Navicula meulemansii sp. nov., (Bacillariophyaceae) from brackish waters in Europe and the U.S.A.

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1 CNova Hedwigia Vol. 98 (2014) Issue 1 2, published online November 20, 2013; published in print February 2014 Article Navicula meulemansii sp. nov., (Bacillariophyaceae) from brackish waters in Europe and the U.S.A. Adrienne Mertens 1, Andrzej Witkowski 2, Horst Lange-Bertalot 3, Lourenço Ribeiro 4* and Erhard Rhiel 5 1 Grontmij Nederland B.V., P.O. Box 95125, NL-1095 HC Amsterdam, The Netherlands 2 Palaeoceanology Unit, Faculty of Earth Sciences, University of Szczecin, Mickiewicza 18, PL Szczecin, Poland 3 Faculty of Biosciences, Institute of Ecology, Phylogeny, Diversity, J.-W. Goethe- University, Senckenberganlage 31 33, D-Frankfurt am Main, Germany 4 Centro de Oceanografia, Faculdade de Ciências da Universidade de Lisboa, Lisboa, Portugal 5 Planktology, ICBM, Carl-von-Ossietzky-University Oldenburg, P.O.Box. 2503, D Oldenburg, Germany With 33 figures and 3 tables Abstract: The new species Navicula meulemansii A.Mertens, Witkowski et Lange-Bertalot sp. nov. is described after study by light microscopy and scanning electron microscopy. Based on new morphological information, the relationship with other taxa is discussed. Navicula meulemansii has a wide geographical distribution in coastal brackish waters (The Netherlands and Germany), European estuaries (Tagus, Portugal), and the San Francisco Bay in California (U.S.A.). Evidence suggests that N. meulemansii has a very broad ecological tolerance, similar to other cosmopolitan species such as Planothidium delicatulum, Navicula gregaria and Nitzschia palea. Key words: Diatoms (Bacillariophyceae), Navicula, new species, brackish water, high conductivity water. Introduction Navicula Bory (sensu stricto), on account of species number, is one of the largest diatom genera (e.g., Cox 1999, Lange-Bertalot 2001). Numerous Navicula species have widespread distributions with a high potential as bioindicators, particularly in *corresponding author 2013 J. Cramer in Gebr. Borntraeger Verlagsbuchhandlung, Stuttgart, Germany. DOI: / /2013/ /2013/0152 $

