First record of Rhodymenia holmesii (Rhodymeniaceae, Rhodophyta) for the Mediterranean Sea from Morocco

Abstract

Background

The rhodymenialean red algal species Rhodymenia holmesii was collected in the lower intertidal zones from Dalya and Al-Hoceima (Northern Morocco, Mediterranean Sea). This represents the first record and description in the Mediterranean Sea.

Results

Moroccan materiel was studied in detail and compared with other closely related species. Descriptions of the morphological features reveal thalli with flaccid blades, 8 cm long, regularly dichotomously branched and attached with stoloniferous holdfast. Anatomically, cortical region composed of 2–3 cell layers and medulla composed of 3–5 cell layers.

Conclusions

This finding indicates that the biodiversity of the related sites is probably richer than generally thought, and other phycological studies will increase the known algal biodiversity of the region.

Background

The genus Rhodomenia (sic) was proposed by Greville in 1830 and included 16 species. Later, other species were added by J. Agardh (1841) who changed the concept of the genus to adopt the suggestion of Montagne (1839) regarding the ratification of the orthography Rhodymenia (J. Agardh 1851). The latter spelling has been conserved over the original “Rhodomenia”.

Rhodymenia’s species have often been confused with other genera. The reason for which several authors (Agardh 1851, 1876; Dawson 1941) divided the genus into five sections or subgenera based on reproductive structures, especially tetrasporangia. Regarding the vegetative morphological features, Guiry (1977) gave a useful comparison of the cortical cells in surface view of three species of Rhodymenia and nine species of other genera with a similar morphology, which help to distinguish between them.

Irvine (1983) described Rhodymenia as thallus with erect or prostrate, usually stipitate fronds, arising from a basal disc or stolons, blades flattened, simple or divided dichotomously, palmately or irregularly; sometimes with marginal or apical proliferations; structure multiaxial, medulla compact, pseudoparenchymatous, with large axially elongated cells, cortex of radial filaments of 2–5 smaller cells. Gametangial plant dioecious; spermatangia in small subapical sori or large irregular patches scattered over blade, produced superficially from outer cortical cells; carpogonial branches 3–4-celled, supporting cell also bearing 2-celled auxiliary cell branch, gonimoblast developing outwards often with 2–3 lobes, almost all cells forming carposporangia, enveloping filaments absent; cystocarps hemispherical, large and protruding, with a pore, formed apically or scattered; tetrasporangia in subapical sori or scattered throughout blade, intercalary in unmodified cortex, cruciate.

The genus Rhodymenia consiste of some 62 species worldwide, which have been recognized as currently accepted taxonomically, distributed through warmer waters from the lower intertidal to depths of about 100 m (Guiry and Guiry 2015). Among these 62 species, only 8 taxa have been reported from the Mediterranean Sea (Rodríguez y Femenías 1889; Giaccone 1969; Huvé and Huvé 1971; Rindi et al. 2002; Rodríguez-Prieto et al. 2013). On the Moroccan Mediterranean coast, the genus is only represented by the type species Rhodymenia pseudopalmata (J.V. Lamouroux) P.C. Silva and R. caespitosa P. Dangeard (Kazzaz and Riadi 2000).

In recent years, there has been an interest increasing in the Moroccan algal biodiversity. Inventories began with that of Riadi and Kazzaz (1998), Riadi et al. (2000) and Kazzaz and Riadi (2000), who assign to the country 455 taxa at specific and intraspecific level, this followed soon afterward by the publication of Benhissoune et al. (2001; 2002a, b; 2003) which were more detailed and confirmed 612 species and intraspecific taxa, 15 taxa excludenda and 35 taxa inquirenda of the benthic marine algal flora of Morocco. More recently, we added 23 species (Riadi et al. 2011, 2013; Hassoun et al. 2014; 2015a, b, 2016; Moussa et al. 2015). Despite these advances, much work remains to be done on the marine benthic flora of Morocco as relatively few habitats have been extensively studied.

In this study, we report on the occurrence of a rhodymenialean species, Rhodymenia holmesii Ardissone, from Morocco and the Mediterranean Sea for the first time.

Materials and methods

Samples were collected from Dalya (35°54′24″N, 5°28′19″W) and Rmoud (35°09′25.1″N, 4°20′01.6″W) from the occidental shores of the Mediterranean Sea. Samplings were performed in 2013 and 2014, in the upper subtidal (0.5–1 m depth) and low intertidal of wave exposed rocky shores. Fresh algae samples were transported to the laboratory in plastic bags with seawater. Studies were carried out on samples preserved in 5 % formalin-seawater solution; anatomical sections were made by hand with a razor blade. The specimens studied were deposited in the Phycological Herbarium of the Phycology and Mycology Laboratory, Faculty of Sciences, Abdelmalek Essaâdi University, Tetouan, Morocco (HTET; 823 and 830: Rhodymenia holmesii). Photomicrographs were taken with a color camera Olympus XC50 (Tokyo, Japan) coupled to Olympus Bx43 microscope. For the nomenclatural purposes, following taxonomic databases were used: Index Nominum Algarum (Silva 2015) and AlgaeBase (Guiry and Guiry 2015).

