Research Article

Algae 2018, 33(3): 243-267 https://doi.org/10.4490/algae.2018.33.8.29 Open Access

An investigation of members of the tribe Ceramieae (Ceramiaceae, Rhodophyta) occurring on both the Mediterranean and Atlantic shores of Morocco

Mustapha Hassoun1,*, Michael J. Wynne2, Hanaa Moussa1, Ghizlane Salhi1, Hanaa Zbakh1, Hassane Riadi1 and Mohamed Kazzaz1 1Department of Biology, Faculty of Sciences, Abdelmalek Essaâdi University, 93000, BP. 2121, M’Hannech II, Tétouan, Morocco 2Department of Ecology and Evolutionary Biology and Herbarium, University of Michigan, Ann Arbor, MI 48109, USA

A taxonomic study was recently carried out on species of the tribe Ceramieae (Ceramiaceae, Rhodophyta), following an evaluation of previously published records and on the basis of field and laboratory investigations. In Morocco, the tribe is represented by 5 genera: Ceramium (21 taxa at specific and infraspecific levels), Gayliella (3 species), and by one species each of Centroceras, Corallophila and Microcladia. Among these, there are five new records for Morocco:Cen - troceras gasparrinii, Ceramium botryocarpum, Ceramium cingulatum, Ceramium echionotum var. mediterraneum, and Gayliella taylorii. The report of C. echionotum var. mediterraneum from the Atlantic coast of Morocco is one of the rare records from outside the Mediterranean. Ceramium ciliatum var. robustum and Ceramium codii are recorded for the first time from the Atlantic coast of Morocco. Centroceras clavulatum is excluded from Moroccan flora having been mis- identified for C. gasparrinii. This paper summarizes the taxonomic characters of these species with images and presents a key for their identification. This report is the first detailed record of the species of the tribe Ceramieae for Morocco. As a result, the total number of taxa at both specific and infraspecific levels accepted in the tribe Ceramieae for Morocco, under current taxonomy and nomenclature, is 27.

Key Words: Centroceras; Ceramieae; Ceramium; Corallophila; Gayliella; Microcladia; Morocco

INTRODUCTION

The red algal tribe Ceramieae C. Agardh ex Greville and the developmental morphology and arrangement of is a highly diverse group in terms of number of taxa at the spermatangia, carposporophyte, and tetrasporangia specific and infraspecific level (more than over 275 spe- (Hommersand 1963, Norris 1993, Cho et al. 2008). On the cies according to Guiry and Guiry 2018). The tribe is Moroccan coast, the tribe Ceramieae is represented by 5 represented in all marine habitats worldwide and is genera: Ceramium Roth, Centroceras Kützing, Coralloph- comprised of 12 genera separated on the basis of thallus ila Weber-van Bosse, Gayliella T. O. Cho, L. J. McIvor et S. habit; shape, number, and arrangement of cortical cells; M. Boo, and Microcladia Greville.

This is an Open Access article distributed under the Received April 29, 2018, Accepted August 29, 2018 terms of the Creative Commons Attribution Non-Com- Corresponding Author mercial License (http://creativecommons.org/licenses/by-nc/3.0/) which * permits unrestricted non-commercial use, distribution, and reproduction E-mail: [email protected] in any medium, provided the original work is properly cited. Tel: +212-678-99-74-09, Fax: +212-539-99-45-00

Copyright © 2018 The Korean Society of Phycology 243 http://e-algae.org pISSN: 1226-2617 eISSN: 2093-0860 Algae 2018, 33(3): 243-267

The red algal genus Ceramium, containing more than De Toni (a genus also belonging to the Ceramieae) in hav- half of all species of the tribe, is one of the largest red al- ing rectangular cortical cells regularly arranged in lon- gal genera. It is common worldwide, with approximately gitudinal rows. However, Corallophila is distinguished 200 currently recognized species (Guiry and Guiry 2018). from all genera of the tribe Ceramieae in having four Representatives occur in nearly all eulittoral or shallow cortical initials produced from each periaxial cell (Norris subtidal habitats (Maggs et al. 2002, De Barros-Barreto 1993, Abbott 1999, Cho et al. 2000). Corallophila is repre- et al. 2006). Ceramium species are usually distinguished sented in Morocco by a single species. by such features as the arrangement of cortical fila- Microcladia, the fifth genus of the tribe Ceramieae ments, the developmental morphology of tetrasporan- that occurs in Morocco (Benhissoune et al. 2003), is also gia, and the shape of apices (Hommersand 1963, Itono represented in Morocco by a single species. The genus 1972, Womersley 1978, Ballantine 1990). Thalli are com- was established by Greville (1830) on the basis of Fucus pletely or incompletely corticated and consist mostly of glandulosus Solander ex Turner and distinguished from branched terete axes that are both prostrate and erect other genera of the tribe in having alternate-distichous or erect only. This genus is easily recognizable because branching, forwardly directed cortical filaments, and a of periaxial cells forming rings at the nodes of the axial continuous surface layer of relatively small, angular cells filaments that give rise to a strict pattern of acropetal (Maggs and Hommersand 1993, Cho et al. 2008). and basipetal cortical filaments (Womersley 1978, Norris The present investigation summarizes the taxonomic 1993, Millar 2002). characters of the species of the tribe Ceramieae that oc- Cho et al. (2008) revised the Ceramium flaccidumcom - cur in Morocco. A key for their identification with illus- plex using both morphological observations and mo- trations is presented. Furthermore, the following five taxa lecular techniques and erected the new genus Gayliella, are reported for the first time from Morocco:Centroceras with five known species assigned to that genus. Gayliella gasparrinii (Meneghini) Kützing, Ceramium botryocar- differs from Ceramium in having three cortical initials pum A. W. Griffiths ex Harvey, Ceramium cingulatum per periaxial cell, of which the basipetal one is produced Weber-van Bosse, Ceramium echionotum var. mediterra- by horizontal division; alternate branching pattern; and neum Mazoyer, and Gayliella taylorii (E. Y. Dawson) T. O. unicellular rhizoids produced only from periaxial cells Cho & S. M. Boo. (Cho et al. 2008). Rhizoidal development is an important feature for distinguishing genera within this tribe. As in Gayliella, the rhizoids in Centroceras arise from periaxial MATERIALS AND METHODS cells only, and both genera share the character of three cortical filaments per periaxial cell (Hommersand 1963, All specimens examined in this study were collected Boo and Lee 1985, Norris 1993, Cho et al. 2008). However, from different localities on the Atlantic and Mediterra- Centroceras differs from most Ceramieae in that sper- nean coasts of Morocco. The study was carried out in the matangia are produced terminally on branched mono- period 2013-2017, in the upper subtidal (-0.5-1 m depth) siphonous filaments that arise from the upper ends of and low intertidal of wave exposed rocky shores. Studies the periaxial cells; rhizoids are cut off from periaxial cells were carried out on samples preserved in 5% formalin- only; cortical cells are angular and arranged in more or seawater solution; sections were made by hand with a less straight rows parallel to the axis (Hommersand 1963). razor blade. When necessary, material was stained with Development of the cortical filaments has been accepted 1% aqueous aniline blue and preserved on glass slides in as one of the important features for recognizing species Karo corn syrup. Voucher specimens were deposited in in the genus Centroceras as well as in the tribe Ceramieae the Phycological Herbarium of the Phycology and Mycol- (Womersley 1978, Won et al. 2009). ogy Laboratory, Faculty of Sciences, Abdelmalek Essaâdi Norris (1993) has transferred several species previous- University, Tetouan, Morocco [= HTET] (Supplementary ly described as Centroceras to Corallophila. Both of these Table S1). Photomicrographs were taken with an Olym- genera are characterized by aligned quadrangular to rect- pus camera XC50 coupled to Olympus Bx43 microscope angular cortical cells covering the internodes. According (Olympus, Tokyo, Japan). For nomenclatural purposes to Weber-van Bosse (1923), Corallophila is similar to Ce- the following taxonomic databases were used: Index No- ramium but it can be distinguished from Ceramium in minum Algarum (2018) and AlgaeBase (Guiry and Guiry having tetrasporangia in stichidia and from Reinboldiella 2018).