2 inland waters. Examples include N. tripunctata (O.F.Müller) Bory, a good indicator of eutrophic waters with average to high electrolyte content (Lange-Bertalot 2001), or N. gregaria Donkin and N. veneta Kützing which are common in brackish to electrolyterich, eutrophic waters (Cox 1995). Marine and brackish water Navicula species are less well known than inland water species. Regional brackish water diatom studies by means of light microscopy (LM) include Brockmann (1950), Hendey (1964), Sullivan & Reimer (1975), Witkowski (1994), and a series of publications from the Baltic Sea (Snoeijs 1993, Snoeijs & Vilbaste 1994, Snoeijs & Potapova 1995, Snoeijs & Kasperoviciene 1996, Snoeijs & Balashova 1998). Recent studies by scanning electron microscopy (SEM) of several dozen Navicula taxa new for science include Witkowski et al. (2000), Rumrich et al. (2000), Lange- Bertalot (2001), Van de Vijver et al. (2002), Lange-Bertalot et al. (2003), Metzeltin et al. (2005), Witkowski et al. (2009, 2010), Bahls (2011), Seddon et al. (2011) and Tuji (2011). These examples mostly originate from brackish water locations including the Gulf of Gdańsk (Baltic Sea), the Andes, Uruguay, San Francisco Bay, and oceanic islands (e.g. Ile de la Possession, Iles Kerguelen, and Galapagos Islands). With the exception of small-celled taxa published from the Gulf of Gdańsk (Lange-Bertalot et al. 2003), most recently established Navicula taxa seem to have a limited geographic distribution. In this paper we describe the small-celled Navicula meulemansii A.Mertens, Witkowski & Lange-Bertalot sp. nov. as species new for science. Material and methods Sampling SiteS: Samples from four geographic areas were studied, i.e. inland waters along the North Sea coast of The Netherlands (provinces of Zeeland, Noord- and Zuid-Holland), Dangast (Jadebusen, German Bight, Germany), the Tagus estuary (Portugal), and San Francisco Bay (U.S.A.) (Table 1). The Zeeland province is located in the south-western part of The Netherlands and consists of islands in the Meuse and Scheldt river estuaries. The type locality of Navicula meulemansii is a canal on Noord-Beveland Island, close to the border of the Scheldt estuary, near the De Valle pumping-station. The material from the locations in The Netherlands, consisting of reed stems, originates from routine sampling campaigns by water authorities. The collection, therefore, followed the Dutch periphyton sampling procedures for submerged macrophytes (viz. Bijkerk 2010) and consisted of five submerged reed stems, 0.1 m in length, in each location. The material from the other sites, namely Dangast, Tagus and San Francisco, were collected by the authors from intertidal sediments (epipelic). Sample processing: Samples were cleaned with hydrochloric acid (10%) and hydrogen peroxide (37%) at 80 C to remove calcium carbonate and organic matter. Naphrax was used as a mounting medium. Diatoms were examined by light microscope (LM) and scanning electron microscope (SEM) techniques. LM examination was carried out with a Zeiss Axioskop 40 microscope equipped with differential interference contrast (DIC) optics. Images were produced with a Leica DMLB digital camera with a PLAN-apochromatic 100 (1.4 n.a., numerical aperture) oil immersion objective. For the SEM study, a part of the suspension was filtered through polycarbonate membrane filters with a pore diameter of 3 µm, pieces of which were fixed on aluminium stubs after airdrying. The stubs were sputter-coated with 50 nm of gold. SEM studies were performed with a Hitachi S4500. A total of 70 specimens of Navicula meulemansii from the type locality and the other sampling sites were measured. 202

3 Table 1: Sampling sites, including codes, coordinates, and collectors (AM Adrienne Mertens; AW Andrzej Witkowski; ER Erhard Rhiel; LR Lourenço Ribeiro; SS Scott W.Starratt). Location code NL ( ) EL ( ) collector The Netherlands Canal, pumping station de Valle, Zeeland (Type locality) AM Canal, pumping station Waarde, Zeeland AM Pit Kattendijksedijk, Zeeland AM Marsh near Zeedijk, Schakerlooppolder, Zeeland AM Scour hole Suyderbraec Scharwoude, Noord-Holland MM AM Ditch at junction Hoofdweg W.Voorneweg, Zuid-Holland BOP AM Ditch Steenweg, Zuid-Holland GOP AM Heenvliet pit, Zuid-Holland BO AM Germany North Sea tidal flat (Dangast, Jadebusen) DA ER Portugal Tagus Estuary TE LR USA San Francisco Bay - Salt marsh of Benicia St. Park BP SS Results Taxonomy Order: Naviculales Family: Naviculaceae Genus: Navicula Bory de St. Vincent Section I Navicula sensu Lange-Bertalot (2001) Navicula meulemansii A.Mertens, Witkowski et Lange-Bertalot nov. spec. Synonym: "Navicula spec. 4" sensu Witkowski et al. (2004, Plate 1, Figs 23 26). DeScriptio: Quamvis dimensiones minores frustula comparate fortiter silicificata. Valvae ellipticaelanceolatae, apicibus fere obtuse rotundatis interdum aliquid cuneatis numquam protractis. Longitudo µm, latitudo µm. Raphe paulo lateralis extremis centralibus fere dense sitis inter se. Area axialis anguste sive angustissime lanceolata versus mediam valvarum. Area centralis parva vel vix formata irregulariter asymetrica paucis striis mediis inaequaliter abbreviatis utrimque. Striae transapicales fortius radiantes proximaliter transientes parallelae vel leviter convergentes, in 10 µm. Lineolae striarum comparate satis aspectabiles microscopio photonico non plus quam ca in 10 µm enumeratae microscopio electronico. HolotypuS (hic designatus): Praep in coll. Andrzej Witkowski (SZCZ), Institute of Marine Sciences, University of Szczecin, Poland. Plate 1, Fig

