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Kallymenia crouaniorum (Kallymeniaceae,Rhodophyta), a new red algal species from theLaminaria hyperborea understorey communityMarine Robuchonab, Line Le Galla, Delphine Geyc, Myriam Valerob & Alba Vergésd

a UMR7205 Institut Systématique, Evolution, Biodiversité, CNRS, EPHE, MNHN, UPMC,Muséum National d’Histoire Naturelle, case postale N° 39, 57 rue Cuvier, 75231 Cedex 05Paris, Franceb CNRS, UPMC, UMI 3614 Evolutionary Biology and Ecology of Algae, CNRS, SorbonneUniversités, UPMC Univ. Paris 06, Pontificia Universidad Catolica de Chile, UniversidadAustral de Chile, Station Biologique de Roscoff, CS 90074, 29688 Roscoff, Francec UMS2700 Outils et Méthodes de la Systématique Intégrative, CNRS, MNHN, Service deSystématique moléculaire, Muséum National d’Histoire Naturelle, 75231 cedex 05 Paris,Franced Universitat de Girona, Department of Environmental Sciences, Faculty of Sciences,17071 Girona, SpainPublished online: 18 Nov 2014.

To cite this article: Marine Robuchon, Line Le Gall, Delphine Gey, Myriam Valero & Alba Vergés (2014) Kallymeniacrouaniorum (Kallymeniaceae, Rhodophyta), a new red algal species from the Laminaria hyperborea understoreycommunity, European Journal of Phycology, 49:4, 493-507, DOI: 10.1080/09670262.2014.971348

To link to this article: http://dx.doi.org/10.1080/09670262.2014.971348

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Kallymenia crouaniorum (Kallymeniaceae, Rhodophyta), a newred algal species from the Laminaria hyperborea understoreycommunity

MARINE ROBUCHON1,2, LINE LEGALL1, DELPHINE GEY3, MYRIAMVALERO2 ANDALBAVERGÉS4

1UMR7205 Institut Systématique, Evolution, Biodiversité, CNRS, EPHE, MNHN, UPMC, Muséum National d’HistoireNaturelle, case postale N° 39, 57 rue Cuvier, 75231 Cedex 05 Paris, France2CNRS, UPMC, UMI 3614 Evolutionary Biology and Ecology of Algae, CNRS, Sorbonne Universités, UPMC Univ. Paris 06,Pontificia Universidad Catolica de Chile, Universidad Austral de Chile, Station Biologique de Roscoff, CS 90074, 29688Roscoff, France3UMS2700 Outils et Méthodes de la Systématique Intégrative, CNRS, MNHN, Service de Systématique moléculaire, MuséumNational d’Histoire Naturelle, 75231 cedex 05 Paris, France4Universitat de Girona, Department of Environmental Sciences, Faculty of Sciences, 17071 Girona, Spain

(Received 28 February 2014; revised 19 June 2014; accepted 10 July 2014)

In this paper we describe Kallymenia crouaniorum Vergés & Le Gall, sp. nov. (Kallymeniaceae), a new marine red alga fromthe north-eastern Atlantic Ocean. rbcL and LSU sequences of this species, previously misidentified in the field as Kallymeniareniformis, diverged from those of other Kallymenia species by at least 7.5% and 5.2%, respectively. Kallymenia crouaniorumalso has a set of distinctive vegetative and reproductive characteristics, including a deeply lacerate frond, a short stipe, dentatemargins, large cortical cells up to 110 μm in diameter, highly refractive stellate medullary cells with arms up to 1000 μm inlength, and a monocarpogonial branch system. Molecular phylogenies inferred from rbcL and LSU data indicated, albeit withweak support, that this new species is a sister taxon of a lineage encompassing the generitype K. reniformis, as well as mostspecies of Kallymenia included in the phylogenetic analysis. The main morphological characters that delineate monocarpo-gonial Kallymenia species are presented. Moreover, after reviewing the literature and several herbarium specimens, we foundin the Weber-van Bosse Herbarium a specimen collected at Roscoff in August 1894 with the anatomical characters of thespecies described here, confirming that this newly described species has in fact been overlooked and is not a recentintroduction.

Key words: Gigartinales, Kallymenia crouaniorum, Kallymenia reniformis, Kallymeniaceae, north-eastern Atlantic, reproduc-tion, Rhodophyta, taxonomy

Introduction

The macroalgal flora of the north-eastern Atlantic hasbeen closely studied since the end of the 18th centuryand has long been considered one of the best charac-terized floras in the world (see introduction in Dixon& Irvine, 1977). Nonetheless, the advent of molecularsystematics has demonstrated that the vegetative andreproductive characteristics traditionally used for spe-cies delimitation are not always consistent with theresults of molecular phylogenetic approaches becauseof both convergence leading to cryptic diversity, andphenotypic plasticity causing variation in morpholo-gical characters (e.g. Saunders, 2005; Le Gall &Saunders, 2010; De Clerck et al., 2013). Reliableidentification of seaweeds, based solely on morpholo-gical characters, is therefore a challenging task.

Moreover, in the north-eastern Atlantic, subtidal com-munities have received little attention compared withintertidal communities (Smale et al., 2013). We there-fore undertook, along the north-eastern Atlantic coastof France, a survey of the understorey algal flora offorests of Laminaria hyperborea (Gunnerus) Foslie,an emblematic subtidal species on European coastsfrom Norway to Portugal. Seaweeds were initiallyidentified by gross morphology in the field and sub-sequently by DNA sequences of the mitochondrialgene COI (cox1) and/or the nuclear gene LSU.Kallymenia reniformis (Turner) J. Agardh is a con-spicuous but variable species that is abundant in L.hyperborea kelp forests (Bunker et al., 2010) and isthe only member of the genus currently recorded forthe English Channel and British Isles (Guiry & Guiry,2014).