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RESULTS AND DISCUSSION tics for distinguishing genera within this tribe (Table 1) (Hommersand 1963, Womersley 1978, Boo and Lee 1985, As mentioned above, on the Moroccan coast the tribe Boo and Yoon 1993, Norris 1993, Cho et al. 2008, Won et Ceramieae is represented by 5 genera reported since the al. 2009). earlier inventories of Kazzaz and Riadi (2000) followed by that of Benhissoune et al. (2003) reviewing the Ceramia- Ceramium les Oltmanns. They are Ceramium, Centroceras, Coral- lophila, Gayliella, and Microcladia. Recently, Hassoun et Unlike the majority of the genera in the Ceramiales, al. (2016) added two species of Ceramium, and five taxa no single reproductive feature is diagnostic of the genus are added in the present study. As a result, the total num- Ceramium and, in fact within the genus itself, only tet- ber of species and varieties in the tribe Ceramieae for rasporangial features are sometimes useful as taxonomic Morocco, under current taxonomy and nomenclature, is characters, the male and female reproductive structures 27. being essentially uniform throughout. The tribe Ceramieae is distinguished from other tribes There are 22 taxa of Ceramium that occur in Morocco; in the Ceramiaceae by the cortication of all axes arising among these, three new records added in this study: Ce- nodally, closing completely or leaving a clear gap over ramium botryocarpum, C. cingulatum, and C. echiono- the internodes; elongate determinate ramuli absent; tet- tum var. mediterraneum. rasporangia from periaxial or cortical cells (Norris 1993, Womersley 1998). Key to species and varieties of Ceramium Branching pattern, cortication of main axes, develop- 1a. Cortical bands with spines ------2 ment of the cortical filaments, rhizoidal development 1b. Cortical bands without spines ------6 and tetrasporangial features are important characteris- 2a. Spines unicellular ------3

Table 1. A comparison of genera of the tribe Ceramieae in Morocco Ceramium Centroceras Corallophila Gayliella Microcladia Cortication Incompletely or Completely corti- Mostly or completely Incompletely corti- Completely corticate completely corti- cate corticated cate cated Branching pattern Pseudo-sub-dichot- Usually dichoto- Unbranched or Alternate Alternate-distichous omous or irregu- mous pseudodichoto- larly branched mous Growth of cortical Acropetal and Mostly basipetal Mostly basipetal Two acropetal and Acropetal cells basipetal one basipetal Corticating 3-5 per periaxial cell 3 per periaxial cell 4 per periaxial cell 3 per periaxial cell 4 per periaxial cell filaments or cells Inner cortical cells Well-developed Absent Developed at nodes Absent Well-developed along axis along axis Rhizoids Multicelullar cut off Multicellular, pro- Unicellular cut from Unicellular, elon- Multicellular, simple from periaxial and duced from peri- periaxial and inner gate, produced or branched; pro- cortical cells axial cells only cortical cells from periaxial cells duced from cortical cells Origin of From outer cortical From monosi- From cortical cells From cortical cells From outer cortical spermatangia cells phonous filaments cells borne on periaxial cells Tetrasporangial From inner corti- From periaxial cells On stichidia or From only periaxial Arising initially from features cal cells and / or regular branches, cells and fully cov- periaxial cells and periaxial cells from periaxial cells, ered with cortical then from cortical occasionally from cells cells or from corti- cortical cells cal cells only Cystocarps With involucral With involucral Without involucral With involucral With involucral branches branches branches branches branches References Dixon (1960), Hom- Hommersand Weber-van Bosse Cho et al. (2008) Maggs and Hom- mersand (1963), (1963), Won et al. (1923), Norris mersand (1993) Boo and Lee (1994) (2009), Schneider (1993), Cho et al. et al. (2015) (2000)

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2b. Spines multicellular ------4 11b. Periaxial cells typically 8, rarely 9; branching approx- 3a. Main axes up to 300 μm in diameter, incompletely or imately dichotomous every 8-13 node; branches dif- completely corticated; periaxial cells 8-9; branching ferentiated in tendrils; pluricellular cortex ------pseudodichotomous every 8-14 node; tetrasporan------C. virgatum var. implexocontortum gia formed on adaxial side, 1-2 per node ------12a. Thallus rarely branched or never branched ------13 ------C. echionotum var. echionotum 12b. Thallus branched ------14 3b. Main axes up to 150 μm in diameter, incompletely 13a. Periaxial cells 4; extensive prostrate axis bearing corticated; periaxial cells 6-7; tetrasporangia im- short erect axes; apices are straight and unbranched; mersed, formed in groups, in whorls of 1-5 per node tetrasporangia unilaterally, one to two per node, ------C. echionotum var. mediterraneum strongly protruding, partially covered by cortical 4a. Spines occur singly, 3-4-celled, conspicuous, basal filaments ------C. codii cell of spines 0.7-1 longer than broad, slightly pig- 13b. Periaxial cell 7-8; with prostrate and erect axes, un- mented; main axes usually completely corticated; branched; tetrasporangia whorled and protruding branching pseudodichotomous every 8-12 node ------C. cingulatum ------C. gaditanum 14a. Branching at small intervals, less than 7 segments 4b. Spines formed in whorls ------5 ------15 5a. Spines whorls of 5-6, 3-celled, conspicuous, basal 14b. Branching at longer intervals, more than 7 segments cell of spines 1.5-3 long than broad, non-pigmented; ------17 periaxial cells 6-7; main axes incompletely corticated 15a. Periaxial cells typically 6; branching is regularly al------C. ciliatum var. ciliatum ternate every 2nd node; apices straight to little in- 5b. Spines whorls of 6-8; multicellular, up to 7(-8)-celled; curved; adventitious branches absent; tetrasporan- periaxial cells 8-9; thalli are much branched, much gia formed singly and / or in group, developing in more robust ------C. ciliatum var. robustum the plane of branching, completely naked ------6a. Axes and branches completely corticated or incom------C. callipterum pletely on the basal segments only ------7 15b. Periaxial cells typically 8; branching at intervals of 6b. Axes and branches incompletely corticated through- 4-7 segments ------16 out ------12 16a. Branching regularly pseudodichotomous; little 7a. Branching regular, alternate / pseudo-dichotomous, spaced nodes; apices tightly inrolled ------every 4-9 node; periaxial cells 6-7; apices strongly ------C. siliquosum var. siliquosum inrolled; tetrasporangia formed in groups, in whorls 16b. Branching irregularly dichotomous; long spaced at each node, immersed ------C. pallidum nodes; gland cells present, apices tightly inrolled 7b. Branching irregular ------8 with gland cells ---- C. siliquosum var. lophophorum 8a. Extensive prostrate axes present; adventitious bran­ 17a. Apices divergent and divaricate, straight or incurved ches abundant; periaxial cells 6-7, branching ex- but not strongly inrolled ------18 tremely irregular every 12-17 node ------17b. Apices strongly inrolled ------19 ------C. botryocarpum 18a. Periaxial cells 5-6; branching fairly regularly dichot- 8b. Prostrate axes absent ------9 omous every 6-12 node; many forked adventitious 9a. Cortication complete except in the basal segments; branches, inserted nearly perpendicularly; apices thalli with marked swelling after 3 or 4 basal seg- always divergent and divaricate (never incurved); ments; periaxial cells typically 9; without prostrate tetrasporangia partly covered by cortical cells ------axes, rarely branched; solitary and straight apex; tet------C. cornutum rasporangia whorled and immersed ----- C. giacconei 18b. Periaxial cells typically 5; branching pseudodichoto- 9b. Axes and branches completely corticated throughout mous every 6-17 node; apices straight or incurved; ------10 tetrasporangia entirely naked, in a ring around the 10a. Apices strongly inrolled, periaxial cells 7-9; branch- middle of each node; gland cells absent ------ing pseudodichotomous every 9-15 node; tetraspo------C. deslongchampsii rangia in whorls ------C. secundatum 19a. Tetrasporangia formed singly, rarely more than two 10b. Apices straight or slightly incurved ------11 per segment, on adaxial side of nodes; periaxial cells 11a. Periaxial cells 6-7(-8); branching extremely irregular 6-7; tightly inrolled apices; branching pseudodi- every 10-20 node ------C. virgatum var. virgatum chotomous every 8-13 node; gland cells present; ad-