4 ISotypi: slide EcoLIMS nr in coll. Grontmij, Amsterdam, The Netherlands; slide No. ZU8/36 in Friedrich Hustedt Diatom Collection, Alfred Wegener Institute for Polar and Marine Research, Bremerhaven. locus typicus: Gemaal de Valle Zeeland. Coordinates: (Long E, Lat N) Sample (coll. date 24/05/2005) Leg. A.Mertens V etymology: This species is dedicated to Dr. J.T.Meulemans, past director of Grontmij AquaSense, The Netherlands. Description Light microscopy (Figs 1 24): Frustules, in spite of their small size, strongly silicified. Valves elliptic-lanceolate, tapering towards cuneately rounded apices. Valve dimensions (n=70): length µm, width µm, length-to-width ratio 4.1. Raphe weakly lateral, with external central endings noticeably close. Axial area narrow to narrowly-lanceolate, central area small to barely recognizable, irregular or somewhat asymmetrical due to uneven shortening of the middle striae. Striae strongly radiate, halfway towards apices become parallel to weakly convergent, 15 21/10 µm (n=70). Lineolae densely packed, ca /10 µm (n=10), difficult to count under LM due to small valve size and short striae. Scanning electron microscopy (Figs 25 33): Valve face in external view slightly arched, with an abrupt valve face-valve mantle transition (Fig. 25). Valve mantle relatively deep and structureless (Fig. 26). Transapical striae composed of relatively widely spaced areolae. Virgae space much narrower than the striae themselves (Figs 25 29). Valve interior slightly arched, with transapical striae positioned in relatively deep grooves, bordered by virgae that become thicker towards the centre of the valve (Figs 32, 33). The lineolae internal openings are broader than the vimines with the striae/virgae width proportions being opposite to those obvious on the valve surface. Raphe sternum slightly elevated above the valve face level (Fig. 27). Axial area very narrow, parallel to the raphe sternum. Central area small, asymmetric, very slightly expanded, somewhat larger at the valve secondary side than at the primary side (Fig. 26). External central pores distinct, curved, forming drop-like expansions, deflected towards the valve secondary side (Figs 25 31). Raphe apical external endings strongly hooked in the same direction (Fig. 30). The raphe slit is narrower in the central part of the branches than in the proximal and distal ends (Fig. 29). Internally, raphe slits distinctly oblique, terminating in small helictoglossae (Figs 32, 33). Distribution and ecology Navicula meulemansii has been identified in samples collected from intertidal sediments from the Jadebusen near Dangast (Witkowski et al. 2004), the Tagus estuary (Ribeiro 2010, as Navicula cf. microdigitoradiata), the San Francisco Bay area (Witkowski, personal communication), and from inland brackish waters in the Netherlands. In the intertidal areas, it occurred always infrequently and very rarely (i.e. <1% of relative abundance). In the epiphytic samples from the Netherlands, N. meulemansii was also rare (i.e. <2.5 % of relative abundance) to very rare, but occurred in eight different sites, including the type location. Our unpublished observations showed 204

