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Scrapings from several juvenile Chelonia mydas Linnaeus (green turtle) from Eastern Caribbean and adults from French Guiana allowed for the description of two small and relatively rare epizoic Tursiocola species (Bacillariophyta). Differences with the other eight Tursiocola species previously described are discussed here. Particular attention is given to the cingulum of the two new species and a conceptual key is proposed for Tursiocola species, based on the cingulum structure.
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Two new Tursiocola species (Bacillariophyta) epizoic on green turtles (Chelo-
nia mydas) in French Guiana and Eastern Caribbean
Catherine Riaux–Gobin1,2*, Andrzej WitkoWski3, Damien ChevallieR4 &
Genowefa DaniszeWska–koWalCzyk3
*1 PSL Research University: CNRS–UPVD–EPHE, USR3278 CRIOBE, 2 Laboratoire d’Excellence ‘CORAIL’,
University of Perpignan, F–66860 Perpignan, France; *Corresponding author e–mail: catherine.gobin@
univ–perp.fr
3 University of Szczecin, The Faculty of Geosciences, Palaeoceanology Unit, PL–70–383 Szczecin, Poland,
witkowsk@univ.szczecin.pl
4 UMR 7178–CNRS–Unistra, Institut Pluridisciplinaire Hubert Curien, FR–67087 Strasbourg, France, da-
mien.chevallier@iphc.cnrs.fr
Abstract: Scrapings from several juvenile Chelonia mydas linnaeus (green turtle) from Eastern Caribbean
and adults from French Guiana allowed for the description of two small and relatively rare epizoic Tursiocola
species (Bacillariophyta). Differences with the other eight Tursiocola species previously described are discussed
here. Particular attention is given to the cingulum of the two new species and a conceptual key is proposed for
Tursiocola species, based on the cingulum structure.
Key words: Epizoic diatoms, sea turtles, Tursiocola, morphology, autecology
IntroductIon
Between 1920 and 1958 (bennet 1920; haRt 1935;
omuRa 1950; husteDt 1952; okuno 1954 and nemoto
1956,1958) and more intensively during the last three
decades, increasing interest was given to epizoic dia-
toms (see holmes 1985; van bonn & Denys 1997;
Denys 1997; FRankoviCh et al. 2015a). This has led to
the description of several genera exclusive to this type
of habitat. The first detailed taxonomic investigations
concerned diatoms known to colonize whales, with the
creation of two new achnanthoid genera Bennettella
R.W.holmes and Epipellis R.W.holmes (e.g., holmes
1985; holmes & naGasaWa 1995; Denys & van bonn
2001; Denys & De smet 2010). Until now, both ge-
nera were only known in association with cetaceans.
After 1985, several new diatom genera and species
were discovered and shown to colonize metazoans
(e.g., molluscs, holothurians; see totti et al. 2011; Ri-
aux–Gobin & WitkoWski 2012) and vertebrates (e.g.,
cetaceans, turtles and manatees) from contrasting envi-
ronments (holmes et al. 1993a,b; van bonn & Denys
1997; Denys 1997; FRankoviCh et al. 2015a,b; Pavlov
et al. 2016; Riaux–Gobin et al. 2017), including the
new genera Plumosigma T.Nemoto (nemoto 1956),
Epiphalaina R.W.holmes, naGasaWa & takano (hol-
mes et al. 1993a), Tursiocola R.W.holmes, naGasaWa
et takano (holmes et al. 1993a), Tripterion R.W.hol-
mes, naGasaWa et takano (holmes et al. 1993a), Che-
lonicola majeWska, De steFano et van De vijveR (ma-
jeWska et al. 2015), Poulinea majeWska, De steFano et
van De vijveR (majeWska et al. 2015) and Medlinella
FRankoviCh, ashWoRth et m.j.sullivan (FRankoviCh
et al. 2016).
The species within the genera Epiphalaina and
Tursiocola show very similar morphologies and are
characterized by their small size, an acicular shape and
the presence of pseudosepta. They mainly differ throu-
gh an internal butterfly–shaped structure in Tursiocola
(holmes et al. 1993a: p. 7). Eight Tursiocola species
are currently reported in the literature, with T. podoc-
nemicola C.e.Wetzel, van De vijveR et eCtoR from
a freshwater turtle Podocnemis erythrocephala sPix
(Wetzel et al. 2012), T. denysii FRankoviCh et m.j.su-
llivan from a Loggerhead sea turtle Caretta caretta
(linneaus) (FRankoviCh et al. 2015b), three taxa from
a manatee from Florida Bay (FRankoviCh et al. 2015a),
and the other taxa from whales and Dall’s porpoises
(nemoto 1956; holmes et al. 1993a,b; Denys 1997).
Only three Epiphalaina taxa have been described
thus far, and all were from cetaceans (nemoto 1956;
holmes et al. 1993a,b; Denys 1997). As reported by
150 Fottea, Olomouc, 17(2): 150–163, 2017
DOI: 10.5507/fot.2017.007
Riaux–Gobin et al.: Two new Tursiocola species 151
Wetzel et al. (2012), bRaDy (2010) also found an uni-
dentified Epiphalaina or Tursiocola species on several
species of marine turtles from the Gulf of Mexico. Re-
cently, Robinson et al. (2016) illustrated a Tursiocola
sp. (ref. cit. fig. 2,D).
Scrapings from several juvenile Chelonia my-
das linnaeus (green turtle) from the Lesser Antilles
(Eastern Caribbean) and adults from French Guiana
allowed for the description of two additional species
that can be assigned to Tursiocola due to their charac-
teristic internal structure. Differences with the eight
previously described Tursiocola species are discussed
here. Particular attention is given to the cingulum com-
plex of both new species.
MaterIal and Methods
Materials used in this study were derived from two sour-
ces: 1) scrapings from the carapace of several wild juveni-
le Chelonia mydas from Martinique Island (Grande Anse
d’Arlet 14°30'10.95"N, 61°05'13.00"E and Anse du Bourg
14°29'13.43"N, 61°04'58.88"E, 12–13 October 2015,
CNRS–IPHC survey), 2) scrapings from the carapace of se-
veral nesting adult Chelonia mydas in Aztèque, French Gui-
ana (48° 51' 45.81"N, 2° 17' 15.331"E, 07 April 2016). The
latter samplings were carried out by D.C. during ANTIDOT
surveys (CNRS–IPHC program) which investigated the mi-
gratory behavior of several species of marine turtles, using
genomic, Capture–Mark–Recapture (CMR) and satellite
tracking to understand the migration behavior of the different
turtle species.
The samples were all very small and the described
taxa are relatively scarce. For light microscope (LM) ex-
amination, the samples were washed with distilled water
to remove salts, treated with 30% H2O2 for 2 h at 70 °C to
remove organic matter, rinsed several times in distilled water,
alcohol–desiccated and mounted on glass slides using Na-
phrax®. Diatom slides were examined with a Zeiss Axiophot
200, with differential interference contrast (DIC) optics and
photographed with a Canon PowerShot G6 digital camera
(CRIOBE–USR 3278, Perpignan, France). For SEM exami-
nation, the samples were ltered through 1 µm Nuclepore®
lters and rinsed twice with deionised (milliQ) water to re-
move salts. Filters were air–dried and mounted onto alumi-
num stubs before coating with gold–palladium alloy (EM-
SCOP SC 500 sputter coater) and examined with a Hitachi
S4500 SEM operated at 5 kV, calibrated with a Silicon grat-
ing TGX01 (C2M, Perpignan, France).
‘Foot pole’ (F) and ‘head pole’ (H) refer to ‘the length
between the apex of the valve (foot or head) and the middle
of the central area of the valve’. The ratio (F/H ± σ) is an ap-
proximate measure of the degree of heteropolarity of the cell.