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ventitious branches frequent ------C. diaphanum Among species that have multicellular spines, C. gadi- 19b. Tetrasporangia formed in rows around nodes ---- 20 tanum is mainly distinguished by its usually completely 20a. Periaxial cells 9-10; regularly dichotomous at inter- corticated axes (Fig. 2A & B). Some authors (e.g., Maggs val of 9-14 segments; apice incurved; extensive cor- and Hommersand 1993, Secilla 2012) indicated that the tex in basipetal direction ------C. circinatum spines in this species are typically one per segment and 20b. Periaxial cells 6-8; branching pseudodichotomous of 3-4 cells, but it is worth mentioning that C. gaditanum every 6-9 node; apices strongly inrolled to form for- may develop several spines per segment, short, sparse cipate tips; basipetal cells absent; pseudoperiaxial and inconspicuous in the older parts of the thallus (Fig. cells present; gland cells absent; tetrasporangia at 2C), whereas at the apices and young portions, the spines most four, unilateral, abaxial, but have the tendency are typically one per segment, pigmented and conspicu- to form whorls ------C. tenerrimum ous (Fig. 2D). According to Skage et al. (2005), three species groups Ceramium shuttleworthianum (Kützing) Rabenhorst, are often recognized in Ceramium. One group can devel- a species not occurring in Morocco but widely distribut- op fully corticated internodes; species within this group ed in the north-eastern Atlantic Ocean (e.g., Spain, Por- are characterized by their ability to form cortication that tugal), also has multicellular spines formed usually one completely covers the internodes. In Morocco, six fully per segment, but occasionally a number of spines occur, corticated non-spinose taxa of Ceramium are currently forming a partial or complete whorl according to Dixon recognized. The species of the second group are charac- (1960). However, in C. shuttleworthianum the axes are in- terized by ecorticate internodes and represented by ten completely corticated, and each of its nodes consists of 4 taxa in Morocco. The third group is characterized by cor- periaxial cells (5-6 periaxial cells in C. gaditanum). More- tical spines and is represented by five taxa in Morocco. over, C. gaditanum is the only species with multicellular spines that is completely corticated. Spinose species of Ceramium Ceramium ciliatum, one of the most commonly re- ported species in Morocco, is represented by two variet- It is generally accepted that the presence or produc- ies, C. ciliatum var. ciliatum and C. ciliatum var. robus- tion of spines is a distinctive and defining specific char- tum (Gómez Garreta et al. 2001, Benhissoune et al. 2003). acter (Norris 1993, 2014, Womersley 1998). In Morocco, The var. ciliatum has 3-celled spines that are formed in there are five taxa of Ceramium that have cortical bands whorls of 5-6 and has 6-7 periaxial cells, with pseudodi- with spines: C. echionotum J. Agardh var. echionotum, chotomous branching from every 9-13 nodes and with C. echionotum var. mediterraneum Mazoyer, C. ciliatum strongly inrolled apices (Fig. 3A-E) (Maggs and Hommer- (J. Ellis) Ducluzeau var. ciliatum, C. ciliatum var. robus- sand 1993, Secilla 2012, Rodríguez-Prieto et al. 2013). C. tum (J. Agardh) Mazoyer, and C. gaditanum (Clemente) ciliatum var. robustum, however, has 8-9 periaxial cells Cremades. Among these species, C. echionotum is the and spines up to 8 cells, borne in whorls of 6-8; branch- only one that has unicellular spines, developed near the ing relatively dichotomous, fastigiate and pinnate; apices apices on only the outer faces of nodes or in complete inrolled except in the tetrasporangial thalli where they whorls of 5-7, angled in different directions (Fig. 1A-F) are much less inrolled and almost straight (Fig. 3F-K) (Maggs and Hommersand 1993, Rodríguez-Prieto et al. (Feldmann-Mazoyer 1941, Nakamura 1965, Itono 1972). 2013). The var. mediterraneum differs from the autonym The high number of cells of spines has been considered in the following features: axes always incompletely cor- the main diagnostic character of var. robustum (Coppe- ticated; periaxial cells 6-7 (incompletely or completely jans 1983, Wolf et al. 2011). Most records of var. robus- corticated; periaxial cells 8-9 in the var. echionotum); tum outside the Mediterranean report the presence of tetrasporangia formed in whorls of 1-5 per node (unilat- spines composed of 4 cells (e.g., Nakamura 1965, Itono erally, 1-2 in the autonym). In addition, the axes are up 1972 from the Pacific Ocean), whereas the spines in the to 300 µm in diameter in var. echionotum, whereas they specimens reported from the Mediterranean Sea may be are less than 150 µm in var. mediterraneum (Fig. 1G-J) up to 8 cells (Feldmann-Mazoyer 1941). C. ciliatum var. (Mazoyer 1938a, Feldmann-Mazoyer 1941, Secilla 2012). robustum has been reported from the Mediterranean C. echionotum var. mediterraneum has not previously coast of Morocco (Gómez Garreta et al. 2001), and this been recorded from Morocco, and the record of this vari- is the first record of this variety from the Atlantic coast of ety in this study from the Atlantic coast of Morocco is one Morocco. Our specimens have all diagnostic characters of the rare records from outside the Mediterranean. of var. robustum, and our observations confirm that the

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Fig. 1. (A-F) Ceramium echionotum var. echionotum. (A & B) Habit showing completely or nearly completely corticated axes. (C) Close-up of the outer cortical cells in surface view. (D) Tetrasporangia on adaxial side of upper branches. (E) Inrolled apices. (F) Cross-section of a node showing nine periaxial cells. (G-J) C. echionotum var. mediterraneum. (G) Habit showing incompletely corticated axes. (H) Detail of cortical nodes. (I) Apices inrolled with unicellular spines (arrows) and hyaline hairs (arrowheads). (J) Cross-section of a node showing seven periaxial cells. Scale bars represent: A, B & G, 1 mm; C-F, 200 µm; H-J, 100 μm. [Colour figure can be viewed at http://www.e-algae.org].