Correspondence to: Line Le Gall. E-mail: legall@mnhn.fr

Eur. J. Phycol. (2014), 49(4): 493–507

ISSN 0967-0262 (print)/ISSN 1469-4433 (online)/14/040493-507 © 2014 British Phycological Societyhttp://dx.doi.org/10.1080/09670262.2014.971348

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During dives in the Iroise Sea, at Roscoff andaround the north-western Cotentin peninsula, wefound some algae resembling Kallymenia reniformis.However, they had a cartilaginous texture and stria-tions near the base, whereas most K. reniformis feelssmooth and supple. Although we suspected that thesespecimens were not likely to be genuine K. reniformison the basis of their anatomy, our first attempts toobtain molecular evidence were unsuccessful, asCOI failed to amplify. The use of alternative markers(LSU and rbcL) enabled us to confirm that we hadindeed uncovered an additional Kallymenia speciesfor the north-eastern Atlantic. We then set out toinvestigate whether this species had previously beendescribed.

The genus Kallymenia J. Agardh 1842(Kallymeniaceae, Rhodophyta), which currentlyincludes about 40 species (Guiry & Guiry, 2014), iswidely distributed in both hemispheres. These spe-cies are identified on the basis of a variety of mor-phological features including: (a) the shape of thefrond; (b) the presence/absence of a stipe; (c) theshape, size and disposition of cortical cells; (d) theshape and size of the medullary stellate cells and thelength of the arms of these cells; (e) the presence ofmono- or polycarpogonial branch systems; (f) thepresence of uni- or multinucleate supporting andsubsidiary cells; (g) the mode of formation of goni-moblast initials and (h) the diameter of the gonimo-blast (Agardh, 1842; Norris, 1957, 1964; Abbott,1968; Codomier 1971; Womersley & Norris, 1971;Womersley, 1994; Vergés & Rodríguez-Prieto,2006a, 2006b).

In the present manuscript, we describe the vegeta-tive and reproductive features of Kallymenia sp. fromthe algal understorey of Laminaria hyperborea andinfer its phylogenetic affinities using LSU and rbcLsequence data. We reviewed whether this taxon hadpreviously been described, and examined herbariafrom the 19th century to rule out the possibility thatthe presence of this taxon in the north-eastern Atlanticresults from a recent introduction. In light of theseanalyses, we concluded that we have uncovered a newspecies and here name it Kallymenia crouaniorumVergés & Le Gall.

Materials and methods

Sample collection and herbarium material examined

Nine specimens of Kallymenia were collected by scuba div-ing between 2 and 15 m depth at sites along the coasts ofBrittany and Normandy (France) between 2008 and 2011(Table 1) during a survey of the understorey flora of theLaminaria hyperborea canopy. Samples were cleaned, frozenat −20ºC and then lyophilized for molecular analyses.Additional samples were collected as part of a biodiversityassessment of the French algal flora and dried as herbariumspecimens housed at the Herbarium of the Natural History

Museum of Paris (PC). For molecular analyses, samples werecleaned, dried and preserved in silica gel.

In addition to our collections, all specimens referred to asKallymenia spp. housed in the following European Herbariawere examined to detect misidentifications of this species inthe NE Atlantic: Natural History Museum (BM), Marinariumde Concarneau (CO), National University of Ireland, Galway(GALW) and Nationaal Herbarium Nederland, Leiden (L).Some specimens collected at Oviedo, Spain, and held in thepersonal Herbarium of A. Vergés (SVP) were also examined.Herbarium abbreviations follow Thiers (2014).

Anatomy and morphology

Anatomical and reproductive features were observed insquash preparations, using 10%HCl mixed with 1% acidifiedaniline blue, and in sections made with a razor blade andsubsequently stained in a 1% acidified aniline-blue/distilledwater solution. Habit views were reproduced with a HPOfficejet 6500A scanner (Hewlett-Packard, Palo Alto, CA,USA); photomicrographs were taken with a MRc5 (Zeiss,Berlin, Germany) attached to an Axio Imager A2 microscope(Zeiss, Berlin, Germany).

Molecular sequencing and analysis

Specimens from which we obtained sequences are listed inTable 1, along with collection details, voucher numbers andGenBank accession numbers for rbcL and LSU sequences.DNA extraction, PCR and sequencing reactions were per-formed following the same protocol as described in Vergéset al. (2014).

Purification and sequencing reactions were performed byGenoscope (www.genoscope.fr, Evry, France). Forward andreverse electropherograms were edited and assembled withthe software Codoncode (Dedham, MA). GenBank wassearched on 6 January 2014 for Kallymeniaceae sequences;all were downloaded before sorting rbcL and LSUsequences. For LSU, only sequences longer than 2200 bpwere selected for phylogenetic analysis using the perl scriptfasta_get_seq_length.pl and Fastabox. Outgroup sequenceswere selected from GenBank representatives of theDumontiaceae, Polyidaceae and Gainiaceae, which arefamilies closely related to the Kallymeniaceae. Multiplesequence alignments were constructed for both markersusing SeaView version 4 (Gouy et al., 2010). Genetic dis-tances were computed using the neighbour-joining algorithmin SeaView. Identical haplotypes were removed prior to ana-lysis leading to an LSU alignment including 80 taxa and anrbcL alignment of 67 taxa. Phylogenetic analyses of rbcL andLSU alignments were conducted by Bayesian inference usingMrBayes version 3.2.1 (Ronquist et al., 2012). ML anddistance bootstrap values were calculated using RAxMLversion 8.0.0 (Stamatakis et al., 2008) and SeaView,respectively.