Results and discussion

Systematics

Order rhodymeniales F. Schmitz in Engler, 1892

Family rhodymeniaceae Harvey, 1849

Genus Rhodymenia Greville 1830

Rhodymenia holmesii Ardissone, 1893 (Fig. 1)

Fig. 1

Rhodymenia holmesii Ardissone, 1893: (a–b) habit; (c) thalli with stoloniferous growth giving rise to flattened blades; (d) stipe; (e) transverse section of the blade showing 3–4 layers of medullary cells; (f) transverse section, showing layers and arrangement of cortical cells; (g) surface view of the cortical cells from the apex; (h) cortical cells from the median part and subcortical cells (arrows) in surface view; (i) cortical cells from the stipe in surface view. Scale bars: a–b, 3 cm; c–d, 1 cm; e, 30 μm; f, 100 μm; g, 20 μm; h–i, 30 μm

Basionym: Halyymenia palmetta var. ellisiae Duby, 1830

Synonyms: Rhodymenia palmetta var. ellisiae (Duby) Bornet 1892 (as elisiae)

Rhodymenia pseudopalmata var. ellisiae (Duby) Guiry 1975

Geographic distribution

The type locality of this species is Sussex, England (Athanasiadis 1996), the species appears to be limited to the North Atlantic (Hardy and Guiry 2003; Bárbara et al. 2006; Dizerbo and Herpe 2007) and the utmost localities in the South Atlantic Ocean (Stegenga et al. 1997; Rull Lluch 2002; John et al. 2004). The closest previous records are those of Bárbara et al. (2012), Cires Rodriguez and Cuesta Moliner (2010), both from the Iberian Peninsula; Haroun et al. (2002), John et al. (2004) and Afonso-Carrillo (2014), all from the Canary Islands.

Habitat and collection

Specimens recorded at Dalya in February 2013 growing in association with Gelidium attenuatum (Turner) Thuret and May 2013; also collected at Rmoud in May 2013 and August 2014. In both sites, the species grows on shaded rocky between upper subtidal and low-intertidal substrata.

Description

Thalli are up to 8 cm tall, brown-red, arising from an extensive branched stoloniferous holdfast (Fig. 1a–c), becoming extensively branched in soft rock, giving rise to erect and flaccid blades. Fronds with a short stipe to 10 mm long (Fig. 1d); expand gradually into a fan-shaped, somewhat cartilaginous blade with parallel sides 70 mm long, 5 mm broad and 120–190 μm thick. Blades regularly dichotomously branched; usually with 3–4 orders of branches and with narrow angles in the forks. Marginal proliferations occur from base of plants, often reattaching to the substrate.

Pseudoparenchymatous medulla composed of 3–5 layers of axially elongated to ovoid cells (Fig. 1e), 40–60 μm in periclinally in transversal section and 95–105 μm axially in longitudinal section. Cortical region composed of 2–3 layers of progressively smaller cells (Fig. 1f). Cortical cells fairly spaced in optical section; measuring 3–5 × 5–6.5 μm in the apical parts, 6–7 × (8) 9–10 μm in the median parts of the blade and 7–8 × 12–13 μm in the stipe in surface view (Fig. 1g–i). Subcortical cells regularly arranged, visible from the surface. Reproductive structures were not seen.

Remarks

Benhissoune et al. (2002b) report bibliographically the presence of this species based on Bornet’s citation (1892), Debray (1897), Gattefossé and Werner (1935) and Dangeard (1949) for the Atlantic coast of Morocco.

Bornet (1892, p. 285–286) described briefly a specimen as Rhodymenia palmetta var. elisiæ with narrow linear fronds which internal cells are more elongated and cortical cells are larger than those of Phyllophora palmettoides var. niccæensis (Lamouroux ex Duby) J. Agardh; known currently as Schottera nicaeensis (J.V. Lamouroux ex Duby) Guiry & Hollenberg (Guiry and Hollenberg 1975). This report decline all taxonomical features confirming the species supported by Guiry (1977) who examined Bonet’s materiel and concluded that “the material cited by Bornet (1892, p. 285) from Tangiers under the name Rhodymenia palmetta var. ellisiae are probably not representative of this variety”. Similarly, Dangeard (1949, p. 169) mention R. palmetta var. elisiæ without illustrations and/or descriptions of the morphological features useful for species identification. Otherwise, he described another variety such as: “Thallus repetiter dichotomus flabellatus subsessilis, evidenter stoloniferous, fusco-purpureus, usque ad 8 cm. altus, 200 μ crassus.” corresponding to R. palmetta var. fusco-purpurea (P.J.L. Dangeard) S. Benhissoune, C.-F. Boudouresque, M. Perret-Boudouresque, & M. Verlaque. Guiry (1977) affirm that “the material cited by Bornet (1892, p. 285) from Tangiers under the name Rhodymenia palmetta var. ellisiae are probably not representative of this variety to judge from specimens (BM). Dangeard (1949) recorded specimens of this variety from the Atlantic coast of Morocco but his material has not been examined”. Furthermore, there is no description belonging to Debray (1897) and Gattefossé and Werner (1935) inventories. Nevertheless, R. holmesii, under its synonym entities, is only reported in both checklists.