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A B

D

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Fig. 2. Ceramium gaditanum. (A & B) Habit of the thallus that is completely corticated. (C) Old part of the thallus showing sparse, short spines. (D) Apex with single multicellular spines. Scale bars represent: A, 1 mm; B, 400 µm; C & D, 100 µm. [Colour figure can be viewed at http://www. e-algae.org].

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Fig. 3. (A-E) Ceramium ciliatum var. ciliatum. (A & B) Detail of cortical nodes showing whorled spines, that are 3-celled. Arrows indicate the long basal cells (arrows). (C & D) Inrolled apices with whorled spines. (E) Tetrasporangia arranged in whorls, immersed or partially protruding. (F-K) C. ciliatum var. robustum. (F & G) Habit. (H) Cross-section of a node showing nine periaxial cells. (I & J) Details of spines of up to 7-cells. (K) Partially protrudingtetrasporangia. Scale bars represent: A-G, 200 µm; H-K, 50 µm. [Colour figure can be viewed at http://www.e-algae.org].

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multicellular spines of C. ciliatum var. robustum outside from each corticating initial, while in C. virgatum each the Mediterranean may also up to 7(-8)-cells (Fig. 3I & J). periaxial cells produces two cortical cells acropetally and Benhissoune et al. (2003) reported an allegedly spinose two-three basipetally. In forming only two descending species of Ceramium from Morocco, namely, “Ceramium filaments from each periaxial cell it shows similarity to penicillatum Areschoug”, which they pointed out to be a C. giacconei, which is otherwise quite distinct, chiefly by nom. illeg. That name was based on Gongroceras penicil- its habit. latum Kützing (1849) and later transferred to Ceramium Ceramium virgatum is the conserved type of the genus by Kylin (1907). That name, however, is a nomen. illeg., Ceramium (Greuter et al. 2000). It was cited by Agardh being a later homonym of C. penicillatum De Candolle (1811) as a synonym of C. rubrum and later noted as pos- in Lamarck & De Candolle (1805). So this record for Mo- sibly conspecific withC. nodulosum (Maggs and Hom- rocco is discounted. mersand 1993). Later, Maggs et al. (2002) suggested that the name C. virgatum Roth should be used for C. nodulo- Fully corticated Ceramium sum (Lightfoot) Ducluzeau. Ceramium virgatum var. implexocontortum a variety In Morocco, six fully corticated non-spinose taxa of not found in this study, was reported in only one refer- Ceramium are currently recognized. These are Cerami- ence (González-García and Conde-Poyales 1994) and um botryocarpum A. W. Griffiths ex Harvey, C. giacconei only on the Moroccan Mediterranean coast. Thus, its oc- Cormaci & G. Furnari, C. pallidum (Kützing) Maggs & currence would require confirmation. It is characterized Hommersand, C. secundatum Lyngbye, C. virgatum Roth by a multicellular cortex and branches differentiated into var. virgatum, C. virgatum var. implexocontortum (Solier) tendrils, the number of periaxial cells is almost constant- G. Furnari. Mostly, formerly confused under the illegiti- ly 8; it is very exceptional to find 9 (Feldmann-Mazoyer mate name Ceramium rubrum (Hudson) C. Agardh. Ce- 1941). According to Feldmann-Mazoyer (1941) the pres- ramium pallidum is one among the four species recently ence of these tendrils seems constant; it is a key feature added to Moroccan Ceramieae. Hassoun et al. (2016) de- used to separate this variety. scribed and discussed this species and its relationships The fifth Moroccan completely corticatedCeramium with other species in the genus in detail. It is well marked species, C. secundatum, was previously recorded from by its regular interval of four to nine segments between very few localities (Mazoyer 1938a, González-García and branches and by its regular alternate branching pattern, Conde-Poyales 1994), and our records confirm and ex- becoming more regular at least five orders of branching, tend the distribution of this species in Morocco. It can with dominant zigzag, with branch angles of 35-50° and be differentiated by its pseudodichotomous branching sometimes with ecorticate internode (Fig. 4A-E). A major pattern at 9 to 15 branch intervals; strongly inrolled api- specific character of C. pallidum is the type of the nodal ces; tetrasporangia in whorls at each node on younger cortication. C. pallidum possesses a cortication formed axes; adventitious branches present (Fig. 4F-I) (Maggs by cells of different sizes: a discontinuous outer layer and Hommersand 1993, Maggs et al. 2002). C. secunda- of small cortical cells arranged in rosettes around inner tum is closely related to C. virgatum, and a monophyletic cortical cells (Fig. 4C). Maggs et al. (2002) confirmed that relationship was found between the two species in the the regular and short branching interval is of paramount British Isles by Maggs et al. (2002). However, the regular importance in identifying this species, a character that branching interval of 9-15 segments, showing a range of we can confirm (Fig. 4A & B). This species is absent in intervals within individual samples of 2-5 segments, and the Moroccan Mediterranean side and widely distribut- the numbers of periaxial cells that are up to 9 serve to dis- ed throughout the Atlantic side, which leads us to con- criminate C. secundatum from both C. virgatum and C. clude that this species has been misidentified as other pallidum (Maggs et al. 2002, Hassoun et al. 2016). similar common species such as C. virgatum because As noted above, Ceramium secundatum is similar to C. both species share some similarities. However, C. virga- virgatum and C. pallidum, but in forming two cells di- tum is clearly distinguished by its axes branching every rected acropetally and two-three basipetally it is more 10 to 18 segments and by its extremely irregular branch- similar to C. botryocarpum, a species reported for the ing pattern (Maggs and Hommersand 1993, Maggs et first time from Morocco in this study. However, C. bot- al. 2002, Rodríguez-Prieto et al. 2013). Furthermore, C. ryocarpum is distinguished in forming turfs due to devel- pallidum can be differentiated by its two acropetal cor- opment of extensive prostrate axes attached by a dense ticating filaments and two basipetal that are produced mass of multicellular rhizoids and by its cystocarps

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Fig. 4. (A-E) Ceramium pallidum. (A) Habit. (B) Distal parts of thallus with a dominant zigzag branching pattern. (C) Detail of cortical nodes showing small cortical cells arranged in rosettes around inner cortical cells. (D) Female thallus bearing cystocarps surrounded by involucral branchlets. (E) Tetrasporangial thallus. (F-I) C. secundatum. (F) Main axis showing branching pattern and interval of branching. (G) Cortex of fully corticated axis. (H) Inrolled apices. (I) Cross-section of a node showing nine periaxial cells. Scale bars represent: A, 2 mm; B, D, E & H, 300 μm; C, 100 µm; F, 1 mm; G & I, 200 μm. [Colour figure can be viewed at http://www.e-algae.org].