Analyses were run with four heated Monte-Carlo Markovchains for 2 000 000 generations. Output trees and data weresampled every 100 generations. Appropriate burn-in for eachrun was determined by plotting the overall likelihood againstgenerations prior to estimating the posterior probability dis-tribution. In all analyses, likelihood values were stable afterthe first 200 000 generations. Final results were based on the

M. Robuchon et al. 494

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Tab

le1.

Dataforspecim

ensof

Kallymenia

crouaniorumexam

ined

here.

Taxo

nHerbarium

#LSU

rbcL

Depth

Locality

Region

Date

Leg.

K.croua

niorum

*PC01

7106

6KM89

6872

KM89

6874

−1m

Lam

paul

IleSégal

Brittany

12Aug

.200

9L.L

eGall,J.Utgé,Y.T

urpin

K.croua

niorum

PC01

5230

7KM89

6873

-−6m

Dielette

Normandy

26May

2008

L.L

eGall

K.croua

niorum

PC01

7108

5KM89

6871

-−2m

Les

Belveniou

sBrittany

10Aug

.200

9Y.G

ladu

,A.B

esnier,L

.LeGall

K.croua

niorum

PC01

7108

6KM98

7388

-−2m

Les

Belveniou

sBrittany

10Aug

.200

9Y.G

ladu

,A.B

esnier,L

.LeGall

K.croua

niorum

RMAR13

18KJ961

365

KM89

6877

−4m

StM

athieu

Brittany

10March

2011

L.L

eGall,Y.T

urpin,

K.croua

niorum

RMAR00

49KJ961

361

-−4m

Santec

Brittany

25March

2011

Y.F

ontana

K.croua

niorum

RMAR1133

KJ961

364

-−3m

Rospects

Brittany

14March

2011

L.L

eGall,Y.T

urpin

K.croua

niorum

RMAR22

34KJ961

363

-−4m

Santec

Brittany

28Feb.2

012

M.R

obucho

nK.croua

niorum

RMAR33

75KJ961

360

-−11

mLinious

Brittany

16March

2011

L.L

eGall,Y.T

urpin

Herbarium

BM

K.croua

niorum

(asK.renifo

rmis)

BM

0008

0505

9-

-Islesof

Scilly

BritishIsles

20Sept.18

99E.G

eorge

Herbarium

GALW

K.croua

niorum

(asKallymenia

sp.)

GALW

1488

--

Islesof

Scilly

BritishIsles

7July19

83C.M

aggs

K.croua

niorum

(asKallymenia

sp.)

GALW

1489

--

Islesof

Scilly

BritishIsles

4July

1983

C.M

aggs

K.croua

niorum

(asKallymenia

sp.)

GALW

1493

--

Islesof

Scilly

BritishIsles

4July

1983

C.M

aggs

Herbarium

L-

K.croua

niorum

(asK.renifo

rmis)

L06

5329

4-

-N/A

Roscoff

Brittany

21Aug

.189

4A.W

eber-Van

Bosse

K.croua

niorum

(asK.renifo

rmis)

L06

5326

5-

-−3m

Ríade

Arosa

Spain

1July19

63M.D

onze

K.croua

niorum

(asK.renifo

rmis)

L06

5326

6-

-N/A

Ríade

Arosa

Galicia

5July19

65U.W

.Oosterhoff

SVPPersonal

herbarium

A.V

ergés

K.croua

niorum

SVPOV05

42-

--15m

Artedo

Asturias

11July

1997

N/A

K.croua

niorum

SVPOV05

44-

--15m

Artedo

Asturias

11July

1997

N/A

K.croua

niorum

SVPCANT82

0-

--4

mIslade

Mou

ro,S

antand

erCantabria

16Aug

.200

9N.S

ánchez

&C.P

eteiro

*indicatestheho

lotype

design

ated

here.LSU

andrbcL

correspo

ndto

GenBankaccessionnu

mbers;BM,Natural

History

Museum;CO,M

arinarium

deCon

carneau;

GALW

,NationalUniversity

ofIreland,

Galway;L,

NationaalHerbarium

Nederland

,Leiden.

Kallymenia crouaniorum sp. nov. 495

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pooled samples from the stationary phase of the two inde-pendent runs.

Results and discussion

GROSS MORPHOLOGY: Plants erect, up to 22 cm long, 21cm wide and 110–320 µm thick, shortly stipitate,fixed to the substratum by a small discoid holdfast.Near the base, some ridges present, very strikingunderwater. Young fronds either entirely or partiallylobed (Figs 1–3), pink to red-brown in colourand membranous; old thalli deeply lobed, lacerate(Figs 4–5), cartilaginous and reddish, fertile femalespecimens becoming brownish, with groupedgonimoblasts.

Underwater, the gross morphology of the taxonstudied here was distinct from any other Rhodophytain the north-eastern Atlantic. Despite its similarity toKallymenia reniformis, the fan-shaped frond withconspicuous ridges at its base, as well as the cartilagi-nous texture of the frond, led to initial doubts as totheir conspecificity.