5 Figs Navicula meulemansii A.Mertens, Witkowski et Lange-Bertalot spec. nov. LM. Scale bar = 10 µm. In Fig. 3 holotype specimen is illustrated in DIC microscopy. Figs 1 5 DIC microscopy; Figs 6 24 bright field microscopy. Figs 1 9. Size diminution series of the population of the type habitat (in The Netherlands). Figs Size diminution series of the population from Tagus Estuary, Portugal. the following abundant accompanying species: Catacombas obtusa (Pantocsek) Snoeijs, Cyclotella atomus Hustedt, Navicula gregaria, N. brunellii Poulin, Hudon et Cardinal, N. perminuta Grunow, N. phylleptosoma Lange-Bertalot, N. phyllepta Kützing, Nitzschia inconspicua Grunow, Nitzschia perindistincta Cholnoky, Nitzschia liebetruthii Rabenhorst, Thalassiosira pseudonana Hasle et Heimdal, and T. profunda (Hendey) Hasle. Table 2 provides a summary of salinity and other important environmental parameters from the type locality and from the other seven locations in The Netherlands where N. meulemansii was found. The values for total N and total PO 4 varied up to 26- and 100-fold among the eight locations, whereas the salinity values ranged from 0.3 ppm up to 25.3 ppm. As the physical and chemical parameters presented a rather broad range of values, we assume that Navicula meulemansii tolerates different levels of nutrients (NO x, NH 4 and P) and other environmental variables, such as oxygen concentration, salinity, and ph. In addition, the high levels of nutrient and chlorophyll a concentrations, found in Marsh Zeedijk or Canal Waarde, suggest that this species can be tolerant to eutrophication. However, given that N. meulemansii had low abundances in most of the samples, it is currently difficult to infer its optimal ecological preferences. 205

6 Figs Navicula meulemansii A.Mertens, Witkowski et Lange-Bertalot sp. nov. SEM. Valve face external views. Fig. 25. Valve face external view, arrowheads point to relatively long lineolae (white) and rather narrow virgae (black). Fig. 26. Valve face external view showing the transition of the valve face into the mantle. Note that the transition is areolated and relatively high, whereas the valve mantle is solid (arrow). Arrowhead in the centre of the valve points to central area which is broader at the valve secondary side. Figs. 27 and 28. Valve face external view showing strongly geniculate raphe apical endings (arrow in Fig. 27). All specimens originate from the tidal flat in Dangast. 206

7 Figs Navicula meulemansii A.Mertens, Witkowski et Lange-Bertalot sp. nov. SEM. Figs Valve surface external view. Note the peculiar raphe external central endings (arrow in Fig. 29). Figs 32, 33. Valve internal view, note the transapical striae positioned between relatively thick virgae (arrowheads in Fig. 32). Figs 29, 33 from tidal flat in Dangast. Figs from the type habitat in The Netherlands. 207

8 Table 2: Physical and chemical parameters from different locations in The Netherlands with Navicula meulemansii. Location Date Cl Salinity Conductivity N-NH 4 N-NO 3 N-NO 2 tot-n ortho- tot- SO 4 O 2 O 2 ph BOD 5 Chl-a PO 4 PO 4 (mg/l) ( ) (ms/cm) (mg/l) (mg/l) (mg/l) (mg/l) (mg/l) (mg/l) (mg/l) (%) (mg/l)(mg/l)(mg/l)(mg/m 3 ) Canal de Valle Canal de Valle Canal Waarde < Pit Kattendijkse Dijk Marsh Zeedijk < > Suyderbraec Ditch Hoofdweg Ditch Steenweg Heenvliet pit