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A B C

F

E

D

G

Fig. 5. Ceramium botryocarpum. (A) Habit of the thallus showing abundant adventitious branchlets (arrows). (B & C) Axes with tetrasporangia arranged in whorls, immersed or partially protruding. (D) Thallus with cystocarps consisting of a single gonimolobe surrounded by involucral branchlets. (E) Prostrate axes with dense mass of multicellular rhizoids. (F) Cross-section of a node showing seven periaxial cells. (G) Detail of the apex. Scale bars represent: A, 5 mm, B & E, 1 mm; C & D, 400 µm; F & G, 200 μm. [Colour figure can be viewed at http://www.e-algae.org].

consisting of a single (rarely two) globular gonimolobe prominent, formed in wide bands in mature axes, 3 to 8 (Maggs and Hommersand 1993, Secilla 2012). Our collec- tetrasporangia at each node, and cystocarps consisting tions of C. botryocarpum (Fig. 5A-G) agree with previous of a single gonimolobe. Ceramium botryocarpum is re- descriptions and illustrations given by Maggs and Hom- ported from the Atlantic coast of Morocco and not found mersand (1993) and Secilla (2012), in having prostrate on the Mediterranean side. It is widely distributed in the axes attached by a dense mass of rhizoids, giving rise to North Atlantic Ocean from Ireland to Portugal (Guiry and erect axes; branching irregular or regularly dichotomous Guiry 2018). This is the first report of this species outside every 12-17 node; abundant adventitious branches; api- the northeastern Atlantic coast of Europe. ces incurved to strongly incurved; periaxial cells 6-7; Ceramium giacconei (a species not found in this tetrasporangia immersed in the cortex, rarely semi- study) was described by Cormaci and Furnari (1991) to

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A B

Fig. 6. Ceramium cingulatum. (A) Habit. (B) Detail of a thallus that is incompletely corticated with protruding tetrasporangia. Scale bars represent: A, 400 µm; B, 200 µm. [Colour figure can be viewed at http://www.e-algae.org].

accommodate the entity previously known in the Medi- thalli, creeping and erect without branching, and with terranean as Ceramium cingulatum Weber-van Bosse. protruding tetrasporangia (Fig. 6A & B). Tetrasporophytic By comparing some Mediterranean specimens with the and sterile plants were collected in February to August; type material of C. cingulatum, Cormaci and Furnari female and male plants were not found. This species was described the Mediterranean material as C. giacconei reported from the Atlantic coast of northern Morocco, sp. nov. Records of C. cingulatum from Mediterranean commonly inhabiting upper sublittoral zone of rocky ex- coast of Morocco by González-García and Conde-Poy- posed shores, as an epiphyte on larger algae. ales (1991, 1994) were considered as a misidentification for Ceramium giacconei by Gómez Garreta et al. (2001). Ceramium with ecorticate internodes In its original description, Cormaci and Furnari (1991) detailed the main features used to identify this species: Ten non-spinose species of Ceramium with ecorticate erect thalli with the marked swelling after 3 or 4 basal internodes are currently recognized from Morocco: Ce- segments, corticating filaments unequally developed ramium callipterum Mazoyer, C. cingulatum Weber-van from a cortical initial, cortication complete except on Bosse, C. circinatum (Kützing) J. Agardh, C. codii (H. Rich- the basal segments (Cormaci and Furnari 1991, Cho et ards) Mazoyer, C. cornutum P. J. L. Dangeard, C. deslong- al. 2003). The combination of these characters makes it champsii Chauvin ex Duby, C. diaphanum (Lightfoot) distinct from all other species of Moroccan Ceramium. Roth, C. siliquosum (Kützing) Maggs et Hommersand Furthermore, Ceramium giacconei is also distinguished var. siliquosum, C. siliquosum var. lophophorum (Feld- from C. cingulatum, a species reported for the first time mann-Mazoyer) Serio, and C. tenerrimum (G. Martens) from Morocco in this study, by its tetrasporangia being Okamura (see Gómez Garreta et al. 2001, Benhissoune immersed in the cortex and thalli being completely erect et al. 2003, Hassoun et al. 2016). C. cornutum, one of the (Cormaci and Furnari 1991, Cho et al. 2003), while C. cin- Ceramium species that was recently added to Morocco gulatum is characterized by its incompletely corticated by Hassoun et al. (2016), is a species described from Cap

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Vert. This species was collected from the Moroccan At- cur in Morocco: C. siliquosum var. siliquosum, occurs on lantic coast. It is well marked by the apices being always the Mediterranean and Atlantic shores of Morocco and divaricate, never incurved, and by the many forked ad- C. siliquosum var. lophophorum was previously reported ventitious branches, with the lateral branches inserted only from the Mediterranean shores by González-García nearly perpendicularly (Fig. 7A-E). These two characters and Conde-Poyales (1994). The latter, not found in this make it a very distinct species, not just from Moroccan study, differs from the autonym in having inrolled apices Ceramium but from all other species of the genus. with conspicuous gland cells, developed on their outer Tetrasporophytic plants of C. cornutum are observed side; and irregularly dichotomous branching (Feldmann- from February to August, cystocarpic plants from May to Mazoyer 1941). September. This species has been previously reported in Among species cited bibliographically from Morocco the warm temperate and tropical parts of the eastern At- by only a single reference are those of C. deslongchampsii lantic Ocean with vegetative and tetrasporophytic thalli. by Mazoyer (1938a) and of C. codii by González-García Now, both tetrasporophytes and female gametophytes and Conde-Poyales (1994). The latter species was first have been found. described by Richards (1901) for a small alga that was Ceramium diaphanum (Lightfoot) Roth is well known, collected in Bermuda as an epiphyte on Codium, and it but it appears that literature records of this species from has been recognized as being widely distributed in warm Morocco are based upon taxonomic confusion. The only temperate and tropical areas. Among the 14 described citations referred to C. diaphanum are those under C. creeping Ceramium species characterized by a predomi- nodosum sensu Griffiths et Harvey and C. tenuissimum nantly prostrate habit, C. codii is the only one that occurs (Roth) J. Agardh, nom. illeg. (Maggs and Hommersand in Morocco. 1993). It has been recorded several times as C. tenuissi- Within the genus, three cortical initials per periaxial mum (Roth) Areschoug nom. illeg., and as C. nodosum cell have been reported in Ceramium reptans T. O. Cho sensu Griffiths et Harvey. But it has probably also been et Fredericq, C. periconicum and C. codii (Cho and Rios- confused with C. siliquosum (Kützing) Maggs et Hom- mena-Rodriguez 2008). However, C. codii is recognized mersand as pointed out by Benhissoune et al. (2003) in by a combination of the following characters: prostrate that C. siliquosum is one of the names available for C. di- axes producing unbranched, upright axes dorsally, four aphanum sensu Harvey, and literature records of C. sili- periaxial cells per axial cell, three cortical cells cut off per quosum are difficult to assess owing to taxonomic con- periaxial cell with the basipetal cortical cell cut off hori- fusion. However, this takes into consideration that these zontally on the prostrate axis, and 1-2 tetrahedrally divid- records were probably based upon Harvey’s specimens ed tetrasporangia produced per periaxial cell (Cho and and illustrations (C. diaphanum sensu Harvey) and on Fredericq 2006, N’Yeurt and Payri 2010). Likewise, this Feldmann-Mazoyer’s (1941) concept of C. diaphanum minute species of Ceramium is easily distinguished by its var. diaphanum. minimal nodal cortication, sparse to simple branching, At the macromorphological level, these two species (C. and its long internodes (Fig. 7H & I). diaphanum and C. siliquosum) share some similarities, Ceramium deslongchampsii, a species not found in mainly in the extent of cortical development, each peri- this study, also has prostrate axes, but not predominant- axial cell gives rise to two cells directed acropetally and ly so, and bears numerous densely tufted and densely two basipetally, in the branching pattern: pseudodichot- branched erect axes. These features are in contrast to C. omous, but at intervals of 4-7 segments in C. siliquosum codii, which has unbranched erect axes and apices (Itono (Fig. 7F & G), 8-13 segments in C. diaphanum; and some- 1972, Maggs and Hommersand 1993, Cho and Fredericq what in the curvature of the apices, they are mostly tight- 2006). C. deslongchampii also differs from C. codii in that ly inrolled (Maggs and Hommersand 1993). However, C. the tetrasporangia are formed in groups in a row around siliquosum has tetrasporangia located in whorls protrud- nodes (one or two tetrasporangia develop from a single ing from the upper half of the nodes and entirely covered periaxial cell in C. codii), by 5-6 periaxial cells per axial by ascending cortical filaments, which contrasts with C. cell, each periaxial cell produces two acropetal and two diaphanum, in which tetrasporangia are scattered singly basipetal cortical filament (only 4 inC. codii and two or in small groups on the adaxial side of the node and acropetal, one basipetal cortical filament).C. cingula- partially covered. Furthermore, conspicuous gland cells tum, a species reported in Morocco (the Atlantic coast) are present in C. diaphanum but absent in C. siliquosum. for the first time in this study, also has prostrate axes, but Two varieties of Cermium siliquosum are known to oc- it is more closely related to C. giacconei than any other