Terminology and abbreviations. For the description of
the frustule and its parts, terminology follows anonymous
(1975), Ross et al. (1979) and RounD et al. (1990).
results
In addition to Chelonicola spp. and Tripterion spp.,
several of the turtle scrapings revealed two rare and
acicular taxa from the genus Tursiocola. One very
small sample (‘31CM’ from a nesting Chelonia mydas
from Aztèque, see Mat. & Meth.) was found to have
both Tursicola species, one of which is very rare. In
LM it is almost impossible to separate and correctly
discriminate the two latter taxa.
Light microscopy (Figs 112): A total of 12 frustules
or valves were photographed (Figs 1–12). Pseudosepta
are visible on each image. The striation of the valves is
barely visible and difcult to resolve. Figs 7–12 likely
illustrate the dominant species (Tursiocola yin–yangii
sp. nov., see below), which is slightly more acicular
and smaller than the second taxon (T. guyanensis sp.
nov.) possibly illustrated in Fig. 6 (see SEM descrip-
tion of each taxon). In cingular view (Figs 1–5) it is
almost impossible to distinguish between the two taxa,
as their stria densities are very similar (see below).
Taxonomic notes: In LM, Tursiocola yin–yangii sp.
nov. and T. guyanensis sp. nov. are most similar to Tur-
siocola staurolineata Denys (Denys 1997, gs 42a–
52) and T. olympica (husteDt) holmes, naGasaWa et
takano (Denys 1997, gs 65–75; FRankoviCh 2015b,
gs 31–33), except for their average smaller size. How-
ever, these two species are also similar to Epiphalaina
aleutica var. aleutica (holmes et al. 1993a, gs 1–2;
Denys 1997, gs 1–10) and to E. aleutica var. lineata
(Denys 1997, gs 24–39, no SEM). SEM was therefore
essential for a full description of the new taxa.
Tursiocola yin–yangii rIaux–GobIn et WItoWskI sp.
nov. (Figs 7–12, 13–29)
Description: Valves small, acicular, with acute apices
[n = 66 (SEM); 8.7–14.5 µm (mean ± σ 11.7 ± 1.4)
long; 1.32–1.37 µm wide; 36–42.8 striae in 10 µm
(mean ± σ 39.7 ± 1.6); length/width 7.8 (Table 1)].
Frustule biraphid, isovalvar, rectangular in girdle view.
Valve face not cuneate. Very slight difference between
the length of the raphe branches (see SEM morpho-
logy). Pseudosepta present. Complex cingulum com-
posed of numerous narrow copulae (see SEM). Never
in chains. Found as epizoic on Chelonia mydas.
SEM morphology
Externally: Pole showing the valvocopula closed pole
[with a second short row of puncta (see below)] is just
slightly longer than the other pole (n = 27, ratio F/H
± σ 0.99 ± 0.05), e.g., the specimen illustrated in Fig.
16 has a head pole that is signicantly longer than the
foot pole and a slightly cuneate shape in girdle view
(foot pole slightly narrower). Valve margins straight to
slightly undulate. Striae uniseriate, parallel to slightly
radiate, denser on both apices. Each stria is composed
of four areolae externally ornamented by an ‘S’–shaped
opening resembling a yin–yang symbol (Figs 14–15,
17, 19–22). Each areola is internally closed by a round
and domed hymenate pore occlusion (Fig. 28, position
Figs 1–12 (LM): (7–12) Tursiocola yin–yangii sp. nov.; (6) Tursioco-
la guyanensis sp. nov. Note the pseudoseptae and the barely visible
valve striation. In girdle view (Figs 1–5) it is almost impossible to
distinguish between the two taxa. Scale bars 10 µm.
of slits or perforations is not apparent in SEM). Pres-
ence of a relatively wide and slightly bow–tied stauros
(the striae delineating the central area are divergent,
Figs 14–15), void of areolae up to the margins and
externally thickened (Figs 14–15). Raphe liform and
straight. Proximal raphe endings well separate, spathu-
late and straight–coaxial (Fig. 14). Terminal raphe s-
sures hooked on the same side and terminating in a sort
of contorted areola (Fig. 17). Small apical area void of
areolae (Fig. 17 arrow). Cingulum composed of up to
5 copulae on each valve. The valvocopula appears to
be open and narrow, with one advalvar row of round
puncta which are slightly denser than the striae, and a
supplementary short row of scarce and larger puncta
on its closed pole. These supplementary puncta, sym-
metrically positioned on both valves (Fig. 21 arrow-
heads), give a polarity to the frustule. The pole with
the supplementary puncta (on the closed pole of the
valvocopulae) may correspond to the head pole of the
frustule (Fig. 23 arrowhead). The other copulae (up
to four) are open, narrow and show only one row of
puncta (Figs 19–22).
Internally: A pseudoseptum extends from the apices
as siliceous plates covering ca. one–fourth of the valve
length on each apex (Figs 24–26). The pseudoseptum
continues as very narrow strips along the valve mar-
gins (Fig. 28 arrows), and widens into two concave
wings in the central area, creating a relatively narrow
‘buttery–like’ structure (Figs 24, 28). The raphe lies,
more or less symmetrically, on the top of a siliceous rib
(Fig. 28). One unique pearl–like knob lies in between
the proximal raphe endings (Fig. 28). On cleaned mate-
rial, it is possible to see the ‘S–shaped’ external open-
ing of each areola (Fig. 27 arrow) through the internal
corroded hymenes (Fig. 27 arrowhead shows the pe-
riphery of the corroded hymen).
Holotype: Specimen on the SEM stub BM001231764
(National History Museum, London, U.K.) illustrated
in Fig. 13.
Isotypes (Here designated): Slide BM 101 856 (Natu-
ral History Museum, London, UK), Slide SZCZ 24042
in collection a. WitkoWski (The Faculty of Geosci-
ences, Szczecin, Poland).
Type locality: Nesting Chelonia mydas from French
Guiana (Site ‘Aztèque’) (48°51'45.81"N, 2°17'
15.331"E). Sample named ‘31CM’. Sampling date: 07
04 2016. Collector: Damien ChevallieR.
Etymology: The epithet was given in reference to the
‘S’–shaped external opening of the areolae, resembling
a yin–yang symbol.
Habitat: Wild nesting Chelonia mydas in French Gui-
ana.
Taxonomic notes: Characterized by its small size,
narrow and linear shape, complex cingulum and unique
external areola opening, this taxon is relatively easy to
distinguish from other Tursiocola species (Table 1).
Tursiocola guyanensis rIaux–GobIn et WItoWskI sp.
nov., Figs 30–44.
Description: Very rare, valves small, narrow–elliptical
to acicular, with round apices [n = 21 (SEM); 12–13.9
µm (mean ± σ 12.9 ± 0.7) long; 1.70 µm wide; 33–
40.6 striae in 10 µm (mean ± σ 37.9 ± 1.7); length/
width ca. 7.8]. Frustule biraphid, isovalvar, rectangu-
lar in girdle view. Very slightly heteropolar, though the
difference between the length of the raphe branches is
difcult to discern (see SEM morphology). Speudo-
septa present. Complex and wide cingulum composed
of numerous copulae (see SEM). Never found in chains
in fresh material. Epizoic on Chelonia mydas.
SEM morphology
Externally: Valve margins with three undulations
(Fig. 30). Pole of the frustule showing the closed pole
of the copula n°2 (see below), very slightly longer
than the other pole. Striae uniseriate, in higher densi-
ties on both apices, parallel to very slightly divergent
on mid–valve, composed most often of four oblong
transapically elongate areolae that are constricted two
to three times along their length (Fig. 31 arrowhead).