9 Table 3: Morphometric characteristics of Navicula meulemansii and related taxa. Data from N. meulemansii are based on measurements made in 70 specimens, with the exception of the lineolae (n=10). Data from other taxa adapted from Lange-Bertalot (2001). N. meulemansii Navicula spec. 4 N. microdigitoradiata N. digitoconvergens N. cryptotenella Length (µm) Width (µm) Length/width ratio Striae in10 µm Lineolae in 10 µm > Valve shape ellipticlanceolate linearlanceolate elliptic- to linear-lanceolate broadly elliptical narrow to broadly lanceolate Valve ends cuneately rounded obtusely rounded obtusely rounded broadly rounded acutely rounded Raphe weakly lateral central pores very close, bent towards valve secondary side weakly lateral central pores close weakly lateral central pores very close weakly lateral distant central pores weakly lateral tear-shaped central pores Central area Striae very small and asymmetric larger to the secondary side strongly radiate, halfway towards the ends, become parallel to weakly convergent above the Voigt s fault small and irregular strongly radiate, convergent at the ends elliptic and very small strongly radiate, parallel to weakly convergent at the ends asymmetric rhombic strongly radiate to convergent at the ends small and irregular radiate, parallel to convergent at the ends Discussion Although Navicula, typified by N. tripunctata (Cox 1979, Lange-Bertalot 2001), is a homogenous genus, it is possible to morphologically distinguish some groups of taxa which seem to be closer related to each other than to others (e.g. Witkowski et al. 1998, Lange-Bertalot 2001). One of such groups is the Navicula digitoradiata (Gregory) Ralfs group, which includes N. microdigitoradiata Lange-Bertalot, N. digitoconvergens Lange-Bertalot, N. cryptotenella Lange-Bertalot, N. capitatoradiata Germain ex Gasse, and N. meulemansii. The most characteristic features of these taxa are: an arched valve face, a deep mantle, a valve interior with relatively deep grooves in which the lineolae are positioned, and radiate and shortened transapical central striae form a peculiar and easily recognizable central area. Species with arched valve face and deep mantles are, nevertheless, within the revised circumscription of Navicula s.s. (Cox 1999), and N. digitoradiata group was placed in Section I Navicula, proposed by Lange-Bertalot 209

10 (2001) which comprises species with similar raphe systems to N. tripunctata, i.e. with external central raphe pores deflected to the secondary side. Our first LM observations suggested that Navicula meulemansii was conspecific with Navicula spec., as illustrated by Witkowski et al. (2000, Plate 126, Figs 8 29), and also to Navicula spec. 4 of Lange-Bertalot (2001, Plate 52, Figs 8 29). Indeed, it was referred before as "Navicula spec. 4" in Witkowski et al. (2004, Plate 1, Figs 23 26). However, this proved not to be correct, as our thorough SEM studies show that N. meulemansii has a number of unique characters, justifying the description as new species. Navicula meulemansii, in its overall morphology, appears to be closely related to Navicula spec. 4 sensu Lange-Bertalot (2001) and N. microdigitoradiata Lange-Bertalot, but N. meulemansii can be distinguished from Navicula spec. 4 sensu Lange-Bertalot by the number of striae and by the significantly lower lineolae density in the latter species. Navicula spec. 4 sensu Lange-Bertalot has lineolae in 10 µm (Lange-Bertalot, 2001), whereas N. meulemansii has in 10 µm. In addition, when the valve shapes of these two taxa are compared, it is clearly visible that N. meulemansii has valves of elliptic-lanceolate shape and distinct acute ends, whereas Navicula spec. 4 has valves with a more linear-lanceolate shape and the apices are slightly set off (Lange-Bertalot 2001). The difference in valve shape between the two taxa is best expressed in length-to-width ratio, which in N. meulemansii amounts to 4.1 whereas in Navicula spec. 4 it is 5.1. Also significant is a difference in the striae number which in N. meulemansii is in 10 µm, whereas it is in 10 µm in Navicula spec. 4 sensu Lange-Bertalot (2001). Morphometric data ranges, as well as descriptions of relevant morphological features of N. meulemansii and similar taxa are summarised in Table 3, for an easier comparison. Data on N. meulemansii are based on our own measurements; whereas the information on similar taxa was adapted from Lange-Bertalot (2001). The general valve outline of N. meulemansii is similar to N. microdigitoradiata although the latter species always has broader valves, even when the specimens of N. microdigitoradiata are very short. The specimen selected as the holotype of N. meulemansii (Fig. 3) is relatively long (27 µm), in comparison with specimens observed from other locations, but it is still narrower (width 5 µm) than N. microdigitoradiata specimens. The two species also differ in terms of stria density which is in 10 µm in N. meulemansii versus in 10 µm in N. microdigitoradiata (Lange-Bertalot 2001). The lineolae density in both species is similar. For N. microdigitoradiata, Lange-Bertalot (2001) stated that the lineolae are "densely packed" and are not resolvable in LM, meaning that their number exceeds 35 in 10 µm. SEM counts of the lineolae density for N. meulemansii were found to be in 10 µm. Navicula digitoconvergens has a valve outline similar to both, N. meulemansii and N. microdigitoradiata, but it is distinctly larger and it has a lower stria density. The cosmopolitan freshwater species Navicula cryptotenella also has broader valves than N. meulemansii (Table 3) and the raphe has narrow, tear-shaped central pores (Lange-Bertalot 2001). None of the established taxa of Navicula s. str. can be confused with the new species. Its combination of characters appears unique, in particular, when the SEM features are considered. However, this also indicates that a correct identification solely by LM is difficult for closely related Navicula species and that probably other methods, i.e. molecular probes and hybridization techniques are needed to provide a clear differential diagnosis. 210