The Moroccan distribution of this species was ambiguous; but with this study, we record and confirm its presence on the Moroccan and the Mediterranean shores.

Our observations are in agreement with general vegetative features previously described by Guiry (1977) as R. pseudopalmata var. ellisiae and Irvine (1983). It is also clearly conforms to the illustrations given by Pérez-Cirera et al. (1989) and the ecology data given by Hiscock and Maggs (1984).

The most conspicuous characters defining Rhodymenia holmesii are the evidence in shape and size of the external cortical cells in surface view and the presence of the stoloniferous basal part. The combination of these characters makes this species clearly distinct from all other Moroccan and Mediterranean species, such as R. caespitosa, R. delicatula P.J.L. Dangeard, R. pseudopalmata and R. pseudopalmata var. fuscopurpurea (Conde et al. 1996; Kazzaz and Riadi 2000; Benhissoune et al. 2002a, 2002b; Antolić et al. 2013). Besides the fact that all these species are characterized by an erect thallus attached to the substrata by a single basal part except R. ardissonei, which have a prostate habit, other characters help to distinguish them from R. holmesii.

This species bears similarity to R. coespitosella L’Hardy-Halos, a species endemic to the French coast in Baie de Morlaix, having a short stipe ending in a small disc and surrounded by many stoloniferous filaments (L’Hardy-Halos 1976). Whereas R. holmesii grows from stoloniferous holdfast with a short stipe, up to 10 mm long. Furthermore, besides the dichotomous branching which is characteristic of almost all the Rhodymenia species; R. coespitosella present blades with 2 to 3 mm in width, although R. holmesii forms a linear frond which maintained more or less the same width for most of its length (5 mm broad). The most conspicuous difference is the external cortical cells dimensions. In R. holmesii, cortical cells are approximately 3–5 × 5–6.5 μm in the apical parts, 6–7 × (8) 9–10 μm in the median parts of the blade and 7–8 × 12–13 μm in the stipe, when in R. coespitosella, the cortical cells are in fact smaller according to the descriptions made by L’Hardy-Halos (1976).

Rhodymenia holmesii shares a prostrate stoloniferous portion with R. leptophylla J.Agardh known from New Zeland (Adams 1994) and R. natalensis Kylin from South Africa (Silva et al. 1996). It differs from the first in that the thalli of this species is thinner with compressed blades 40–150 μm in diameter and from the second by its smaller size and narrower blades (Wynne 1986; Rull Lluch 2002; N’Yeurt and Payri 2010).

As shown in Table 1, one of the most relevant morphological characters to distinguish Moroccan Rhodymenia species R. holmesii, R. caespitosa, R. delicatula, R. pseudopalmata, R. pseudopalmata var. fuscopurpurea and the related species S. nicaeensis is the persistent presence of stolons. Both, R. holmesii and S. nicaeensis share this feature unless they differ by the arrangement of cortical cells. Moreover, the dimensions and the appearance of the cortical and medullary cells of R. holmesii are remarkably different especially the appearance of superficial cells of the stipe. Furthermore, in R. holmesii, specimens attained heights of 80 mm while other Rhodymenia exceed 100 mm high, except the diminutive species R. delicatula which never exceed 22 mm high. The width of the fronds is also an important feature: R. holmesii is never more than 5 mm broad at the median part of the blade while R. pseudopalmata; R. caespitosa; R. pseudopalmata var. fuscopurpurea and S. niccaensis frequently attain 10 mm (Table 1).

Table 1 Morphological characters used to distinguish Rhodymenia holmesii, R. caespitosa, R. delicatula, R. pseudopalmata, R. pseudopalmata var. fuscopurpurea and Schottera nicaeensis

Conclusion

This is the first reference of the occurrence of this species in the the Mediterranean Sea. The recent studies have concluded that present knowledge of the Moroccan and Mediterranean marine flora is still incomplete and indicate that the biodiversity is probably richer than generally thought, because the finding of new records is still relatively frequent. Further phycological studies in that Sea may further increase the known algal biodiversity of the region.

Abbreviations

Not applicable.