Areolae close to the raphe are diamond–like or quad-
rangular (Figs 33 arrowhead). Areolae of the apex, near
the mantle, often vermiform or with three (or more)
constrictions (Fig. 34 arrowhead). Areolae internally
closed by domed hymenes (Fig. 44, arrowhead, slits
or perforations not apparent in SEM). Relatively large
stauros (slightly bow–tied, Fig. 32), void of areolae up
to the margins, externally thickened. Raphe straight.
152 Fottea, Olomouc, 17(2): 150–163, 2017
DOI: 10.5507/fot.2017.007
Figs 13–18 (SEM external views), Tursiocola yin–yangii sp. nov.: (13) holotype specimen; (13, 16) entire frustules, (16) specimen slightly
wedge–shaped in girdle view, foot pole slightly narrower, and head pole with the valvocopulae closed poles (arrowheads); (15) striae compos-
ed of two rows of sigmoid areolae; (14) central area with a domed fascia and spathulate proximal raphe endings; (15) striae composed of three
to four areolae; (16) somewhat spaced slightly narrower near both poles; (18) frustule acicular in valve view; (17) detail of apex (head pole)
with a terminal raphe ending terminating in a contorted areola (arrow) and the valvocopula showing one row of round puncta and a supplemen-
tary row of scattered larger puncta (arrowhead). Scale bars 3 µm (16); 2 µm (13, 18); 500 nm (14, 15, 17).
Riaux–Gobin et al.: Two new Tursiocola species 153
Figs 19–23 (SEM, external views). Tursiocola yin–yangii sp. nov.: (23) entire frustule in girdle view with the head pole showing the closed pole
of the valvocopula (framed arrowhead); (19–22) the margins of the cingular bands are demarcated; (19–21) details of the frustule head pole
with the closed apex of the valvocopula (arrowheads, copulae annotated ‘1’) and open supplementary copulae (annotated ‘2’ to ‘5’); (22) detail
of the frustule foot pole with the open apex of the valvocopula; (21, 22) the same frustule. Scale bars 2 µm (23); 1 µm (20–22); 500 nm (19).
154 Fottea, Olomouc, 17(2): 150–163, 2017
DOI: 10.5507/fot.2017.007
Figs 24–29 (SEM, internal views), Tursiocola yin–yangii sp. nov.: (24) entire valve; (25–26) details with the pseudoseptum extending on both
apices and continuing as narrow strips along the margins; (27) striae are parallel. Detail of the areolae with corroded hymenes (arrowhead) and
underlying sigmoid areola apertures (arrow). (28) detail of the central area with the buttery structure, raphe slightly lateral and a single knob
in between the proximal raphe endings, note the narrow strips along the valve margins; (29) broken frustule with the sigmoid external areola
apertures (arrow), the section of the buttery structure (framed arrowhead) and the internally domed areola hymenes (arrowhead). Scale bars
3 µm (24), 1 µm (25–26), 700 nm (29), 400 nm (28), 200 nm (27).
Riaux–Gobin et al.: Two new Tursiocola species 155
Figs 30–35 (SEM). Tursiocola guyanensis sp. nov.: (32) frustule in valve view; (30) frustule in girdle view, valvocopula apices with vermiform
puncta (arrowheads); (35) central area with a fascia and spathulate proximal raphe endings; (31) fascia in girdle view (arrow), areolae vermi-
form with two to three constrictions (arrowhead); (33) detail of the valve apex with a reinforcement in one side of the terminal raphe ending,
and diamond–like areolae near the raphe (arrowhead); (34) apex in girdle view with the raphe ending terminating in a contorted areola (arrow),
areolae vermiform on the mantle and on the valvocopula apex (arrowheads). Scale bars 3 µm (30), 2 µm (32), 1 µm (31), 500 nm (33–35).
156 Fottea, Olomouc, 17(2): 150–163, 2017
DOI: 10.5507/fot.2017.007
Figs 36–40 (SEM, external views), Tursiocola guyanensis sp. nov.: (40) entire frustule in girdle view with black shadows corresponding to the
siliceous internal septa and central structures (arrows); (36–39) detail of the frustule apex (the margins of the cingular bands are demarcated)
with vermiform puncta on the pole of the valvocopulae (annotated ‘1’, Fig. 37 arrowheads), with the presence of 5 supplementary open copulae
(annotated ‘5’ to ‘6’). Figs 39 (valve head pole, with the closed pole of the 2nd copula) and Fig. 38 (valve foot pole) of the frustule illustrated
in Fig. 40. Scale bars 3 µm (40); 2 µm (36–39).
Riaux–Gobin et al.: Two new Tursiocola species 157
Proximal raphe endings coaxial, well separated and
spathulate. Terminal raphe ssures strongly hooked on
the same side, externally ending in a vermiform areola
(Fig. 34 arrow). Small apical area void of areolae (Fig.
33). Wide cingulum, composed of numerous copulae
(up to 6 per valve). The valvocopula is wide, with an
advalvar row of round to oblong poroids and a second,
abvalvar, apical row (1/4 of the valve length, on each
apex) with transapically elongate and vermiform po-
roids (Fig. 37 arrowheads) with more or less the same
density as the striae. The supplementary copulae have
only one row of puncta that decrease in diameter from
the 2nd to the 6th copula (e.g., in Figs 37, 38). The 5th and
6th copulae are weakly silicied and narrow. Frustule
head pole and foot pole are very similar and hard to
distinguish. The closed pole of the 2nd copula points out
of the head pole of the cell.
The transapically elongate and vermiform
puncta on both apices of the valvocopulae are very si-
milar to the areolae on the valve apices (Figs 37–38
arrowheads). These vermiform puncta are present sy-
mmetrically on both apices of the valvocopula. The
valvocopulae appear to be closed and present tabs stan-
ding on the wings of the central structure (Fig. 43). In
cleaned material we found no free valvocopula, only
narrow open cingular bands, impossible to be attribu-
ted to T. yin–yangii sp. nov. more than to T. guyanensis
sp. nov. More observations are needed to clearly de-
scribe each cingular band.
Internally: Presence of a transverse, narrow and thic-
kened structure (Figs 41–44), with lateral expansions
reminiscent of a buttery (Fig. 43 arrows). A picture
of the entire pseudoseptum has not yet been obtained.
In Fig. 40 (arrows) the black shadows at each pole of
the frustule and on the central part, mark the presence
of siliceous internal thickenings corresponding to the
septa and central structures.
Holotype: Specimen on the SEM stub BM001231764
(National History Museum, London, U.K.) illustrated
in Fig. 32.
Isotypes (Here designated): Slide BM 101 856 (Natu-
ral History Museum, London, UK), Slide SZCZ 24042
in collection a. WitkoWski (The Faculty of Geosci-
ences, Szczecin, Poland).
Type locality: Nesting Chelonia mydas in French Gui-
ana from ‘Aztèque’ (48°51'45.81"N, 2°17'15.331"E).
Sampling date: 07 04 2016. Collector: Damien Che-
vallieR. Also present, as rare, on juvenile Chelonia
mydas at ‘Anse du Bourg’, Lesser Antilles (14° 29’
13.43’’N, 61°44 58.886’’W).
Etymology: The epithet guyanensis was given in refe-
rence to French Guiana (Guyane), the location where
the species was rst found.
Habitat: Nesting wild adult Chelonia mydas from
French Guiana, host Tursiocola guyanensis sp. nov.
In sample ‘31 CM’, this latter taxon is rare, while T.
yin–yangii sp. nov. is more abundant. T. guyanensis
was also observed as very rare on 3 juvenile specimens
of Chelonia mydas from Martinique Islands (Lesser
Antilles). Until now, this species was not observed in
samples taken from Chelonia mydas from the South
Pacic, nor were they found on Dermochelys coriacea
(leatherback turtle), or Lepidochelys olivacea (olive
Ridley turtle) from Guiana.
