Navicula dermochelycola sp. nov., presumably an exclusively epizoic diatom on sea turtles Dermochelys coriacea and Lepidochelys olivacea from French Guiana

Epizoic diatoms have been described from diverse hosts (from invertebrates to vertebrates) and diverse environments (from freshwater to marine; see i.e. Wuchter et al. 2003; Wetzel et al. 2010; Riaux-Gobin & Witkowski 2012; Romagnoli et al. 2014; Frankovich et al. 2016; Riaux-Gobin et al. 2017 and references therein). Several genera have been described as presumably obligately epizoic (or potentially commensal, even if no specific study on real relationships between the host and the diatom has ever been published), including Epipellis R.W. Holmes, Bennettella R.W. Holmes (Holmes 1985; Holmes & Nagasawa 1995; Denys & Van Bonn 2001; Denys & De Smet 2010), Epiphalaina R.W. Holmes, Nagasawa & Takano, Plumosigma T. Nemoto, Tursiocola R.W. Holmes, Nagasawa & Takano (Nemoto 1956; Holmes et al. 1993; Denys 1997), Chelonicola Majewska, De Stefano & Van de Vijver and Poulinea Majewska, De Stefano & Van de Vijver (Majewska et al. 2015) and Medlinella Frankovich, Ashworth & M.J. Sullivan (Frankovich et al. 2016). At the species level, several diatoms have also been described as possibly obligate epizoic, including Tripterion kalamensis R.W. Holmes, S. Nagasawa & Takano (1993) and Tripterion philoderma R.W. Holmes, S. Nagasawa & Takano (1993), Pseudofalcula hyalina (Takano) F. Gómez, L. Wang & S. Lin (Takano 1983; Gomez et al. 2018), Pseudohimantidium pacificum Hustedt & Krasske in Krasske (Krasske 1941; Fernandes & Calixto-Feres 2012), Luticola deniseae Wetzel, Van de Vijver & Ector (Wetzel et al. 2010), and Mastogloia sterijovskii A. Pavlov, Jovanovska, C.E. Wetzel, Ector & Levkov (Pavlov et al. 2016).

In 2014–2018, a total of 142 sea turtles from the Equatorial West Atlantic, the Caribbean Basin and the South Pacific were sampled. In the course of these studies, presumably an exclusively epizoic species of Navicula was encountered. The purpose of the presented report is to describe this new taxon based on light and scanning electron microscopy observations.

Navicula dermochelycola Witkowski, Kociolek & Riaux-Gobin sp. nov. LM Fig. 1a–e, SEM Figs 2–4, Table 2.

Figure 1a–e (LM)

Figure 2a–g (SEM)

Figure 3a–d (SEM)

Figure 4a–c (SEM)

Description: Valves small (15–25 μm long, 4–5 μm wide), lanceolate to linear-lanceolate, with subrostrate to capitate apices (with varied shapes of apices in smaller specimens; Fig. 1a–e, Fig. 2a–e). In LM, a distinct terminal hyaline area is visible at each apex (Fig. 1a–e), corresponding to the helictoglossa and adjoining structure detailed with SEM (Fig. 3b).

External view (SEM): Raphe filiform, axial area very narrow and linear. Central area moderately expanded, round to irregular, more or less symmetrical, delineated by alternately longer and shorter striae on both sides of the raphe (Fig. 2a–e). Proximal raphe endings distant, slightly expanded and bent toward the valve primary side (opposite to distal raphe endings; Fig. 3a–c). Distal raphe ends hooked, typical for Navicula sensu stricto (Fig. 2c). Transapical striae radiate, in the middle strongly arched around the central area, becoming slightly convergent toward the apices. Striae equidistant, 24–30 in 10 μm. Transapical striae composed of apically elongate areolae, aligned along a rhombic pattern, ca. 50 in 10 μm. Valve surface flat with oblong striae forming areolae positioned between slightly raised virgae (Fig. 2g).

Internal view (SEM): Raphe slit opening laterally along an elevated rib (Fig. 4a). Internal proximal raphe endings close to each other and simple (Fig. 4c). Raphe terminating distally as an obliquely-positioned helictoglossa surrounded by an elevation or thickened terminal nodule (Fig. 4b), corresponding to the hyaline apical area observed in LM (see above). Girdle narrow, composed of several open and plain copulae. The margin of the valvocopula externally ornamented with one raw of short transapical and elongate puncta or slits (7 in 500 nm, Fig. 3d), absent on the head pole (= closed pole) of the copula.

Holotype: LM slide BM 101 943 (National History Museum, London, U.K.); illustrated in Figure 1.

