Populations of the fragilarioid diatom Synedropsis roundii are described from the phytoplankton of the Albufera of Valencia, a large and shallow eutrophic lagoon in the Spanish Mediterranean coast. The specimens collected are described and illustrated under light and scanning electron microscopy. This is the first documented record of this species since its description, and the first Synedropsis taxon found in the Mediterranean region. The genus was believed to inhabit exclusively marine polar waters until 2003 when S. roundii was described in a tropical coastal lagoon in Brazil. Afterwards, the similar species S. karteteri was also found in a tropical location (Perdido bay, Florida). Both the Albufera lagoon and the type locality (Imboassica Lagoon, SE Brazil) are similar in some ecologically features. The ecological and biogeographical implications of this finding are briefly discussed.
Keywords: Albufera of Valencia, diatoms, biogeography, lagoon, phytoplankton, taxonomy
Synedropsis Hasle et al. is a genus of pennate, araphid diatoms that inhabits preferentially in marine arctic/antarctic communities. The genus was proposed to encompass Fragilaria Lyngb./Synedra Ehr. taxa where the pores in the apical pore field are arranged in slits which are not recessed below the valve surface, and bearing a single rimoportula per valve located close to the apex (Fernandes et al., 2007; Hasle et al., 1994; Medlin and Desdevies, 2016). The genus is relatively recent, with no reports in pre-Holocene deposits (Stachura-Suchoples et al., 2016, but see Srivastav 2003), and current phylogenetic studies show that it is clearly paraphyletic (Karsten et al., 2006), forming a well-supported clade along with other closely related taxa such as Tabularia, Ulnaria, Grammonema, as well as some species of Fragilaria (Belando et al., 2018; Medlin et al., 2008). Actually, Synedropsis is one among many diatom genera separated from Fragilaria after careful ultrastructural investigations. Fragilaria was originally conceived to gather species that form linear colonies, in contrast with the morphologically similar Synedra Ehr. (Hoagland and Rosowski, 1978; Williams and Round, 1987). Since early times, the systematic position of these taxa, together with their subgeneric classification, has been controversial, and the taxonomic problems addressed (with the confluence of phylogenetic and nomenclatural issues) are still not well resolved (Williams, 2006, 2011). Contrary to Synedropsis, Fragilaria cells are characterized by having linking spines and apical pore fields and rimoportulae at the valve ends (Williams, 1986), and the presence of uniseriated striae was later considered also apomorphic (Williams and Round, 1987).
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Current taxonomic databases (Guiry and Guiry, 2018) consider 11 validly published Synedropsis taxa, together with some fossil species (Srivastav, 2003). Until recently, Synedropsis was believed to be exclusively a marine genus with polar distribution (Cefarelli et al., 2016), but in 2003 a Synedropsis bloom occurring in a tropical brackish coastal lagoon in southeastern Brazil was documented (Melo et al., 2003). A new species S. roundii was characterized (Melo et al. 2003) in this habitat. A similar taxon, S. karsteteri Prasad, was reported later in Perdido Bay (Florida), a shallow brackish estuarine bay located in northeastern Gulf of Mexico (Prasad and Livingston, 2005). In this paper, we describe a S. roundii population growing in a Mediterranean coastal lake in the East of Spain, which constitutes the unique occurrence of this species apart from the type locality, together with the first documented record of a Synedropsis taxon in the Mediterranean region.
Materials and methods
The Albufera of Valencia is a shallow, oligohaline lagoon (salinity 1-2 ‰) situated in the Mediterranean Spanish coast (39° 20’ N, 0° 21’ W). It is located in the Natural Park of the Albufera (210 km2), a wetland protected by the Ramsar Convention and the European Habitat list NATURA 2000. It is the largest Spanish coastal lagoon with a surface area of 23.2 km²and an average depth of 1.2 m. Since the last century, the lake functions as a reservoir for the demands of the surrounding rice cultivation. Lake water level is regulated by sluices gates situated on its three outlet channels that flow into the Mediterranean Sea (Romo et al., 2013). Since the 1960s, eutrophication rapidly turned the Albufera lagoon into a turbid, algal dominated state that eliminated submerged macrophytes and reduced general biodiversity (Romo et al., 2005; 2008).