Taxonomic notes: The internal central area of Tursio-
cola guyanensis (Figs 40–43), with a narrow silicied
transverse structure and semblance of wings (Fig. 42
arrows), are characteristic of the genus Tursiocola.
There are similarities between our taxon and T. deny-
sii FRankoviCh et m.j.sullivan in FRankoviCh et al.
(2015b). T. denysii, like our taxon, has closed valvo-
copulae ornamented on their apices by a second row of
puncta simply referred to as ‘abvalvar pores’ (ref. cit.,
g. 28 arrow). In T. guyanensis sp. nov, the poroids
are long and vermiform. Furthermore the valvocopu-
lae in T. guyanensis sp. nov. are wide whereas those
in T. denysii seem more narrow. Additional features
that differentiate the two taxa include the following:
T. guyanensis sp. nov. is more acicular than T. denysii
(length/width = ca. 7 in T. guyanensis versus ca. 4.8 in
T. denysii), with striae less strongly radiate, less areolae
per stria and most likely a more complex cingulum.
Furthermore, the areolae in T. denysii are described as
‘transapically elongated’ but not constricted in their
middle.
A taxon presented as Tursiocola sp. from a lea-
therback turtle in Robinson et al. (2016, g. 2–D), with
an internal narrow transapical structure with lateral
triangular wing–shaped expansions, and valvocopulae
showing apices with a double row of puncta, may be
similar to our new taxon.
dIscussIon
Several studies have attempted to nd reliable char-
acters to distinguish Tursiocola from Epiphalaina.
holmes et al. (1993a) suggested that the buttery–like
internal structure could serve to discriminate between
the two latter genera (Table 1). Thereafter, Wetzel et
al. (2012) pointed that the copulae in Tursiocola sys-
tematically have two rows of puncta versus only one
in Epiphalaina. It is now clear that the latter does not
hold and that the ornamentation of the copulae varies
among Tursiocola species (FRankoviCh et al. 2015a,b
and present study, Table 1): For example, Tursiocola
costata FRankoviCh et m.j.sullivan has copulae with
only one row of punctae (Table 1).
The two taxa reported here belong to Tursioco-
la, and species from this genus may be differentiated
ultrastructurally, particularly by the: 1) shape of the
external areola opening, 2) external shape and width
of the stauros, 3) proximal raphe endings shape, 4)
complexity of the cingulum (simple or composed of
158 Fottea, Olomouc, 17(2): 150–163, 2017
DOI: 10.5507/fot.2017.007
Table 1. Morphometrics and characteristic features of Tursiocola and Epiphalaina published species [(+) present, (–) absent, (nd) not specied, ( ) = as observed from the original illustration and/or from recent bibliogra-
phic references].
Heteropo-
larity
Frustule
outline
Lenght
(µm)
Width
(µm)
Striae in 10
µm
and posi-
tion
Areola
shape
Proximal raphe
endings
Valvocopulae Copulae Stauros in
external side
Internal
central
knob(s)
Internal
buttery
structure
Tursiocola yin–yangii sp.
nov.
Present study
difcult to
observe
acicular, acute
apices
8.7–14.5 1.32–
1.37
36–42.8
parallel,
sligtly
radiate on
mid–valve
’S’–shaped round to spathu-
late, coaxial
open, narrow,
1 row of round
puncta, and
short row of
bigger puncta at
foot pole
multiple relatively wide,
bow–tie shaped
1 knob +
Tursiocola guyanensis
sp. nov.
Present study
very slight narrow–ellipti-
cal to acicular
12–13.9 1.7 33–40.6
parallel,
sligtly
radiate on
mid–valve
oblong with
constrictions
round to spathu-
late, coaxial
closed, wide, 1
row of round to
elongate puncta,
and a partial row
of vermiform
puncta at both
apices
multiple relatively wide,
bow–tie shaped
nd + (remains
to be fully
illustrated)
Tursiocola omurai
(t.nemoto) Denys
in Denys1997 (no SEM)
Basionym: Stauroneis omu-
rai nemoto
in nemoto 1956
nd median sub-
constriction
of the valves,
rostrate ends
20–30 4–5 30
parallel
indistinctly
punctate
(round to
rectangular)
nd closed,
2 rows of round
puncta
nd central area very
narrow, linear
fascia
one hump +
Tursiocola staurolineata
Denys in Denys1997
slight linear to very
narrowly
lanceolate,
constricted at
the pseudo-
septa
15–32.9 2.2–3.2 34–36
parallel in
mid–valve,
slightly
radiate on
apices
more or less
round
coaxial, slightly
enlarged
closed girdle bands, normally
2 per frustule, two rows of
aligned round poroids
narrow, straight,
small roundish
central area
2 knobs +
Tursiocola olympica
(Hustedt) R.W.holmes,
naGasaWa et takano in
holmes et al. 1993a
Basionym: Stauroneis
olympica husteDt1952
nd linear lanceo-
late, round
apices
15–35 1.5–4 28–32
(almost
parallel)
round (0.16–
0.22 µm in
diameter)
(slighlty deected) closed girdle bands, double
row of puncta
(fairly broad,
rectangular to
bow–tie shaped)
1 knob +
Riaux–Gobin et al.: Two new Tursiocola species 159
Table 1 Cont.
Tursiocola podocnemicola
C.e.Wetzel, b.van De
vijveR et l.eCtoR
in Wetzel et al. 2012
nd narrow lanceo-
late, acute
apices, slightly
constricted
15–26 1.5–2 30–35
parallel
round, oval
to rectan-
gular
strongly curved
unilaterally
2–3 open bands, 1 row of
large pores and a short row
of smaller pores (or 2 rows,
unclear)
rectangular
stauros
2 knobs +
Tursiocola ziemanii FRan-
koviCh et m.j.sullivan
in FRankoviCh et al. 2015a
narrow lanceo-
late, rostrate
apices
20–61 2.4–5.2 22–25
convergent
in mid–
valve, paral-
lel on apices
oval doubly hooked
unilaterally
only 2, open, 2 rows elongate
pores
diamond–shaped
central area, +
stauros
2 knobs +
Tursiocola costata FRanko-
viCh et m.j.sullivan
in FRankoviCh et al. 2015a
+ lanceolate,
drawn out ros-
trate apices
17–29 2.5–3.9 22–29,
onvergent,
raised virgae
circular to
oval to irre-
gular
strongly deected
on one side
2 copulae, open , 1 row of
circular to oval pores
diamond–shaped
central area,
narrow stauros
2 knobs +
Tursiocola variocopu-
lifera FRankoviCh et
m.j.sullivan
in FRankoviCh et al. 2015a
narrow,
constricted in
the middle in
girdle view
31–57 2.9–4.7 25–28
slightly
convergent
in mid–
valve, paral-
lel on apices
oval,
ne slit–like
elongate
areolae
straight expanded coarsely striated,
open , 2 rows of
linear pores
when pre-
sent, ner
striation,
1 row
of linear
pores
diamond–shaped
central area, nar-
row rectangular
stauros
2 knobs +
Tursiocola denysii Franko-
vich & M.J.Sullivan
in Frankovich et al. 2015b
slight narrowly
lanceolate,
change in
curvature to
juncture of
pseudoseptum
10–20 2–2.9 26–34,
radiate, to
parallel on
apices: 37–
43
elongated straight, asymme-
tric spathulate
closed, 1 row of
ovoid pores, a
second abvalvar
row of similarly
spaced pores
up to 4,
open
wide bow–tie
stauros
1 knob +
Epiphalaina aleutica
(T.Nemoto) R.W.Holmes,
S.Nagasawa & Takano in
Holmes et al. 1993a, see
also Denys 1997
+
lanceolate 15–26
(28–42
in Ne-
moto)
1.75–3 30–32
more or less
parallel,
radiate on
apices
approximati-
vely circular,
0.15 µm in
diameter
(coaxial, not enlar-
ged)
open, 1 row of
round to rectan-
gular perfora-
tions
3 open
bands, 1
row of
puncta
fairly broad,
rectangular to
buttery–shaped
1 knob–
like struc-
ture
Epiphalaina aleutica var.