VEGETATIVE MORPHOLOGY: Multiaxial, with a compactcortex composed of several (up to 5) layers of cellsdecreasing in size towards the surface and a laxmedulla of slender filaments intermixed with a net-work of stellate cells (Fig. 6). Cortical cells are joinedand form networks parallel to the frond surface; innercortical cells are also connected to medullary cells andmedullary filaments. Inner cortical cells are stellate,

hyaline, with the cell body up to 110 µm in diameter;mid-cortical layers composed of cells that are slightlystellate, irregular in shape or ovoid, hyaline or brown-ish when containing floridean starch, cells near thecentre of the blade having a cell body up to 100 µm indiameter and the cell body 25–50 µm in diameter forcells located away from the blade centre; outer corticalcells polyhedral or irregular in shape, rose to red incolour, 6–10 µm in diameter, and compactly arranged(Fig. 7). Medulla formed by very conspicuous stellatecells, highly refractive (Figs 8–11), with a cell body 30(–60) µm in diameter, and arms extending to 800 (–1000) µm connected to the medullary filaments or tothe inner stellate cortical cells. Medullary filamentsnumerous, composed of one to several cells, simple orbranched, hyaline or brownish, and 2–10 µm indiameter.

We observed a set of specific vegetative characterssuggesting that this species belongs to the genusKallymenia: foliose frond, cortex of several layersof cells decreasing in size outwards, and filamentousmedulla with stellate cells. However, the size andshape of the stellate medullary cells distinguish thistaxon from Kallymenia reniformis (arm length ofstellate medullary cells < 400 μm in K. reniformisand up to 1000 μm in the species described here).Moreover, these two taxa can be differentiated by thelength of their inner cortical cells (< 60 μm in K.reniformis and to 110 μm in the species studiedherein).

Figs 1–5. Kallymenia crouaniorum, sp. nov. Habit. Fig. 1. Holotype (PC0171066). Figs 2–3. Sterile specimens (PC0152307,RMAR0049). Figs 4–5. Tetrasporophytes (PC0171086, PC0171085). Scale bar = 5 cm.

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REPRODUCTIVE MORPHOLOGY: Plants non-procarpic.Carpogonial branch systems monocarpogonial, arisingfrom inner cortical cells and developing through thecortex. They consist of a supporting cell, rounded or

ovoid when young (Fig. 12), but lobed when mature(Figs 13–16), that supports up to six subsidiary cellswhich are rounded at first (Figs 6–7), but becomeenlarged and lobed (Figs 8–9), and a three-celled

Figs 6–11. Kallymenia crouaniorum, sp. nov. Vegetative anatomy. Fig. 6. Cross-section of the thallus (SVP OV0544). Fig. 7. Cortexin surface view (PC0171085). Figs 8–11. Different types of stellate cells present in the inner cortex and in the medulla. Mid-corticalcells (mcc) with or without short arms and large volume, inner cortical cells (icc) with arms developing in all directions, and giantmedullary stellate cells (Figs 10, 11; msc) in a squash preparation (PC0171066). Scale bar = 100 µm (Fig. 6), 20 µm (Fig. 7), 50 µm(Figs 8–11).

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carpogonial branch (Figs 13–16). The two basal cellsof the carpogonial branch are ovoid and the carpogo-nium is prolonged by a basally twisted trichogyne(Figs 14–16). After fertilization, the supporting cellfuses with subsidiary cells forming a stellate fusioncell (Figs 17–18), up to 180 µm in diameter, anddevelops digitate protuberances that become connect-ing filaments. Connecting filaments are hyaline, andare sometimes divided near the fusion cell (Fig. 18),and septate at the base, measuring up to 2 mm in lengthand 2 µm in width, with a swollen apical extremity.Auxiliary cell branch systems are similar in shape toyoung carpogonial branches, measuring up to 40 µm indiameter, with a rounded supporting cell acting as the

auxiliary cell, which supports up to six rounded sub-sidiary cells (Fig. 12). The connecting filamentattaches to the supporting cell of the auxiliary cellbranch system, and the gonimoblast filamentsare initiated from the connecting filament. Protrudingcystocarps, grouped in the middle and upper parts ofthe frond, grow in the direction of the medulla,760–2000 µm in diameter (Fig. 19), and are non-ostio-late, as the carpospores are released through a pore.Carpospores are 10–16 µm in diameter.Spermatangia unknown. Tetrasporangia scattered inthe outer cortex, elongate-ovoid and cruciatelyor irregularly divided, 18–24 µm in diameter(Figs 20–23).

Figs 12–18. Kallymenia crouaniorum, sp. nov. Reproductive structures. Fig. 12. Young carpogonial branch system or auxiliary cellsystem with the supporting cell and five subsidiary cells (sc: supporting cell) (PC0171066). Figs 13–16. Monocarpogonial branchsystems (cbr1, first carpogonial branch cell; cbr2, second carpogonial branch cell; cp, carpogonium; sc, supporting cell; subc,subsidiary cell; t, trichogyne). Figs 17–18. Fusion cells developing connecting filament (arrows) (Figs 13–15: PC0171066; Figs 15–16: SVP OV0542; Fig. 17: SVP OV0544; Fig. 18: SVP OV0542). Scale bar = 10 µm (Fig. 12), 20 µm (Figs 13–17), 40 µm.

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The reproductive morphology of the genusKallymenia features a carpogonial cell system com-posed of a supporting cell giving rise to several sub-sidiary cells, with one or more three-celled carpogonialbranches arising on the supporting cell, a fusion cellformed after fertilization, involving the supporting celland the subsidiary cells, connecting filaments arisingfrom the fusion cell, a gonimoblast consisting ofnumerous carposporangia intermixed with filamentswithin the medulla, and tetrasporangia lying withinthe outer cortex, scattered, cruciate, zonate or irregu-larly divided (Norris, 1957; Hommersand & Ott 1970;Womersley, 1994; Vergés, 2001; Vergés & Rodríguez-Prieto, 2006a, 2006b). All these features were clearlyobserved in the taxon studied here.