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A B C

D E F

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I

Fig. 7. (A-E) Ceramium cornutum. (A & B) Habit. (C & D) Female thallus bearing cystocarps surrounded by involucral branchlets. (E) Upper part of thallus showing tetrasporangial rows and divaricate and divergent apices. (F & G) C. siliquosum var. siliquosum. (F) Habit. (G) Thallus showing interval of branching. (H & I) C. codii. (H) Detail of nodal cortication. (I) Axis with long internodes. Scale bars represent: A, B, F & G, 1 mm; C-E, 400 µm; H, 30 µm; I, 100 µm. [Colour figure can be viewed at http://www.e-algae.org].

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species in the genus as discussed above. this species (Mazoyer 1938b, Anderson and Stegenga It is interesting that Ceramium codii, one of the most 1989). This species, which has a type locality of Mazagan commonly reported species in the eastern North Atlantic (Al Kadoda), Morocco (Silva et al. 1996), but not found Ocean and the Mediterranean Sea, was cited in only one during this study, has a limited distribution in the north- reference from Morocco (Mediterranean side). Thalli up eastern Atlantic Ocean (Guiry and Guiry 2018). The little- to 4 mm in length were sometimes found, but a length of known species Ceramium callipterum is recognized by 0.3-0.7 mm was the typical size. The species is likely to be the following characteristics: main axes with a regular simply overlooked when collecting or sorting due to its alternate branching, at every second segment, giving the small size. On the other hand, C. codii may not be as wide- plants a plumose appearance, apices that are straight to spread a species as is widely reported in the literature, slightly incurved, 6 periaxial cells per node, exserted and and it may comprise several distinct entities (Coppejans prominent tetrasporangia, formed singly or in groups, 1977, Cho and Fredericq 2006). This is the first record of sometimes forming small clusters (see Mazoyer 1938b, p. this species from the Moroccan Atlantic coast. 17, Fig. 2) As mentioned above, 21 taxa of Ceramium at specific As above mentioned, five taxa of this genus reported and infraspecific level are known from Morocco. Of these, previously from Morocco were not found during the only one, C. tenerrimum, has cortication produced acrop- present study: C. callipterum, C. giacconei, C. deslong- etally only (Fig. 8A-D). It is a key feature in the identifica- champsii, C. virgatum var. implexocontortum, and C. sili- tion of this species because some of the other characters quosum var. lophophorum. appear to be variable. For example, De Barros-Barreto et al. (2006), Nunes et al. (2008), and Serio et al. (2011) Gayliella characterized this species with eight to nine periaxial cells. However, a periaxial cell number of nine was not re- The genus Gayliella was erected by Cho et al. (2008) ported for C. tenerrimum by Lagan and Trono (2017), but to accommodate the Ceramium flaccidumcomplex us- according to those authors it varied between 6-8 periaxial ing molecular techniques and morphological analyses. cells. In addition, the periaxial cell number varied within The genus is clearly distinguished by the production of individual thalli and axes studied by Simons (1966). The three cortical initials per periaxial cell, of which the third number reported by Rodríguez-Prieto et al. (2013) varied is directed basipetally and divides horizontally (Fig. 9F & between 6-7, never eight or nine. However, we note that G). All species in the genus are incompletely corticated this species appeared to be particularly variable and that and have alternate branching (Fig. 10A-D); unicellular its morphological limits, particularly, reduced the value elongate rhizoids are produced from periaxial cells (Fig. of the number of periaxial cells to distinguish species. 9I & J). In contrast to C. tenerrimum, the number of periaxi- Three Gayliella-related taxa were reported from Mo- al cells in C. circinatum is one of the important distin- rocco with little morphological information: Ceramium guishing features of this species. This is the only species flaccidum (Harvey ex Kützing) Ardissone, C. gracillimum among Ceramium occurring in Morocco that has nine to (Kützing) Griffiths et Harvey, and C. gracillimum var. bys- ten periaxial cells (Fig. 8H). Moreover, C. circinatum has soideum Mazoyer (Dangeard 1949, Benhissoune et al. a different cortication to that of C. tenerrimum, that is, 2003). In the present study, G. taylorii (E. Y. Dawson) T. both acropetal and basipetal in the former species and O. Cho et S. M. Boo is newly added from Morocco. In ad- only acropetal in the latter. Generally, C. circinatum dition, the three reported taxa have been found to repre- develops an extensive cortex in the basipetal direction sent Gayliella flaccidaand Gayliella mazoyerae T. O. Cho, (Fig. 8E-G) (Simons 1966, Coppejans and Boudouresque Fredericq et Hommersand. 1981, Sansón 1994). Moreover, the intervals of branching of the main axes in C. circinatum (every 9-14 node) are Key to species of Moroccan Gayliella greater than in C. tenerrimum (every 6-9 node) (Feldma- 1a. Periaxial cells number 4; cortex <70 µm long; basip- nn-Mazoyer 1941, De Barros-Barreto et al. 2006). Both of etal cells one row; branching intervals 4-5 on main these species occur on the two shores of Morocco, Atlan- axes, 4-6 on lateral axes; gland cells inconspicuous, tic and Mediterranean. rarely observed; tetrasporangia whorled, tetrahe- Ceramium callipterum is the species that has very drally divided ------G. mazoyerae small intervals of branching of the main axes, at inter- 1b. Periaxial cells number >4, basipetal cells 2-3 rows ---- vals of only 2 segments. This is a key feature separating ------2

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A B C D

E F

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Fig. 8. (A-D) Ceramium tenerrimum. (A) Habit. (B & C) Details of cortication of nodes. (D) Detail of strongly inrolled apices. (E-J) C. circinatum. (E) Habit. (F & G) Detail of cortication of nodes showing extensive cortex developed in basipetal direction. (H) Detail of the periaxial cells in cross- sectional view of a node. (I & J) Thalli with incurved apices. Scale bars represent: A & F-J, 200 µm; B-D, 50 µm, E, 1 mm. [Colour figure can be viewed at http://www.e-algae.org].