Phytoplankton samples were taken biweekly between February of 2016 and January of 2017 and fixed with Lugol’s solution until laboratory processing. Clean diatom frustule suspensions were obtained oxidizing organic matter with hot hydrogen peroxide 30% v/v. Carbonate inclusions were removed adding a few drops of hydrochloric acid. Permanent microscopic slides were mounted using a refractive resin (Naphrax®). Diatoms were identified under 1000× light microscopy (LM) with a Leica® DM-RB equipped with Differential Interference Contrast (Nomarski) optics. Light microscopy (LM) photographs were taken with an OPTIKA® camera. The scanning electron microscopy (SEM) study was conducted by placing a drop of the cleaned suspension on a metal structure and allowing it to dry at room temperature, then coated with a 10 nm thick gold layer through a High Vacuum Modular Metallization System (QUORUM Q150T ES). Images were obtained with a MERLIN (Carl Zeiss) microscope, operating at 20 kV. Both LM and SEM photographs were adjusted for brightness and contrast using GIMP (GNU Image Manipulation Program v.2.8.).
Synedropsis roundii Torgan et al.
LM observations. Valves narrowly acicular, somewhat broadened in midvalve, with subcapitate to capitate apices. Length 33–46 µm, width 1.3–2.1 µm, ratio 25–30. Axial area rather broad, linear throughout. Transapical striae inconspicuous under LM, opposed throughout, 22–25 in 10 µm, not becoming denser towards apices, interrupted in midvalve forming a fascia. Marginal spines absent. Areolae not resolvable under LM.
SEM observations. Striae formed by only two roundish areolae throughout, one of them in the mantle. Rimoportula at one of both poles only, internally bilobate, almost circular, lying oblique in subpolar position, extended to ca. one half of the valve breadth and opened through a pore-like foramen. Apical pore fields arranged in ocellulimbi consisting on three rows of small porelli, with no outgrowths or apical spines. The central fascia is delimited by ghost striae. The mantle virgae are internally raised. The valve/mantle transition is abrupt, forming right angles. The closed valvocopulae lack apparent perforations. The areola occlusions are seemingly so delicate that they can be discerned only faintly (Melo et al., 2003) and are easily destroyed by the electron beam.
Distribution and ecology. Synedropsis taxa have probably been recorded as either Fragilaria or Synedra spp. or overlooked (Cefarelli et al., 2016). To our knowledge, S. roundii had been only reported in the type locality so far. Previous studies may have already recorded this taxon as Fragilaria famelica (Kütz.) Lange-Bert. in some dune temporary waters of the Albufera Natural Park (Antón-Garrido et al., 2013). An earlier record of S. hyperborea (Grunow) Hasle in the south coast of Murcia, Spain (Bouza and Aboal, 2008) may correspond also to this taxon. In the Albufera lagoon, S. roundii inhabits its phytoplankton forming extensive populations. However, no S. roundii cells were recorded in routine counts performed during summer, when water inflows to the system reach a minimum.
The lack of connecting spines, together with the presence of opposing striae would advise against the ascription of this species to the genus Fragilaria. On the other hand, this taxon exhibits strong affinities with the newly erected genus Williamsella Graeff et al., mainly the presence of an ocellimbus composed of three rows of porelli (as in W. iraqiensis Al-Handal & Kociolek), the occurrence in waters with moderately high conductivities, and the lack of open valvocopulae and conspicuous areola coverings. However, recently Rioual et al. (2017) argued against the separation of Williamsella, demonstrating that its distinctive characters (mainly the absence of spines, their preference for saline waters, and the external coverings of the areolae) can be found also in other Fragilariaceae, so that they rejected the genus by combining the generitype with Fragilaria as F. crenophila (Graeff et al.) Rioual. Besides, the presence of only one rimoportula per valve precludes classifying Synedropsis taxa within Ulnaria (Kütz.) Compère or Tibetiella Y.L.Li et al. (Al-Handal et al., 2016). Contrary to Synedropsis, the striae in the morphologically similar Tabularia (Kütz.) D.M.Williams & Round are biseriate. The closely related Reimerothrix and Creania differ also in the number of rimoportulae, and Grammonema in the ultrastructure of the ocellulimbus. Finally, the comparative tables published (Al-Handal et al., 2016; Garcia, 2012, 2010; Prasad et al., 2001; Fernandes et al., 2007b) show that the combination of characters in Synedropsis is unique.