Whether the female reproductive structures aremonocarpogonial or polycarpogonial is one of themain taxonomic features for differentiating the speciesof the genus. It separates the species studied here,which is monocarpogonial, from the type speciesKallymenia reniformis, which is polycarpogonial(Norris, 1957; Hommersand & Ott, 1970; Vergés,2001).

PHYLOGENETIC AFFINITIES: Despite repeated attempts,we failed to amplify the most universally used barcodemarker, i.e. the mitochondrial gene coding cyto-chrome oxidase 1, in the species studied here.Therefore, phylogenetic affinities were inferred fromboth LSU and rbcL data, two markers for whichcomprehensive datasets are available in GenBank.

Figs 19–23. Kallymenia crouaniorum, sp. nov. Reproductive structures. Fig. 19.Cross-section of a carposporophyte (SVPOV0542).Fig. 20. Cross-section with tetrasporangia (arrow) immersed in the outer cortex (PC0171085). Figs 21–23. Different patterns oftetrasporangial division (PC0171085). Scale bar = 100 µm (Fig. 19), 40 µm (Fig. 20), 10 µm (Figs 21–23).

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Both phylogenies (Figs 24–25) indicated, albeit withweak support, that the species studied here is the sistertaxon of the lineage containing most species ofKallymenia including the generitype Kallymenia reni-formis. These results indicate that the taxon studiedherein is not closely related to K. reniformis.Furthermore, the level of divergence of this taxonfrom the other Kallymenia species suggests that itshould perhaps even be recognized at the genericlevel. However, in our phylogenies presented heresome species currently assigned to the genus

Kallymenia (i.e. K. tasmanica for the LSU phylogeny,K. cribosa for the rbcL phylogeny andK. lacerata andK requienii for both phylogenies) are not resolved inthe lineage containing the generitype. A revised cir-cumscription of the genus Kallymenia is thereforeneeded, which is beyond the scope of this study. Wetherefore tentatively assign the species studied hereinto the genus Kallymenia. Interestingly, this is thesecond new species of Kallymenia, together with K.ercegovicii, to be described recently in Europeanwaters (Vergés et al., 2014).

Fig. 24. Phylogenetic tree inferred from Bayesian analysis of the LSU dataset. Strongly supported nodes (Bayesian posteriorprobability =1 and ML and distance bootstrap values > 94) are indicated in bold. Otherwise, only Bayesian posterior probabilities>0.75 are indicated.

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TAXONOMIC DISCUSSION: Kallymenia reniformis is theonly species of Kallymenia known to inhabit theBritish Isles and the English Channel (Feldmann,1954; Hardy & Guiry, 2003). To assess whether thespecies studied here had previously been reportedunder a synonym or misidentified as another speciesof the genus Kallymenia, we examined Kallymeniavouchers from European herbaria (BM, GALW, Land PC) that are repositories for a broad range ofhistorical macroalgal samples from the north-easternAtlantic. Given that several of our specimens hadbeen collected in Finistère (Brittany), we thoroughlyexamined the Kallymenia specimens in the herbariumof the brothers Pierre-Louis and Hippolyte-Marie

Crouan (CO), but currently located in Paris (PC) fordigitization). In two folders labelled Callymenia reni-formis (Turn.) J. Ag., we found several specimensannotated ‘nob.’ (Dumontia pseudo-reniformis,Halymenia pseudo-reniformis, Halymenia ulvoidea).All specimens were carefully examined and their anat-omy found to match that of K. reniformis rather thanthat of the taxon described here. However, in BM,GALW and L, we identified specimens conspecificwith the taxon studied herein. These specimens were(mis)identified as K. reniformis (BM 00805059,L0653265, L0653266, L0653294; Figs 26, 28), orwere left as unidentified species of Kallymenia(GALW 1488, GALW 1489, GALW 1493).

Fig. 25. Phylogenetic tree inferred from Bayesian analysis of the rbcL dataset. Bayesian posterior probabilities, ML and distancebootstrap values, respectively, are given for each node. % indicates bootstrap of 100.

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The specimen (L0653294) located in the Weber-van Bosse Herbarium, housed in Leiden (L), alsoundoubtedly belongs to the same species. This speci-men is a fertile female gametophyte collected in 1894at Roscoff, France, which was likely to have beencollected by Anna Antoinette Weber-van Bosse her-self, as she visited France that year (Woelkerling &Lamy, 1995). The presence of this species in Brittanyat the end of the 19th century proves that this entityhas been overlooked for more than a century, possiblyhaving been confused with Kallymenia reniformis.Furthermore, this finding suggests that the speciesstudied herein is autochthonous to the north-easternAtlantic because most introductions are more recent(e.g. Pérez-Cirera et al., 1997; Maggs & Stegenga,1999).