11 Our study points to a possible wide geographical distribution of Navicula meulemansii. This species apparently can live with different levels of nutrient concentrations (Table 2) and has a very broad range of salinity tolerance. In inland brackish waters of The Netherlands, this species was found at salinities ranging from 0.3 to In this respect, it is very similar to true cosmopolitan taxa like Catenula adhaerens (Mereschkowsky) Mereschkowsky, Planothidium delicatulum (Kützing) Round et Bukhtiyarova, Navicula gregaria Donkin, Tabularia fasciculata (Agardh) Williams et Round, and Nitzschia paleacea (Grunow) Grunow. These species are known for their tolerance to a wide range of salinities, from marine to weakly brackish waters, namely inland high conductivity waters which may explain their very broad geographical distribution (e.g. Krammer & Lange-Bertalot 1986, Witkowski et al. 2000, Lange- Bertalot 2001). We expect that further studies will reveal the true worldwide distribution of N. meulemansii. Acknowledgements The authors wish to thank Manfred Ruppel for operating the SEM, John Meulemans for his support, Herman van Dam for his valuable comments, and Grontmij Nederland for their funding. Waterschap Scheldestromen, Waterschap Hollands Noorderkwartier, Waterschap Hollandse Delta disposed chemical data. Dr. Scott W.Starratt has kindly provided samples from Benicia State Park sediment core. Prof. Kevin McCartney is acknowledged for the correction of English language. L.Ribeiro was supported by CO-PEst-OE/MAR/UI0199/2011. This research has also been supported by Polish Ministry of Science and Higher Education grant No. N References BAHLS, L.L. 2011: Three New Species of Navicula (Bacillariophyta) from Oregon and Montana and a Review of Diatom Endemism in the Northwest. N. W. Sci. 85: BIJKERK, R. 2010: Handboek Hydrobiologie. Biologisch onderzoek voor de ecologische beoordeling van Nederlandse zoete en brakke oppervlaktewateren. Rapport , STOWA. Utrecht. BROCKMANN, C. 1950: Die Watt-Diatomeen der schleswig-holsteinischen Westküste. Abh. Senckenberg. Naturf. Ges. 478: COx, E.J. 1979: Studies on the diatom genus Navicula Bory. The typification of the genus. Bacillaria 2: COx, E.J. 1999: Studies on the diatom genus Navicula Bory. VIII. Variation in valve morphology in relation to the generic diagnosis based on Navicula tripunctata (O.F. Müller) Bory. Diat. Res. 14: COx, E.J. 1995: Studies on the diatom genus Navicula Bory. VII. The identify and typification of Navicula gregaria Donkin, N. cryptocephala Kütz. and related taxa. Diat. Res. 10: HENDEy, N.I. 1964: An introductory account of the smaller algae of British coastal waters. V. Bacillariophyceae (Diatoms). HMSO, London. KRAMMER, K. & H. LANGE-BERTALOT 1986: Bacillariophyceae. In: Süßwasserflora von Mitteleuropa. 2/1. Fischer, Stuttgart. Reprint LANGE-BERTALOT, H. 2001: Navicula sensu stricto, 10 genera separated from Navicula sensu lato, Frustulia. Diatoms of Europe 2:

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