Synedropsis roundii differs from other Synedropsis taxa by the characteristic valve outline, the number of slits at the valve poles, and by the presence of a single chloroplast per cell (in contrast with the generitype S. hyperborea) (Melo et al., 2003). The individuals depicted here fit well with the diagnostic criteria defined for this species, both in therms of morphometry and ultrastructural characteristics. The most closely related species is S. karsteteri, with shorter valves and denser striae. Noticeably, both taxa share not only morphological but also ecological features, which suggest a recent speciation episode. These taxa—which, contrary to other Synedropsis, do not form colonies—may constitute a separate clade from strictly marine Synedropsis/Grammonema (Medlin et al., 2008; Stachura-Suchoples et al., 2016) with more euryhaline ecological profiles.
In shallow waters, fragilarioid diatoms occur mainly in the epilithon, although planktonic and epiphytic populations are not uncommon (Birnie, 2000). For instance, the dominance of periphytic Fragilaria is indicative of a low water level in the lake (Lutynska, 2008) and turbulence and resuspension conditions (Nicholls et al., 1980). These diatoms are r-strategists, and are thus able to colonize habitats that undergo frequent environmental changes, such as the littoral zones of lakes (Lotter and Bigler, 2000; Mackay et al., 2003). Particularly, Synedropsis taxa exhibit periphytic habits, usually living attached to other larger diatom cells (Olney et al., 2009), or joined to each other through mucilaginous material forming zig-zag and fanlike colonies (Cefarelli et al., 2016).
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Places with confirmed occurrences of S. roundii (Imboassica Lagoon in Brazil and Albufera Lake in Spain) are characterized by the presence of hypertrophic waters. It is well-known that needle-shaped Fragilariaceae are especially common in spring and autumn (King et al., 2006), and may rise facultatively into the plankton during periods of strong mixing (Barker et al., 2001; Marvan et al., 1975), where they can outcompete cyanobacteria due to their ability to exploit phosphorus pulses (Grover, 1988; Horn, 2003; Sommer, 1986).
This is the first confirmed record of S. roundii outside its type locality. Besides, our study broadens the known distribution of the genus beyond marine polar waters by documenting for the first time a Synedropsis population in the Mediterranean region. Thus, we confirm that the species of Synedropsis are not restricted to polar sea ice and the water column nearby and the fact that S. roundii is not endemic to SE Brazil, as previously hypothesized (Prasad and Livingston, 2005). The occurrence of S. roundii in Imboassica Lagoon was restricted to the oligohaline water periods (Melo et al., 2003) and since this species is able to grow under fluctuating salinities, its tolerance to brackish water is more likely to be the result of genetic changes than probably due to a gradual acclimatization to less saline waters (Prasad and Livingston, 2005).
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Fig. 1. Synedropsis roundii in Albufera of Valencia Lake (E Spain). LM images captured at different foci/illumination angles.
Fig. 2. Synedropsis roundii. Cleaned frustules photographed in SEM. (A) Habitus. A whole frustule in tilted view. Note the presence of a rimoportula opening in a single valve and apex. (B) Central area in valve view showing the fascia and the ghost striae. (C) Valve apex lacking rimoportula aperture. Note the uniseriated striae formed by a single areola and the final lateral pores that constitute reduced striae. (D) Valve apex in internal valve view. Note the apical ocellulimbus typical of the genus (filled arrow), the rimoportula (empty arrow) and the internally raised virgae of the mantle. (E) A detail of image A showing the external foramen of the rimoportula (arrow). (F) Frustule apex in connective view. Note the mantle stria formed by a single areola, the absence of spines and the unperforated valvocopula.
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