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2a. Thalli to 200 µm in diameter; periaxial cells 5-6; Womersley (1978) placed Ceramium taylorii in syn- branching at intervals of 7-9 on main axes, 10-14 on onymy with C. flaccidum, but South and Skelton (2000) lateral axes; gland cells rarely develop from corti- maintained C. taylorii as a separate taxon. They examined cal cells of acropetally corticating filaments and are isotype material of C. taylorii from Cabeza Ballena, Baja ovoid; tetrasporangia unilateral, usually only on ad- California, and noted that the nodal structure is quite axial side ------G. flaccida different from that included under Ceramium flaccidum 2b. Thalli to 120 µm in diameter; periaxial cells 6-7; and concluded that the proposed synonymy of C. taylorii branching at intervals of 3-4 on main axes, 4-6 on under C. flaccidumappears to be unwarranted. Gayliella lateral axes; gland cells develop from cortical cells of flaccida and G. taylorii are collected from the two shores acropetally developed filaments and are ovoid; tet- of Morocco, Atlantic and Mediterranean, while G. mazoy- rasporangia whorled, tetrahedrally divided ------erae was reported only from the Atlantic side. ------G. taylorii The present study is the first detailed description of In Morocco, G. mazoyerae was first reported as Cera- the three species from Morocco. This is the first record mium gracillimum var. byssoideum by Dangeard (1949), of G. taylorii on the Moroccan Atlantic coast and one of which was considered by Cho et al. (2008) to be a taxo- the rare records of this species throughout the Atlantic nomic synonym of this taxon. This species is clearly dis- Ocean. tinguished from all Moroccan Gayliella by its acropetal corticating filaments 1-2 cells long, and only 1 basipetal Centroceras horizontally elongate cell (Fig. 9A-G) and by its nodes consisting of 4 periaxial cells compared with the 5-6 and As currently defined, the genusCentroceras Kützing 6-7 periaxial cells in G. flaccidaand G. taylorii, respective- contains 17 species (Guiry and Guiry 2018). Only one spe- ly (Cho et al. 2008). In forming four periaxial cells, one cies has been reported from Morocco, the type species basipetal horizontally elongate cell and 1-2 cortical cells Centroceras clavulatum (C. Agardh) Montagne. C. clavu- growing acropetally it shows similarity to G. transversalis latum had been thought to have an almost cosmopolitan (Collins et Hervey) T. O. Cho et Fredericq. However, in the tropical-warm temperate distribution (Lüning 1990, van latter species branching intervals are longer, 5-6 celled in den Hoek and Breeman 1990). But several authors noted main axes and 8-10 celled in the lateral axes, compared that the entire group is in need of a systematic revision with the 4-5 and 4-6, respectively in G. mazoyerae (Fig. (e.g., Athanasiadis 1996). 9A-E). De Barros-Barreto et al. (2006) reported that C. clavu- Gayliella flaccida has been reported as Ceramium latum may consist of a species complex. Later, Won et flaccidum from Morocco (Benhissoune et al. 2003). This al. (2009) pointed out that C. clavulatum has a biogeo- species is similar to G. taylorii in the shape of the cortex graphic distribution limited to the Pacific Ocean based because in both species the acropetal corticating fila- on comparative morphological and molecular analy- ments are 3-4 cells long, and the basipetal filament is 2-3 ses of specimens going under the name C. clavulatum cells long (Fig. 10E-I). However, the first species displays worldwide, and according to those authors material an assemblage of characters that clearly distinguishes it going under the name C. clavulatum is often misidenti- from all other species of the genus. Only G. flaccidahas fied and in fact separable into nine discrete taxa based thalli reaching 12 cm in height, and it is the only species on the comparative development of the acropetal corti- that has 5-6 periaxial cells per segment and with inter- cal filaments. Agreeing with Gallagher and Humm (1983) nodes 8-12 times as long as broad, except in the upper who reported the potential taxonomic value of the gland part of the plant (Maggs and Hommersand 1993, Cho et cells. Won et al. (2009) pointed out that the gland cells are al. 2008, Lagan and Trono 2017). The erect thalli in the more important than previously used as one of the key other six species of the genus do not exceed 1.5 cm in characters in Centroceras, and they described two differ- height (Cho et al. 2008). In G. taylorii the thalli grow to ent types of gland cells by their shape: flattened or ovoid. lengths of no more than 1.2 cm, with 6-7 periaxial cells Centroceras gasparrinii has ovoid gland cells (Fig. 11H & per segment and with branching at intervals of 3-4 axial I), whereas in C. clavulatum they are flattened. Further- cells in the main axes and at intervals of 4-6 axial cells more, the numbers of periaxial cells per segment are up in lateral axes (Fig. 10A & B). In addition, branches are to 19 in Centroceras gasparrinii, while in C. clavulatum indeterminate in G. flaccida, while in G. taylorii they are they are 13-16 (De Barros-Barreto et al. 2006, Won et al. sometimes determinate (Cho et al. 2008). 2009, 2010, Schneider et al. 2015).

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A B C

D E F

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Fig. 9. Gayliella mazoyerae. (A) Habit. (B-E) Erect part showing branching pattern and interval of branching. (F & G) Detail of the cortication of nodes showing a periaxial cell (p) and two acropetal cortical initials (c1-c2) and one basipetal-horizontal cortical initial (c3). (H) Apical region. (I & J) Unicelluar rhizoids issued from periaxial cell (p). c1-3, cortical initials, numbered by sequence of formation. Scale bars represent: A-E & H, 100 µm; F & G, 20 µm; I & J, 40 µm. [Colour figure can be viewed at http://www.e-algae.org].

https://doi.org/10.4490/algae.2018.33.8.29 260 Hassoun et al. The Tribe Ceramieae in Morocco

A B C

D E F

G H I

Fig. 10. Gayliella taylorii. (A-C) Thallus showing branching pattern and interval of branching. (D) Apical region. (E) Unicellular rhizoid issued from periaxial cell. (F-I) Detail of mature corticated nodes showing 3-4 cortical cells growing acropetally, 2-3 cortical cells growing basipetally and gland cells (arrows) developing from cortical cells of acropetally corticating filaments. Scale bars represent: A-C, 200 µm; D-F, 100 µm; G-I, 30 µm. [Colour figure can be viewed at http://www.e-algae.org].