A common Mediterranean member of the genusKallymenia, Kallymenia requienii, is the species

most similar to the taxon studied here. Our phylo-genetic analysis (Figs 24–25) shows a clear distinc-tion between these two species and reveals that theyare genetically distant. Despite their morphologicalsimilarities, there is no doubt that they belong totwo different taxa. Comparing K. requienii (Vergés,2001) with our new species revealed some signifi-cant differences (Table 2). Firstly, K. requienii issessile, and has a small (5 × 8 cm) and slightlylobed frond that is clearly differentiated from thestipitate, much larger (22 × 21 cm), deeply lobedand lacerate blade of the taxon studied here; thethickness of the blade in cross-section and the dia-meter of the inner cortical cells are both smaller inK. requienii than in the taxon studied here (cross-sections to 240 μm vs. < 55 μm, respectively; innercortical cells to 320 μm vs. < 110 μm, respectively),although the stellate medullary cells are the same

Figs 26–28. Kallymenia crouaniorum, sp. nov. Specimens found in L and BM herbaria misidentified asK. reniformis. Fig. 26. Fertilefemale gametophyte collected in 1894 at Roscoff, France (L0653294). Fig. 27. Sterile individual collected in Galicia, Spain(L653265). Fig. 28. Tetrasporophyte collected in 1899 at Porth Loo, Isles of Scilly (BM000805059).

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Tab

le2.

Com

parisonof

themaintaxo

nomiccharacteristicsof

themon

ocarpo

gonialspeciesof

Kallymenia.

Lam

ina

Stip

eThallu

ssize

Cross

section

No.of

cortex

layers

Innercortical

cells

Medullary

stellate

cells

Num

berof

subsidiary

cells

intheauxiliary

cellbranch

system

Gonim

oblast

Carposporangia

Tetrasporangia

Distribution

References

K.crassiuscula

Okamura

Round,o

vateor

oblong,

mostly

with

outlobes

buto

ften

split.M

argin

entire

Present

10–2

5×10

–25cm

390–

550µm

5–6

Rounded

Ganglionic,arms80–

130µm

long

7n.d.

n.d.

n.d.

Japan,

Arabian

Sea

Okamura1934

;

Wynne

2000

K.cribrosaHarvey

Sim

ple,perforate.Margin

smooth

Occasionally

present

30×30

cm200–

500

(−1000)µm

3-4

Ovoid

to

polygonalor

spherical

Light

staining,(40

–)

90–160

µm;arm

s

rarely

longer

than

cellbody

3–5

400–600µm

(10–)14–2

0

µm

20–2

8×

17–1

9µm

WandS

Australia

Wom

ersley

&

Norris

1971

;

Wom

ersley

1994

K.p

erforata

J.Agardh

Undulatingto

plaited,

somew

hatu

mbilicate,

waved,p

erforatedand

lobed.

Marginentire

Absent

30–6

0×30

–60cm

1140

µm

1–2

Rounded

n.d.

6–11

n.d.

n.d.

n.d.

Japan,

Ceylon,

Tropics

Abbott&

McD

ermid

2002

K.requienii

(J.A

gardh)

J.Agardh

Entireor

irregularlylobed

Absent

1–5×2–8cm

110–

240µm

4–5

Stellate,<

55µm

Darklystaining,body

cell<50

µm

in

diam

eter,arm

s<

1000

µm

long

4320–480µm

12–1

6µm

20–2

6×

15–1

8µm

Mediterranean

Sea

Codom

ier

1971

;

Vergés2001

K.rubra

Wom

ersley

&Norris

Irregularlylobedor

dissected,

with

some

smallexcrescences.

Marginerose-

undulated

Present

4–12

cmhigh

150–

400µm

3–4

Ovoid

or

trapezoidal*

Moderatelystaining,

refractiv

e,arms<

200µm

*

3–4

n.d.

n.d.

n.d.

SAustralia

Wom

ersley

&

Norris

1971

;

Wom

ersley

1994

K.sessilis

Okamura

Frond

lobedandundulate

with

anentiremargin

andabroadheart-

shaped

base

Absent

Ø30

cmhigh

130–

160µm

3Stellate

Absent

n.d.

150–200µm

10×10

µm

18×20

µm

Japan, Haw

aiian

Islands

Okamura1934

;

K.spinosa

Wom

ersley

&

R.E.N

orris

Gradually

tobroadly

cuneateandcovered

with

branched

spines.

Upper

margin

irregularlylobed

Present

3–7×3–6cm

200–

350µm

3–4

Ovoid

or

trapezoidal*

Staining

3n.d.

n.d.

30–3

8×20–

26µm

SAustralia

Wom

ersley

&

Norris

1971

;

Wom

ersley

1994

K.tasmanicaHarvey

With

marginaland

overlapped

lobes

Present

5–30

cm250–

500µm

3–4

Irregular*

Darklystaining

refractiv

ecells

n.d.

500–1000

µm

12×18

µm

18–3

5×11–

16µm

SAustralia

Wom

ersley

&

Norris

1971

;

Wom

ersley

1994

K.thompsoniiAbbott

&McD

ermid

Inrosettesof

2-3blades.

Marginperforated

and

undulate

Absent

<10

cmbroad

140–

250µm

2Trapezoidal,1

5–

39×30–8

0

µm

Non

observed

n.d.

160–200µm

13×20

µm

13×20

µm

Haw

aiian

Islands

Abbott&

McD

ermid

2002

K.crouaniorum

sp.

nov.

Entireor

slightly

lobed

whenyoung,

lacerate

whenadult.Margin

dentate

Present

22×21

cm110–

320µm

5Stellate,<

110

µm

Highlyrefractiv

e

cells,b

odycell<

60µm,arm

s<

1000

µm

long

<6

750–2000

µm

10–1

6µm

18–2

4µm

N-E

Atlantic

Vergés2001

as

K.requienii

subsp.

atlantica;

Thisstudy

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Tab

le3.