lineata Denys
in Denys 1997 (no SEM)
nd slightly
constricted
or concave in
mid–valve
<2.5 more slender form (on Dall’s porpoise only)
other structures identical to E. aleutica
Epiphalaina radiata
R.W.Holmes, S.Nagasawa
& Takano
in Holmes et al. 1993b
+ slightly
constricted
or concave in
mid–valve
17–31 2.4–4 26–28,
radiate (5–6
puncta,
except in the
central area)
round to oval (coaxial, not enlar-
ged)
open, 1 row of
elongate pores
3 bands
(possibly
open), 1
row of
elongate
pores
(narrow, bow–tie
shaped)
(possibly
1 knob)
160 Fottea, Olomouc, 17(2): 150–163, 2017
DOI: 10.5507/fot.2017.007
multiple bands), 5) valvocopula and supplementary co-
pula ornamentation (the puncta, sometimes identical in
form and dimensions to the valve areolae, are not per-
forations and are closed by domed internal hymenes),
6) closed or open valvocopulae and copulae.
The valvocopula structure, and the presence of
a short supplementary row of puncta at both poles (or
at a single pole) of the valvocopulae and copulae, may
be particularly good criteria to differentiate species.
Unfortunately, all published taxa have not been exa-
mined with the same degree of EM accuracy, so some
details concerning the number of copulae or their orna-
mentation, is not yet known.
Following FRankoviCh et al. (2015a,b) and their ‘ar-
ticial’ key based on diverse morphological features,
Tursiocola denysii FRankoviCh et m.j.sullivan and T.
variocopulifera FRankoviCh et m.j.sullivan have val-
vocopulae that are different from their abvalvar copu-
lae. T. guyanensis sp. nov. and T. yin–yangii sp. nov.
also belong to this category. Nevertheless, some Tur-
siocola species are described as having only 2 cingular
bands (valvocopulae with no supplementary bands),
that are difcult to be qualied as ‘undifferentiated’.
The following key primerily uses the structure
of the cingulum and its diverse degree of complexity,
to separate all currently known Tursiocola taxa.
more than 4 copulae per valve and valvocopulae different from abvalvar copulae................................................2
only 2 or 3 cingular bands per frustule..................................................................................................................6
valvocopulae closed, with 1 row + short segment of ovoid puncta...........................................................T. denysii
different valvocopula ornamentation....................................................................................................................3
valvocopulae broad, with 1 row of round puncta + large segment of vermiform puncta ..............T. guyanensis
valvocopulae otherwise........................................................................................................................................4
valvocopulae open, 2 complete rows of linear puncta.............................................................T. variocopulifera
different valvocopula ornamentation....................................................................................................................5
1 row of round puncta + short segment of scarce round puncta........................................................T. yin–yangii
2 to 3 bands, open, 1 row + segment of smaller puncta.............................................................T. podocnemicola
cingulum with only 2 bands..................................................................................................................................7
valvocopulae open, 1 row of oval puncta................................................................................................T. costata
different valvocopula ornamentation....................................................................................................................8
2 rows of elongate puncta.....................................................................................................................T. ziemanii
valvocopulae otherwise........................................................................................................................................9
valvocopulae closed, 2 rows of round puncta..............................................................................T. staurolineata
Idem, with broader and more rhombic stauros.................................................................................T. olympica
Idem, with distinct median constriction and somewhat rostrated ends...............................................T. omurai
bRaDy m. (2010): Turtletoms: what diatoms make sea turtles
their homes? – In: julius, m. & eDlunD, m.(eds):
21st International Diatom Symposium, abstracts. – p.
84. St. Cloud State University, St. Cloud, MN.
Denys, l. (1997): Morphology and taxonomy of epizoic dia-
toms (Epiphalaina and Tursiocola) on a sperm whale
(Physeter macrocephalus) stranded on the coast of
Belgium. – Diatom Research 12: 1–18.
Denys, l. & De smet, W.h. (2010): Epipellis oiketis (Ba-
cillariophyta) on Harbour Porpoises from the north
sea channel (Belgium). – Polish Botanical Journal
55: 175–182.
Denys, l. & van bonn, W. (2001): A second species in the
epizoic diatom genus Epipellis: E. heptunei sp. nov. –
In: Jahn, R. et al. (eds): Lange–Bertalot–Festschrift:
Studies on Diatoms. Dedicated to Prof. Dr. Dr. h. c.
Horst Lange–Bertalot on the Occasion of his 65th
Birthday. – pp. 167–176, Gantner Verlag: Ruggell
ISBN 3-904144-26-X.
FRankoviCh, t.a.; sullivan, m.j. & staCy, m.i. (2015a):
Three new species of Tursiocola (Bacillariophyta)
from the skin of the West Indian manatee (Trichechus
manatus). – Phytotaxa 204: 33–48. doi: 10.11646/
acknoWledGMents
Many thanks are due to Yonko GoRanD (C2M, University of Per-
pignan, France) for assistance with the SEM and to Jeanine almany
(USR 3278 CRIOBE, EPHE–CNRS–UPVD) for improvements on
the manuscript. An anonymous reviewer is acknowledged for his
helpful comments and Aloisie Poulíčková and Petr hašleR (Editor
in Chief and Technical editor) for their editorial help. Participation
of AW and GD–K was nanced from Topical subsidy of the Polish
Ministry of Science and Education and DC appreciated the nancial
support of the ANTIDOT project (Pépinière Interdisciplinaire Gu-
yane, Mission pour l’Interdisciplinarité, CNRS), the French Guiana
Regional Council, the EDF Foundation and Fondation de France. We
also acknowledge the Institut Pluridisciplinaire Hubert CuRien UMR
7178–CNRS / Unistra and the CNRS–USR 3278–Labex CORAIL
for supporting this research.
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Riaux–Gobin et al.: Two new Tursiocola species 163
... New diatom taxa were described from previously unexplored hosts and geographical locations and it is expected that this trend will continue. Several novel taxa, including new genera, were described from olive ridleys (Lepidochelys olivacea Eschscholtz), loggerheads (Caretta caretta L), and green turtles (Chelonia mydas L.; Frankovich et al. 2015a, Majewska et al. 2015, 2018a, 2018b, Riaux-Gobin et al. 2017. Moreover, a diatom genus thought to be restricted to cetaceans, Tursiocola Holmes, Nagasawa & Takano (Holmes et al. 1993), was found on various aquatic animals such as manatees and marine and freshwater turtles (Wetzel et al. 2012, Frankovich et al. 2015a,b, 2018, Majewska and Goosen, 2020. ...
... The first discovery of a novel Tursiocola species found on a non-cetacean vertebrate was made by Wetzel et al. (2012) who described T. podocnemicola from the carapaces of freshwater turtles (Podocnemis erythrocephala Spix) inhabiting the Rio Negro in the Brazilian Amazon. Although the authors speculated that the few valves observed in the turtle samples might have been transferred from the freshwater dolphins sharing the habitat with P. erythrocephala, later discoveries of new Tursiocola species growing on manatees (Frankovich et al. 2015b(Frankovich et al. , 2018 and sea turtles (Frankovich et al. 2015a, Riaux-Gobin et al. 2017) demonstrated convincingly that the genus is not exclusively cetacean-associated. ...