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Fig. 11. Centroceras gasparrinii. (A) Habit of the lower part of a thallus. (B & C) Tetrachotomous (B) or trichotomous (C) branches at branching points (arrows). (D & E) Adventitious branchlets arranged on abaxial sides of dichotomous axes. (F) Apical region. (G) Lower part of thallus showing rhizoids produced from periaxial cells. (H & I) Mature cortication showing cortical filaments with gland cells (arrows). (J) Cross section of axis showing 14 periaxial cells. (K) Detail of cortical cells on surface view. Scale bars represent: A, 1 mm; B-G, 300 µm; I-K, 30 µm. [Colour figure can be viewed at http://www.e-algae.org].

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Centroceras specimens with a dichotomous habit from op the cortical filaments, in which two acropetal initials Morocco have been recognized as C. clavulatum. It has are cut off from the anterior end of a periaxial cell and been reported from all coasts of Morocco, after the first two basipetal initials are cut off from the posterior end record of this species was made from the Mediterranean (Norris 1993). coast of Morocco by Bornet (1892). It has been known as Despite the fact that Cho et al. (2000) confirmed the ge- a very common species in the Moroccan marine flora. neric concept of Corallophila proposed by Norris (1993) However, the results in this study show that all Centro- and that others have recognized the genus (e.g., Abbott ceras collections with dichotomous branching patterns 1999), the distinctiveness of the genus Corallophila is from Moroccan coasts are not C. clavulatum but C. gas- controversial. Ten species of Corallophila are currently parrinii. recognized worldwide (Guiry and Guiry 2018). Only one Centroceras gasparrinii is similar to C. clavulatum species, Corallophila cinnabarina (Grateloup ex Bory) R. in having a dichotomous branching pattern, straight E. Norris, is recognized in Morocco. spines, ovoid terminal acropetal cortical cells and in the C. cinnabarina is recognizable by the combination of arrangement of cortical filaments (Fig. 11). However, the following characters: plants 1-4 cm tall; prostrate, the branching in C. gasparrinii is sometimes tri- to tet- may also produce an extensive pseudodichotomously rachotomous by the production of additional branches branched upright system; forcipate tips; pericentral cells from the nodal region of a branching point (Fig. 11B & C). 6, sometimes 7 or 8; two acropetal and two basipetal cor- The adventitious branches that arise from periaxial cells ticating filaments on each pericentral cell, with the latter are short, usually inrolled toward the axis and arranged longer and forming rows of rectangular corticating cells on the abaxial side of the dichotomous axis (Fig. 11D & with long axes perpendicular to the thallus axis, cortical E). Furthermore, in C. gasparrinii the ovoid shape of the cells broader than long and arranged in regular files, tet- gland cell clearly separates it from C. clavulatum. rasporangia immersed. C. gasparrinii is recognizable by the combination of C. cinnabarina was not found during the present study. the following characters: terminal acropetal cortical cells It has been reported only in one reference by González- ovoid; gland cell ovoid; axial cells with 12 to 19 periaxial García and Conde-Poyales (1994), without illustrations cells; branching is pseudodichotomous to trichotomous and / or descriptions. and, rarely tetrachotomous, at intervals of 10-13 axial cells; spines straight, whorled at each node; tetrasporan- Microcladia gia covered, with involucral branchlets (Fig. 11). In light of our study, C. clavulatum is excluded from the Moroc- The morphological characters of Microcladia are can flora, and C. gasparrinii is now recognized instead of somewhat related to those of Ceramium. In the above C. clavulatum. genera, the periaxial cells are produced in a rho- domelacean sequence and lateral branches originate Corallophila from the apical cell, whereas in the more primitive gen- era Carpoblepharis and Reinboldiella the periaxial cells The generic concept of Corallophila was revised by are produced in opposite pairs, and the indeterminate Norris (1993) and later by Cho et al. (2000). According to branches originate from periaxial cell. Since certain Ce- Cho et al. (2000) Corallophila is intermediate between ramium are completely corticated, as in Microcladia, Ceramium and Centroceras in some features, but the ge- several authors have found it difficult to differentiate the nus is distinctive in having tetrasporangia in stichidia, two genera. However, Hommersand (1963) distinguished almost completely embedded in the cortex. Cystocarps species of Microcladia from fully corticated species of naked, without involucral branches, spermatangia that Ceramium in having thalli producing secondary cortical occur on outer cortical cells, rhizoids formed from peri- cells in an acropetal direction only (producing secondary axial to inner cortical cells, rectangular cortical cells that cortical cells in both an acropetal and basipetal direction are regularly arranged in longitudinal rows and grow ba- in Ceramium). sipetally. Norris (1993) identified that the development The genus Microcladia includes 10 species worldwide of spermatangia on the cortical cells and tetrasporangia (Guiry and Guiry 2018). Most of them are distributed on being mostly covered by outer cortical cells as key char- Pacific coasts. It is one of the most geographically lim- acters for Corallophila. In most species of Corallophila, ited genera known, with four endemics species (Silva et each periaxial cell cuts off four cortical initials that devel- al. 1996, Guiry and Guiry 2018). The type species Micro-

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cladia glandulosa is the most widely distributed species rini. As a result, C. clavulatum is excluded from Moroc- and the only species of the genus currently recognized can flora and replaced with C. gasparrinii. from Morocco (Benhissoune et al. 2003), although most The presence of the genus Gayliella is confirmed and of these references for Morocco that cite this species are three species are listed of which G. taylorii is newly added without illustrations and / or descriptions. from Morocco, and G. mazoyerae is reported and illus- Microcladia glandulosa is distinguished from other trated for the first time after the only record of this spe- species in the genus by the following combination of cies was made by Dangeard (1949) as Ceramium gracil- characteristics: fronds tufted, 2-10 cm high, with pros- limum var. byssoideum. The presence of Microcladia and trate axes that give rise to numerous erect axes; branch- especially Corallophila in Morocco requires special at- ing is regularly in an alternate or pseudodichotomous, at tention in future investigations. intervals of 6-10 axial cells, at an angle of 30-60°; abun- Not all of our collected specimens have been identified dant angular gland cells; periaxial cells 6-8 of unequal in this study because many of them could not be clearly size, the first abaxial and the last adaxial; tetrasporangia characterized due to lacking critical features. This study in upper branchlets, unilateral, abaxial, singly or in pairs showcases the need for more phycological studies in or- from the side of the first periaxial cells, immersed; cysto- der to clarify the Moroccan algal biodiversity, particularly carps sessile on abaxial on outer edges of upper branch- in difficult-to-reach or inaccessible areas that remain es, enclosed by 2-3 involucral branchlets. poorly known. The abundant gland cells of M. glandulosa are a very conspicuous feature. Gland cells are also present in the South African Microcladia exserta M. J. Wynne, as de- SUPPLEMENTARY MATERIAL scribed by Wynne (1985). But the gland cells in the type of the genus are less numerous and smaller than the cor- Supplementary Table S1. Collection data for speci- tical cells. In terms of their high number and conspicu- mens of the Ceramieae examined in this study (http://e- ousness, the gland cells in M. exserta seem to be the most algae.org). highly developed of any member in the tribe Ceramieae (Wynne 1985). REFERENCES

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