Com

parisonbetweenK.croua

niorum

andKallymenia

specieswith

unkn

owncarpog

onialb

ranchsystem

s.

Lam

ina

Stip

eThallu

ssize

(cm)

Cross

section

(µm)

No.

ofcortex

layers

Stellatecells

(µm)

Gonim

oblast

diam

eter

(µm)

Tetrasporangia

(µm)

Distribution

References

K.b

aldw

inii

E.Y.D

awson

Palmatelylacerate,w

ithvein-like

thickeningsin

laceratesegm

ents

Present

13–2

4×28

cm200–

270µm

n.d.

40–5

0µm

500µm

n.d.

Gulfof

California

Daw

son1966

K.b

erggrenii

J.Agardh

Entire,lobed,

laciniate,or

laciniate-lobate,

oftenproliferatingin

spathulateto

lanceolatelobes

Occasionally

present

30cm

broad

n.d.

n.d.

n.d.

1000

µm

n.d.

New

Zealand

J.Agardh1876

;Chapm

an&

Parkinson

1974

K.b

leckii

E.Y.D

awson

Auriculate,irregularlylaceratelylobed,with

fewscatteredproliferations.F

orked

veinsnear

thebase

Present

13–2

4×28

cmn.d.

n.d.

15–2

5(40)

µm

600µm

n.d.

Gulfof

California

Daw

son1966

K.b

rachycystid

eaJ.Agardh

Irregularmarginwith

afewlobes

Present

23×15

cm60

–80µm

325

–30µm

n.d.

n.d.

New

South

Wales,

Australia

Wom

ersley

&Norris1971

K.callopyllo

ides

Okamura&

Segaw

a

Initially

linear,then

dividedinto

manymain

branches

irregularlyinto

subpalmato-

dichotom

oussegm

ents

Present

4–5×5–

7cm

n.d.

3-4

n.d.

n.d.

n.d.

Japan

Okamura1935

K.chilensisLevring

With

acuneatebase

deeply

dividedinto

segm

ents

Absent

17cm

125–

175µm

1-2

n.d.

120–

150µm

n.d.

Chile

Levring

1960

K.g

uaym

asensis

E.Y.D

awson

Flabellate,d

eeplydividedinto

manybroad,

roundedsegm

ents

Present

5–7cm

high

60–7

0(130)µ

mn.d.

n.d.

n.d.

n.d.

Gulfof

California

Daw

son1944

K.lacinifo

liaLevring

Laciniate,w

ithlaceratemargins

10cm

high

200–

300µm

2–3

n.d.

n.d.

n.d.

Antarctica

Levring

1944

K.limminghei

Montagne

Pseudopeltateor

fan-shaped.M

argins

smooth

Present

1×2cm

130µm

2–3

n.d.

n.d.

n.d.

Western

Caribbean

Littler&

Littler

2000

K.m

orelii(M

ontagne

&Millardet)

Børgesen

Lobed

with

numerousproliferations

from

theedge

Present

n.d.

n.d.

3–4

n.d.

n.d.

n.d.

I.Mauritiu

sandI.

Réunion

Børgesen1951

K.n

orrisiiH

ollenberg

&I.A.A

bbott

Spathulateto

auriculatewhenyoungand

with

ruffled

lobeswhenmature

Occasionally

present

>30

cmhigh

n.d.

n.d.

Giant,4

000-5000

µm

<3000

µm

15×20

–25

California

Abbott1

968

K.o

ligonem

aYam

ada

Fan-shaped,

slightly

perforated.M

argin

lobed,

slightly

undulate.

Present

4×6cm

125µm

n.d.

n.d.

1000

µm

n.d.

Japan

Yam

ada1941

K.p

acifica

Kylin

Sim

ple,circular

whenyoung,

anddissected

bylobeswhenmature

Present

240–

300µm

4–5

Highlyrefractiv

e3000

–4000µm

California,

Philip

pines

Abbott1

968;

Silv

aetal.

1996

K.sagam

iana

Yam

ada

Irregularlylobedor

deeply

split

into

segm

entsor

undulate.M

arginwith

spinousprotuberances

Absent

20cm

broad

1200

–1400µm

5–8

n.d.

n.d.

Irregularlyshaped

anddivided

Japan

Yam

ada1938

K.schmitziD

eToni

Flabellate,w

ithroundedlobes

n.d.

16cm

160–

190µm

n.d.

n.d.

n.d.

n.d.

Arctic

Sea?

DeTo

ni1897

K.stip

itata

Okamura

Oblong,

gradually

expandingto

roundish,

obovateor

transversely

expanded

mem

brane,sometim

eslobed.

Present

30×20

–30cm

80–1

40µm

2–3

n.d.

n.d.

n.d.

Japan

Okamura1934

K.spathulata(J.

Agardh)

Codom

ier

exP.G.P

arkinson

Elliptical,w

ithnumerousspathulate

proliferations

allo

verthethallus

Absent

30×12

cm150–

300µm

5Ganglionic,yello

wstaining,2

5µm

n.d.

n.d.

Mediterranean

Sea

Codom

ier1971

;Vergés2001

K.veleroaeE.Y.

Daw

son

Entirewhenyoungbutsplits

anddevelops

laceratedsegm

ents

Absent

<4cm

high

80–9

0µm

n.d.

n.d.

n.d.

n.d.

Gulfof

California

Daw

son1944

K.crouaniorum

,sp.

nov.