... Although slight asymmetry about the apical axis was reported in some of the specimens of T. denysii (Frankovich et al. 2015a), strong dorsiventrality that characterised 100% of the 200+ valves of T. neliana observed in this study should be considered a feature characteristic of the new species. The ranges of the valve length and width recorded for T. neliana are broader than those reported for the remaining sea turtle-associated Tursiocola taxa, although this observation may be biased to some extent by an unequal number of valves measured in each of the studies (Frankovich et al. 2015a, Riaux-Gobin et al. 2017. For example, due to the scarcity of available specimens, some of the taxonomically important characters (including internal structures) in T. guyanensis could not be documented, and the more accurate description of the species awaits further investigations (Riaux-Gobin et al. ...
Article
Full-text available
Tursiocola, a presumably exclusively epizoic diatom genus, comprises species found on various aquatic animals such as cetaceans, manatees, and marine and freshwater turtles. The genus is characterised by linear or lanceolate valves with well-developed pseudosepta at both poles, a valvocopula with three pairs of siliceous tabs, and a butterfly-like structure extending from the central nodule on the internal side of the valve. The current study describes a novel species of Tursiocola, T. neliana Majewska sp. nov. that grows epizoically on leatherback sea turtles from the Eastern Coast of South Africa based on detailed observations using light and scanning electron microscopy. The new taxon resembles the other currently known sea turtle-associated Tursiocola species in possessing relatively small, slightly heteropolar valves with acute apices and a strongly reduced butterfly structure on the internal side. However, T. neliana differs from all other members of the genus in being distinctly dorsiventral, with a clearly bowtie-shaped central area, unequal stria density on two sides of the raphe-ster-num, and up to 8 areolae per stria. The description of the new taxon brings the total number of the sea turtle-associated Tur-siocola species known so far up to four. An emended description of Tursiocola is proposed based on the new observations presented in this and other recent reports. Furthermore, the current understanding of the genus ecology is summarised.
... However, we use 'commensal' conditionally, as no particular study has, to our knowledge, completely tested and described the relationship between these diatoms and their host. These possible sea turtle 'commensals' include Achnanthes elongata and A. squaliformis (Majewska et al., 2017b), Chelonicola costaricensis (Majewska et al., 2015a), C. caribeana (Riaux-Gobin et al., 2017b); Labellicula lecohuiana (Majewska et al., 2017c), Medlinella amphoroidea (Frankovich et al., 2016), Poulinea lepidochelicola (Majewska et al., 2015a), Tripterion societatis (Riaux-Gobin et al., 2017b), Tursiocola denysii (Frankovich et al., 2015a), T. yinyangii and T. guyanensis (Riaux-Gobin et al., 2017a). The presumed biogeography of these diatoms and the extent of their exclusivity to a host species and lifestyle have not been adequately documented; this manuscript is a first attempt. ...
... Society Archipelago; Tables 1 and 2). These samples include the type material for several recently described epizoic diatoms: Tursiocola yin-yangii and Tursioloca guyanensis (Riaux-Gobin et al., 2017b), Tripterion societatis and Chelonicola caribeana (Riaux-Gobin et al., 2017a). Navicula dermochelycola is included here, but formally described elsewhere (Riaux-Gobin et al., 2020). ...
... However, we use 'commensal' conditionally, as no particular study has, to our knowledge, completely tested and described the relationship between these diatoms and their host. These possible sea turtle 'commensals' include Achnanthes elongata and A. squaliformis (Majewska et al., 2017b), Chelonicola costaricensis (Majewska et al., 2015a), C. caribeana (Riaux-Gobin et al., 2017b); Labellicula lecohuiana (Majewska et al., 2017c), Medlinella amphoroidea (Frankovich et al., 2016), Poulinea lepidochelicola (Majewska et al., 2015a), Tripterion societatis (Riaux-Gobin et al., 2017b), Tursiocola denysii (Frankovich et al., 2015a), T. yinyangii and T. guyanensis (Riaux-Gobin et al., 2017a). The presumed biogeography of these diatoms and the extent of their exclusivity to a host species and lifestyle have not been adequately documented; this manuscript is a first attempt. ...
... Society Archipelago; Tables 1 and 2). These samples include the type material for several recently described epizoic diatoms: Tursiocola yin-yangii and Tursioloca guyanensis (Riaux-Gobin et al., 2017b), Tripterion societatis and Chelonicola caribeana (Riaux-Gobin et al., 2017a). Navicula dermochelycola is included here, but formally described elsewhere (Riaux-Gobin et al., 2020). ...
Article
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Sea turtles harbour epizoic diatoms of which several taxa are considered exclusively epizoic and possible 'commensals'. The epizoic diatom communities were examined from 124 individuals representing four turtle species (Chelonia mydas, Eretmochelys imbricata, Lepidochelys olivacea and Dermochelys coriacea), from three well-defined areas: Eastern Caribbean, Equatorial West Atlantic and South Pacific. Overall, the epizoic diatoms are very small and need electron microscopy to be accurately identified. Non-Metric MultiDimensional Scaling analyses permitted us to evaluate these diatom assemblages according to turtle species and biogeography. Differentiation was mainly driven by 14 taxa in the diatom genera Chelonicola, Tripterion, Tursiocola, Olifantiella, Navicula and Achnanthes. The highest diatom species richness was found associated with E. imbricata. Dermochelys coriacea and L. olivacea exhibit lower diatom diversities. Some difference in colonization was detected between C. mydas adults and juveniles at the same site, with higher diatom diversity for the juveniles. Within C. mydas we show geographic differentiation of their diatom assemblages, particularly between populations of the Equatorial West Atlantic and South Pacific. Two Tursiocola species 'commensal' to C. mydas seemed to be geographically restricted to French Guiana and the Caribbean. Dermochelys coriacea has a diatom assemblage very different from those of the three other turtles, probably due to its particular behaviour. Lepidochelys olivacea is also unique in the complete lack of Chelonicola species. Based on our results, the diatoms Tripterion societatis and Chelonicola spp. (as currently defined) appear to be mutually exclusive on turtle hosts. This study adds significantly to our understanding of the global distribution of epizoic diatoms on sea turtles. We discuss to what extent these diatoms can be used as a geographic marker with regard to the biogeography of the diatoms themselves and their host.
... With the recent increased interest in diatom diversity on marine vertebrates [1][2][3][4] in general and sea turtles in particular [5][6][7][8][9][10], a considerable number of sea turtle-associated diatom taxa have been described within the last five years [11][12][13][14][15][16][17][18][19][20][21][22][23][24] and it became clear that diatoms constitute an important element of the sea turtle epi-microbiome on both juvenile and adult individuals. Several sea turtleassociated diatom species have thus far only been reported from this substratum, suggesting a very close, even possibly obligatory relationship between the sea turtle-associated diatoms and their hosts. ...
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In recent years, biofilm-forming diatoms have received increased attention as sea turtle epibionts. However, most of the research has focused on carapace-associated taxa and communities, while less is known about diatoms growing on sea turtle skin. The current study investigated diatom diversity on the skin of loggerhead sea turtle heads detached from the carcasses found along the Adriatic coast between 1995 and 2004 and stored frozen for a prolonged period of time. By using both light and scanning electron microscopy we have found diatom frustules in 7 out of 14 analysed sea turtle samples. Altogether, 113 diatom taxa were recorded, with a minimum of seven and a maximum of 35 taxa per sample. Eight taxa, Achnanthes elongata, Berkeleya cf. fennica, Chelonicola sp., Licmophora hyalina, Nagumoea sp., Navicula sp., Nitzschia cf. lanceolata, and Poulinea lepidochelicola exceeded 5% of relative abundance in any one sample. The presumably obligately epizoic diatom taxa, A. elongata, Chelonicola sp., and P. lepidochelicola, dominated in six loggerhead samples, contributing up to 97.1% of the total diatom abundance. These observations suggest that on the sea turtle skin highly specialised taxa gain even greater ecological advantage and dominance over the co-occurring benthic forms than in the carapace biofilms. The suitability of frozen sea turtle skin specimens for diatom analysis and limitations of this approach are discussed.