Isotypes (here designated): Slide SZCZ 25795 in collection A. Witkowski (Institute of Marine and Environmental Sciences, Szczecin, Poland).

Type locality: Nesting Dermochelys coriacea ‘103’ from the Equatorial West Atlantic (French Guiana, locality Yalimapo); 5°44’47.96”N; 53°56’37.36”W. Collector: Damien Chevallier.

Etymology: The epithet dermochelycola was given referring to the turtle host, Dermochelys coriacea (“dermochely” from the turtle host Dermochelys, and “cola” from colere, meaning living in Latin).

Distribution: Found on seven nesting DC from French Guiana (localities: Yalimapo and Aztèque) out of 20 specimens analyzed. Found also on one nesting LO (locality: Cayenne, French Guiana) out of six specimens analyzed. Apparently absent on other turtle species (83 CM, 13 EI) and observed only in French Guiana.

Taxonomic remarks: This diatom is unique among many species of Navicula due to the areolae of striae, which are more ellipsoidal in this new taxon. Our new species resembles Navicula rostellata Kützing (Table 2), but the central striae are alternately longer and shorter (Fig. 2g), and the new species is distinguished by a higher stria density compared to N. rostellata (28 in 10 μm, versus 12–14 in N. rostellata). N. rostellata is a freshwater taxon (Kützing 1844; Lange-Bertalot 2001; Potapova & Kociolek 2011), even if also reported from brackish and marine habitats. The new species also shares some similarities with Navicula salinarum Grunow, but is distinguished by a higher stria density compared to N. salinarum (13–17 in 10 μm in N. salinarum) and a different valve shape (roughly elliptical-lanceolate in N. salinarum; Krammer & Lange-Bertalot 1986; Patrick & Reimer 1966; Kociolek 2011). Widespread Navicula capitatoradiata Germain (Germain 1981; Rushforth & Spaulding 2010) also shares some similarities with our new species, but is lanceolate in shape, has a lower stria density and a smaller central area compared to our taxon (Germain 1981; Gasse 1986; Lange-Bertalot 2001). Navicula fucicola Taasen (Taasen 1975), which is endophytic in “the mucilage of the apical slit of Fucus vesiculosus L.” (op. cit.: p. 5), also shares some similarities with the new taxon in terms of size and striae densities (12–22 μm in length, 5–7 μm in width, 20–24 striae in mid-valve, 24–28 near apices), but the latter is broadly elliptic-lanceolate in contrast to N. dermochelycola sp. nov., which is lanceolate to linear-lanceolate.

The central area in N. fucicola is also less expanded than in our new taxon (Taasen 1975). It should be noted that the ornamentation on the valvocopula of N. dermochelycola sp. nov. (one row of short slits; Fig. 3c–d) seems unusual for this genus.

Behavioral studies of marine turtles have not reported any deaths or diseases due to macro- and micro-flora associated with their carapace and skin, while deaths due to accidental fishing (Finkbeiner et al. 2011 and references therein) or following the ingestion of plastics (Nelms et al. 2015; Wilcox et al. 2018; Yaghmour et al. 2018) are confirmed and listed. Furthermore, studies describing cleaning stations for sea turtles (Sazima et al. 2010) tend to prove that turtles come there to restrict the proliferation of algal epibiont material on their bodies and are not that much inconvenienced by them. We can therefore hypothesize that diatoms (such as Navicula dermochelycola sp. nov.) live in a close relationship with their host and that the term commensalism (no vital damage to one with respect to the other, but shelter for diatoms and perhaps a mode of dissemination) can be used. However, we have used the term “presumably exclusively epizoic” throughout the text.

On the other hand, diatoms as well as macroalgae need light to grow, even if epizoic Tursiocola from Manatees was demonstrated to be apochlorotic (Frankovich et al. 2018). Thus, an excessive sediment discharge, such as the one by the Amazon River to the Guiana coast, may affect the acclimation of diatoms on turtles, possibly explaining the very poor colonization on turtles in that region (Riaux-Gobin et al. in revision). Moreover, DC is considered to be the most deep-diving sea turtle (Bjorndal 1996; Dodge et al. 2011), which probably prevents effective growth of diatoms.

Nevertheless, 33% of the DC individuals examined in this study host a specific diatom (Navicula dermochelycola sp. nov.) that has never been found elsewhere, except for one LO individual from the same environment (as mentioned above). The acclimation of this taxon may also be due to the specific structure of the leather-like carapace of DC.

As a result of the present survey of sea turtles from tropical sectors of the Atlantic and Pacific oceans, a new benthic diatom taxon is reported, which so far has never been found in another environment. Navicula dermochelycola sp. nov. was only present in French Guiana and mainly hosted by DC.