Entireor

slightly

lobedwhenyoung,

laceratewith

dentatemarginwhenadult

Present

22×21

cm110–

320µm

5Hightly

refractiv

ecells,

body

cell<60

µm,arm

s<1000

µm

long

750–

2000

µm

Cruciate,18

–24

NEAtlantic

Thisstudy

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shape, size and colour. Both taxa are monocarpogo-nial; however, the female reproductive structuresand the carposporophyte of K. requienii are smallerthan those of the Atlantic taxon, as is the diameterof a mature carpogonial cell system (85 μm in K.requienii and up to 140 μm in the taxon studiedhere) and the diameter of the carposporophyte (<480 μm in K. requienii and <2000 μm in our newspecies) (Codomier, 1971; Vergés, 2001; Vergés &Rodríguez-Prieto, 2006a). It is noteworthy that K.requienii has been reported in the north-easternAtlantic from Galicia (Bárbara et al., 2005), butexamination of the Galician specimens located inLeiden (L0653265 and L0653266) indicate thatthese were probably misidentified and belong tothe species described here. Furthermore, the recordof K. requienii in Brittany made by ‘Associationpour la découverte du monde sous-marin’(ADMS, Castric-Fey et al., 2001), in light of ourresults, is more likely to be our species.

Finally, to ensure that the new entity had not beendescribed from outside European waters, we reviewedthe characters of Kallymenia species with a monocar-pogonial cell system (Table 2) or unknown femalereproductive structures (Table 3). Some significantdifferences in morphology and anatomy of both vege-tative and reproductive structures distinguish the spe-cies studied here. Although frond morphology in thegenus Kallymenia is subject to plasticity, it has oftenbeen used for species delineation. In particular, thepresence or absence of a stipe, lobes, perforations,spines or excrescences are considered distinctive char-acteristics at the species level. The main morphologi-cal features distinguishing the species of Kallymeniaare summarized in Tables 2 and 3.

Taxonomic conclusions

In conclusion, after rejecting all potential assign-ments of the taxon here studied to a previouslydescribed species of Kallymenia, we consider that itdiffers from other Kallymenia species mainly infrond shape, the diameter of the inner cortical cells,the conspicuous and refractive stellate medullarycells with very long arms, a monocarpogonial branchsystem and carposporophyte size. In light of thesefeatures, along with the phylogenies that place thetaxon studied herein as sister to the lineage contain-ing most Kallymenia species including the generi-type, we concluded that this taxon is a newKallymenia species that inhabits the north-easternAtlantic, occurring with the type species of thegenus, K. reniformis. We propose to name itKallymenia crouaniorum in honour of the Crouanbrothers, because looking through their herbarium,it appears that they had suspected the presence ofmore than one entity in the genus Kallymenia inBrittany.

Kallymenia crouaniorumVergés& LeGall, sp. nov.(Figs 1–23)

DIAGNOSIS: Thallus erect, foliose, up to 20 cm high, 15cm broad and 320 μm thick. Fronds lobed when youngand deeply lobed or laciniate when adult. Inner cortexof hyaline stellate cells, with arms up to 100 μm long.Medullary cells very conspicuous and highly refrac-tive, with the cell body up to 60 μm in diameterand arms extending in all directions, up to 1000 μmlong. Monocarpogonial with a three-celled carpogo-nial branch and a lobed supporting cell bearing up toeight rounded subsidiary cells, often lobed.Non-procarpic; auxiliary cell system formed by arounded auxiliary cell and supporting up to sixrounded subsidiary cells. Mature carposporophyte to2000 μm in diameter. Spermatangia unknown.Tetrasporangia cruciately or irregularly divided andup to 26 μm in diameter.

HOLOTYPE: PC0171066 (Fig. 1). Female gametophyte.

TYPE LOCALITY: Collected in Lampaul, Ile Ségal,France, at 2 m depth, 12 August 2009 by L. Le Gall,J. Utgé and Y. Turpin.

ETYMOLOGY: Named in honour of the Crouan brothersfor their outstanding contribution to the knowledge ofthe macroalgal flora of the north-eastern Atlantic andfor their interest in the genus Kallymenia.

Acknowledgements

We thank the curators of the National University ofIreland (GALW), and the National HerbariumNederland (L) for their assistance in loaning voucherspecimens. We thank Professor Juliet Brodie andJoanna Wilbraham for their assistance during AlbaVergés’ visit to the Herbarium of the Natural HistoryMuseum London (BM) funded by the Synthesys Grantshe received in 2009 to revise the Kallymenia specimenshoused at BM. Line Le Gall is grateful to all those whocontributed to the temporary move of the Crouan collec-tion, housed at the Marinarium of Concarneau, to theNational Herbarium of Paris, for digitization prior to itsreturn to Concarneau. DNA sequencing was carried outat the CNRS-UMS 2700 in Service de SystématiqueMoléculaire, MNHN acknowledges funds provided byAction Transversale du Muséum National d’HistoireNaturelle (Taxonomie moléculaire: DNA Barcode etgestion durable des collections) as well as the‘Bibliothèque du vivant’ (INRA-MNHN-INEE-CNRS)and the ‘Parc Naturel Marin d’Iroise’ (conventionCNRS-UPMC-PNMI N°LS64816) projects. We areextremely grateful to the ‘Service Mer et Observation’at the Station Biologique de Roscoff and the SMEL team(Synergie, Mer et Littoral) as well as divers of the ParcNaturel Marin d’Iroise and Yves Gladu and Jose Utgéfor contributing to specimen collection. Finally, wewould like to thank Bruno Dennetière for his insightsregarding historical collections and the International

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Code of Botanical Nomenclature, as well as AlexandraDavies and Carolyn Engel-Gautier for linguisticassistance.

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