... Since the publication of the first report describing sea turtle-associated diatom communities (Majewska et al. 2015c), interest and knowledge in this subject have grown. Several new diatom taxa have been described, and biofilms on different sea turtle species from different geographical regions investigated, using both morphology-based and molecular techniques (Frankovich et al. 2015(Frankovich et al. , 2016Kaleli et al. 2018;Majewska et al. 2015aMajewska et al. , 2017aMajewska et al. , 2017bMajewska et al. , 2017cMajewska et al. , 2018Riaux-Gobin et al. 2017aRivera et al. 2018). Although epizoic diatom biodiversity, ecology, and function are far from being fully understood, and baseline information collection remains a major priority, investigations testing specific hypotheses are required to improve the current balance between speculation and available data. ...
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The current study investigated diatom communities on juvenile green turtles foraging in neritic habitats around five Iranian islands. The primary objectives were to (1) compare species composition, growth form structure, and abundance of diatom communities associated with sea turtles foraging within the restricted boundaries of local feeding pastures, and (2) assess the level of uniqueness of the epizoic diatom flora in comparison with biofilms growing on floating debris. All observations and diatom counts were performed using scanning electron microscopy. The effect of the sampling location was apparent among sea turtle samples and reflected in significantly different cell densities. Diatom abundances were significantly higher on sea turtles (758-1836 cells mm −2) than on floating debris samples (9-189 cells mm −2). Epizoic diatom communities were composed of 20 diatom taxa and dominated by erect forms belonging to the so-called 'marine gomphonemoids', Chelonicola and Poulinea, previously reported on sea turtles from other geographical regions. The diatom flora found on floating debris was composed of 21 taxa. Only four taxa, Amphora cf. bigibba, Cocconeis cf. neothumensis var. marina, Psammodictyon constrictum, and Tabularia affinis, were recorded from both sea turtles and floating debris samples, and none of these exceeded 4% of the average relative abundance on the sea turtle carapaces. The study reveals a clear substratum preference in sea turtle-associated diatoms, with no evidence for species turnover across the investigated region over different sampling seasons, thus confirming previous speculations that sea turtle diatom communities would show a high level of uniqueness and stability.
... Specimens were analyzed with JEOL JSM-7001F (JEOL, Tokyo, Japan) scanning electron microscopes at 5 kV. The morphology of the epizoic diatoms found was compared with images and information available in the relevant literature (e.g., Holmes et al. 1989, 1993, Wetzel et al. 2012, Frankovich et al. 2015a,b, 2018, Riaux-Gobin et al. 2017. ...
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With the advent of more comprehensive research into the microbiome and interactions between animals and their microbiota, new solutions can be applied to address conservation challenges such as husbandry and medical care of captive animals. Although studies on epizoic algae are relatively rare and function and role of those mainly photosynthetic organisms in the animal microbiome is not well understood, recent surveys on epizoic diatoms show that some of them exhibit traits of obligate epibionts. This study explores diatom communities on captive-born manatees from the Africarium in Wroclaw, Poland. The light and scanning electron microscopy analyses revealed that skin of all animals sampled was dominated by apochlorotic Tursiocola cf. ziemanii, an epizoic species described recently from Florida manatees, that reached 99,9% of the total diatom abundance. Despite using media with a wide range of salinity (0-34PSU), the isolated Tursiocola cells did not grow, whereas the normally pigmented Planothidium sp., that was only occasionally found on the animal substratum, survived in all culture media tested. Our observations provide direct evidence that manatee-associated Tursiocola endure the dramatic salinity changes that occur regularly during their host life cycle, and can thrive in an artificial captive setting, if the manatee substratum is available. The impact of the practices and routines used by the Africarium on the manatee-associated diatoms is briefly discussed.
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Background: Our understanding of the importance of microbiomes on large aquatic animals—such as whales, sea turtles and manatees—has advanced considerably in recent years. Recent activity describing the epizoic diatoms growing on marine vertebrates suggests that these epibiotic diatom communities constitute diverse, polyphyletic, and compositionally stable assemblages that include both putatively obligate epizoic and generalist species. Here, we outline a successful attempt to culture putatively obligate epizoic diatoms without their hosts and propose further applications and research avenues in this growing area of study. Results: We cultured cells of epizoic diatoms from multiple host species sampled in the wild and captivity. Analyzing the DNA sequences of these cultures, we found that several unique diatom taxa have independently evolved to occupy in epibiotic habitats. We created a library of reference sequence data for use in metabarcoding surveys of sea turtle and manatee microbiomes that will further facilitate the use of environmental DNA for studying host specificity in epizoic diatoms and the utility of diatoms as indicators of host ecology and health. Conclusions: Our discovery that epizoic diatoms can be cultured independently from their hosts raises several questions about the nature of the interaction between these diatom species and their hosts. We encourage the interdisciplinary community working with marine megafauna to consider including diatom sampling and diatom analysis into their routine practices.
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Marine epizoic diatom, Protoraphis atlantica is reported for the first time in coastal waters off Kasargod and open ocean waters off Kannur along the southeastern Arabian Sea. Diatoms infested exclusively the urosome of calanoid copepods Labidocera sp. and Candacia catula. The taxonomic description, ecological habit, and distribution of Protoraphis are described in the present paper along with microscopical analyses. With the present report from the southeastern Arabian Sea, the geographical distribution of Protoraphis can be extended to Indian waters.
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Although diatoms colonize a vast diversity of immersed hard-surfaced objects and organisms, many diatom species, and sometimes entire genera, show a clear preference towards a particular type of substratum. Studies of animal-associated diatoms indicate that some epizoic forms may require this specific habitat to thrive, and new diatom taxa are expected to be found on as yet unexplored animal hosts. The current study is the first to investigate the diatom flora of sea snakes. Three museum specimens of yellow-bellied sea snakes (Hydrophis platurus) collected over a period of 23 years from the southeastern coast of South Africa were examined for their diatom flora. Diatoms were abundant on the sea snakes, but communities were composed of only a few species. A previously undescribed species of Nagumoea contributed over 99% of the total diatom assemblage on both the sea snake skin and sea-snake-associated barnacles (Octolasmis sp.). This diatom dominant is described here as Nagumoea hydrophicola sp. nov., based on detailed observations of its frustule ultrastructure using light and scanning electron microscopy. The species is most similar to N. serrata, sharing a similar valvocopula morphology with two rows of pores. However, it can be distinguished from all currently known congeners by its lanceolate central area, short distal raphe endings not reaching the valve mantle, and doubly perforated abvalvar girdle bands. Environmental preferences of the new species are discussed in the context of its host's biology.
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Background The Aegean Sea coast of Turkey hosts one of the most important nesting grounds for loggerhead sea turtles ( Caretta caretta ) in the Mediterranean Sea. Previous studies have revealed that the sea turtle carapace provides favourable conditions for various epibiontic organisms. Epibionts occurring on the carapace have been examined from different locations in the oceans. Methods This is the first time such a high number (39) of samples collected from nesting turtles during such a long time period (extending from 2011 to 2018) has been used for the study of the diatom component of the microbiome on the turtle carapaces. A total of 33 samples were investigated in terms of light microscopy (LM) and scanning electron microscopy (SEM). Six unprocessed biofilm fragments were subject to SEM observations. Results A total of 457 epizoic diatom taxa belonging to 86 genera were identified. Epizoic forms, e.g., Achnanthes spp., Chelonicola spp. or Tripterion spp. (also identified by SEM observations of the undisturbed pieces of the microbiome) dominated in terms of relative abundance, but the highest numbers of taxa were ubiquitously represented by Navicula (79), Nitzschia (45), Amphora (40), Cocconeis (32), Diploneis (25) and Mastogloia (23). Navicula perminuta and Delphineis australis were the most frequent taxa, present in 65% of the samples, both with an average relative abundance of 10%. The results of our study revealed that diatoms are an essential component of the loggerhead sea turtles’ microbiome, in terms of high biodiversity and abundance. Although strict epibionts provide a signature of the turtle microbiome, the carapace as a solid substrate attracts numerous benthic diatom species which are considered opportunistic forms and can be found in the surrounding benthic habitats of the vast ocean littoral space.
