustees of
the ritish useum ondon p
n
orris
r. e. — otes on some awaiian eramiaceae
hodophyceae including two new species Japanese Journal of
Phycology
oKamura K. — Icones of Japanese algae +
oliveira filHo e. c. — lgas marinhas do sul do estado
do spirito anto rasil – eramiales Boletim de Faculdade
de Filosofia, Ciências e Letras, Universidade de São Paulo
ot
saunders g. W. & mcdeviT d. c. — ethods for
barcoding photosynthetic protists emphasizing the macroalgae
and diatoms Methods in Molecular Biology https
doiorg_
saunders g. W. & moore T. e. — efinements for the
amplification and sequencing of red algal barcode and
edo phylogenetic markers a summary of current primers
profiles and strategies Algae httpsdoiorg
algae
scHneider c. W. — orth arolina marine algae
ome eramiales hodophyta including a new species of
Dipterosiphonia Journal of Phycology httpsdoi
orgjtbx
s
cHneider
c. W. — n annotated checklist and bibli
ography of the marine macroalgae of the ermuda islands
Nova Hedwigia httpsdoiorg
scHneider c. W. & searles r. b. — Seaweeds of the South-
eastern United States. Cape Hatteras to Cape Canaveral uke
niversity ress urham p
soares l. p., guimarães s. m. p. b., fuJii m. T., yonesHigue-
valenTin y., baTisTa m. g. s. & yoKoya n. s. —
allus ontogeny morphology and molecular phylogeny of
Madagascaria atlantica sp nov ompsopogonophyceae ho
dophyta a diminutive crustose species uncovered in the tlan
tic cean Aquatic Botany httpsdoiorgj
aquabot
s
onder
o. g. — lantae uellerianae lgae annis
et collectae Linnaea
sTamaTaKis a. — x version a tool for phylogenetic
analyses and postanalysis of large phylogenies Bioinformatics
httpsdoiorgbioinformaticsbtu
T
aylor
W. r. — Marine Algae of the Northeastern Coast
of North America
nd
ed niversity of ichigan ress nn
rbor p
T
Hiers
b. m. continuously updated — ndex erbariorum
lobal irectory of ublic erbaria and ssociated taff ew
ork otanical ardens irtual erbarium ew ork vail
able from httpsweetgumnybgorgscienceih
W
illiams
l. g. — lgae from the black rocks in p
earse
a. s. &
Williams l. g. eds e biota of the reefs off the arolinas
Journal of the Elisha Mitchell Scientific Society
WollasTon e. m. — ecognition of the genera Spongoclo-
nium onder and Lasiothalia arvey eramiaceae hodophyta
in southern ustralia Botanica Marina httpsdoi
orgbotm
Womersley H. b. s. & WollasTon e. m. — ribe pon
goclonieae chmitz in Womersley ed
e Marine Benthic Flora of Southern Australia art era
miales – eramiaceae asyaceae tate erbarium of outh
ustralia ichmond
Wynne m. J. — checklist of benthic marine algae of the
tropical and subtropical western tlantic second revision Nova
Hedwigia eiheft
W
ynne
m. J. — hecklist of benthic marine algae of the
tropical and subtropical western tlantic fifth revision Nova
Hedwigia eiheft
Submitted on 22 August 2023;
accepted on 27 October 2023;
published on 17 January 2024.
10 CRYPTOGAMIE, ALGOLOGIE • 2024 • 45 (1)
Schneider C. W. & Saunders G. W.
appenDix 1. — Collection details and GenBank accession numbers for specimens included in this study.
Name Voucher Collection SSU COI-5P rbcL
Dasythamniella
dasyura (Harvey)
Womersley
GWS000335
Australia, VIC, Warrnambool, 15.XI.1997, G. Kraft
EU718686 – –
GWS015175
Australia, TAS, Burying Ground Point, 21.I.2010,
G. Saunders & K. Dixon
–HM917616 KU381976
Haloplegma sp. 2WA GWS025420 Australia, WA, Pt. Peron, 13.XI.2010,
G. Saunders & K. Dixon
–KU381919 KU381989
Pleonosporium
australicum
(Womersley)
G.W.Saunders &
C.W.Schneider,
comb. nov.
GWS015077 Australia, TAS, George Town, Windmill Point,
19.I.2010, G. Saunders & K. Dixon
–OR336105 OR336109
GWS015200
Australia, TAS, Burying Ground Point, 21.I.2010,
G. Saunders & K. Dixon
–OR336106 –
Pleonosporium borreri
(Smith) Nägeli
PD2941 Spain, Galicia, P. Díaz-Tapia, sourced from
GenBank
_ _ MK814701
Pleonosporium hirtum
(Hooker f. & Harvey)
Laing
GWS001468
Australia, TAS, Bicheno, 25.XI.2002, G. Saunders
–HM915913 KU381977
Pleonosporium
novae-angliae
G.W.Saunders &
C.W.Schneider,
sp. nov. (holotype)
GWS005733 United States of America, RI, Fort Wetherill,
10.VIII.2007, G. Saunders & B. Clarkston
OQ561850 OQ561797 OQ561894
GWS017847 United States of America, MA, Woods Hole,
Garbage Beach Breakwater, 14.IV.2010,
B. Clarkston, D. McDevit, M. Bruce,
A. Savoie & C. Longtin
– – OR336111
(rbcL-3P only)
Pleonosporium
ricksearlesii
C.W.Schneider &
G.W.Saunders,
sp. nov. (holotype)
CWS/TRP 15-21-3
(BDA1944)
Bermuda, Somerset Island, Ely’s Harbour,
30.VI.2015, C. Schneider & T. Popolizio
–OR336107 OR336112
Pleonosporium sp.
3GWS
GWS021133 Canada, BC, Haida Gwaii, Masset Inlet,
Cowley Islands, 9.VI.2010, G. Saunders &
K. Dixon
–HQ919416 KU381986
Pleonosporium cf.
squarrosum Kylin
GWS031006 Canada, BC, Gwaii Haanas, Tanu Island, Tanu,
14.VI.2012, G. Saunders & K. Dixon
OQ561854 KU381855 KU381982
Plumaria plumosa
(Hudson) Kuntze
CH029 France, Cap Gris-Nez, 21.VIII.1997, H-G. Choi AF488382 – –
GWS009779 Canada, NS, Brier Island Western Light
(exposed rocky site), 29.V.2008, H. Kucera &
S. Hamsher
–HM917150 KU381993
Ptilota asplenioides
(Esper) C.Agardh
CH801 Japan, Nemuro, 30.VI.1995, H-G. Choi EU718696 – –
GWS035795 Canada, BC, Gwaii Haanas, SGang Gwaay
(rocks to NW), 18.VIII.2013, G. Saunders &
K. Dixon
–KU381943 KU381991
Spermothamnion
repens (Dillwyn)
Magnus
GWS014712 United States of America, MA, Plymouth,
White Horse Beach, 12.IV.2010,
B. Clarkston, D. McDevit, M. Bruce,
A. Savoie & C. Longtin
OQ561858 HM919017 OQ561899
Spongoclonium
conspicuum Sonder
GWS000303
Australia, VIC, Warrnambool, 13.IX.1997, G. Kraft
EU718705 –OR336110
APPENDIX