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With regard to vertebrates, obligately epizoic diatoms (Bacillariophyta) were first described from cetaceans, but the turtles, both freshwater and marine, also host very specific floras. Several scrapings of juveniles of Chelonia mydas have allowed the description of two new taxa with asymmetry to the transapical axis: Tripterion societatis sp. nov. and Chelonicola caribeana sp. nov. These taxa are very small, and possess some morphological plasticity. Such plasticity might suggest inclusion in genera of taxa with characteristics slightly different from the original diagnosis of these genera. Based on our observations, an emended diagnosis is proposed for the genus Chelonicola.
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With regard to vertebrates, obligately epizoic diatoms (Bacillariophyta) were first described from cetaceans, but the turtles, both freshwater and marine, also host very specific floras. Several scrapings of juveniles of Chelonia mydas have allowed the description of two new taxa with asymmetry to the transapical axis: Tripterion societatis sp. nov. and Chelonicola caribeana sp. nov. These taxa are very small, and possess some morphological plasticity. Such plasticity might suggest inclusion in genera of taxa with characteristics slightly different from the original diagnosis of these genera. Based on our observations, an emended diagnosis is proposed for the genus Chelonicola
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Medlinella amphoroidea gen. et sp. nov. is described from the dorsal neck skin of loggerhead sea turtles (Caretta caretta). The presence of girdle septa, multiple copulae, and the marine epizoic habitat of Medlinella amphoroidea are characteristic features shared with many species in the similar Tripterion, Chelonicola, and Poulinea genera. The semi-lanceolate valve shape, the asymmetric valve face with distinct dorsal and ventral striae, and the volate pore occlusions distinguish Medlinella from these genera. Medlinella amphoroidea accounted for up to 50% of all diatom valves on the skin of examined loggerhead turtles. Examination of the type slides of Tripterion kalamensis and T. philoderma for comparative purposes revealed morphological features that were either insufficiently or incorrectly described in the original publications. Our observations confirm that T. philoderma lacks septa and therefore does not conform to the genus description of Tripterion. The description of cingulum structure in Tripterion kalamensis is amended to identify multiple porose copulae that are open at one end. While the description of Medlinella creates another monotypic genus within a group of similar marine epizoic genera, we feel the novel character state (volate occlusions) present in this taxon is significant. Clearly, however, further phylogenetic analysis of morphological, or the development of molecular characters in the group of similar genera is required.
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The macro-epibiotic communities of sea turtles have been subject to growing interest in recent years, yet their micro-epibiotic counterparts are almost entirely unknown. Here, we provide the first evidence that diatoms are epibionts for all seven extant species of sea turtle. Using Scanning Electron Microscopy, we inspected superficial carapace or skin samples from a single representative of each turtle species. We distinguished 18 diatom taxa from these seven individuals, with each sea turtle species hosting at least two diatom taxa. We recommend that future research is undertaken to confirm whether diatom communities vary between sea turtle species and whether these diatom taxa are facultative or obligate commensals.
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Mastogloia is one of the few species-rich diatom genera the majority of whose taxa inhabit the marine environment with only a small number of taxa in freshwater habitats. An ongoing revision of the Macedonian diatom flora, mainly over the last decade, has revealed many previously misidentified taxa. Currently, seven freshwater Mastogloia taxa have been recorded from Macedonia: M. elliptica (C. Agardh) Cleve, M. dansei (Thwaites) W. Smith, M. grevillei W. Smith, M. lacustris (Grunow) Grunow, M. ohridana Cvetkoska & Levkov, M. albertii nom. nov. and M. sterijovskii sp. nov. The main morphological features have been analysed with light and scanning electron microscopy. These taxa inhabit a variety of freshwater habitats, including oligotrophic rivers, eutrophic ponds, mine lakes, thermo-mineral springs, with one species from fossil sediments of ancient Lake Ohrid. Mastogloia albertii nom. nov., which we also lectotypify, is a new name for M. smithii var. amphicephala Grunow, since the latter is clearly distinct from the lectotype of M. smithii Thwaites. In addition, one of the observed taxa does not fit within any previously described Mastogloia taxa and is hereby described as a new species, M. sterijovskii. Mastogloia sterijovskii was found as epizoic on the dorsal carapace of the European pond turtle, Emys orbicularis Linnaeus, from the Mladost reservoir near Veles, central Macedonia. This species resembles M. albertii in valve outline, but can be distinguished by the shape of the valve apices and its size.
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Tursiocola denysii sp. nov. is described from the dorsal neck skin of loggerhead sea turtles (Caretta caretta), bringing the total number of known species in the genus Tursiocola to eight. A gradient of striae density on the valve face, the low length: width ratio of the valves, radiate striae at mid-valve, and a second partial row of pores on the valvocopulae are characteristics that expand the range of morphological diversity within the genus. The different morphology of the pars interior and the pars exterior of the valvocopula is described for the first time in the genus. T. denysii accounted for up to ca. 40% of all diatom valves on the skin of loggerhead turtles. This is the first report of a new epizoic diatom species from the skin of loggerhead sea turtles.
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Marine mammals such as whales and dolphins have been known for a long time to host a very specific epizoic community on their skin. Less known however is the presence of a similar community on the carapaces of sea turtles. The present study is the first describing new taxa inhabiting sea turtle carapaces. Samples, collected from nesting olive ridley sea turtles (Lepidochelys olivacea) on Ostional Beach (Costa Rica), were studied using light and scanning electron microscopy. Two unknown small-celled gomphonemoid taxa were analysed in more detail and are described as two new genera, closely related to other gomphonemoid genera with septate girdle bands, such as Tripterion, Cuneolus and Gomphoseptatum. Chelonicola Majewska, De Stefano & Van de Vijver gen. nov. has a flat valve face, uniseriate striae composed of more than three areolae, simple external raphe endings, internally a siliceous flap over the proximal raphe endings and lives on mucilaginous stalks. Poulinea Majewska, De Stefano & Van de Vijver gen. nov. has at least one concave valve, uniseriate striae composed of only two elongated areolae, external distal raphe endings covered by thickened siliceous flaps and lives attached to the substrate by a mucilaginous pad. Chelonicola costaricensis Majewska, De Stefano & Van de Vijver sp. nov. and Poulinea lepidochelicola Majewska, De Stefano & Van de Vijver sp. nov. can be separated based on stria structure, girdle structure composed of more than 10 copulae, raphe structure and general valve outline. A cladistics analysis of putative members of the Rhoicospheniaceae indicates that the family is polyphyletic. Chelonicola and Poulinea are sister taxa, and form a monophyletic group with Cuneolus and Tripterion, but are not closely related to Rhoicosphenia, or other genera previously assigned to this family. Features used to help diagnose the family such as symmetry and presence of septa and pseudosepta are homoplastic across the raphid diatom tree of life.
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Three new species of Tursiocola are described from the skin of the West Indian manatee bringing the total number of known species in the genus to seven. The range of morphological diversity within the genus is greatly expanded. The number of poroid rows on the copulae is no longer a valid characteristic for the separation of Tursiocola from the ceticolous genus Epiphalaina. The presence of a butterfly-like structure in the central area of the former is at present the best criterion for separating the 2 genera. The 3 new Tursiocola species accounted for nearly 90% of all diatom valves on the manatee skin. No other diatom taxa previously described as new from the skin of cetaceans were present on the manatee.