New records on the rich loriciferan fauna of Trezen ar Skoden (Roscoff, France): Description of two new species of Nanaloricus and the new genus Scutiloricus
Author
Neves, Ricardo Cardoso
Author
Kristensen, Reinhardt Møbjerg
Natural History Museum of Denmark, University of Copenhagen, Copenhagen Ø, Denmark
Author
Møbjerg, Nadja
Department of Biology, August Krogh Building, University of Copenhagen, Copenhagen Ø, Denmark,
text
PLoS ONE
2021
e 0250403
2021-05-05
16
5
1
42
journal article
301517
10.1371/journal.pone.0250403
b83f9ed2-1a72-4f1e-b9b0-10d6940f37fa
1932-6203
PMC8099068
33951070
13151726
Nanaloricus valdemari
sp. nov.
(
Figs 1–7
).
urn:lsid:zoobank.org:act:
A0E2CDB1-6F62-4F86-82DF-43F2A06ED519
Synonymy.
Nanaloricus
sp.
sensu
[
26
];
Nanaloricus
n. sp.
sensu
[
27
].
Material examined.
Holotype
(
Fig 1
). Adult male collected on
7 February 2013
at the type locality at ca.
45 m
water depth, mounted in glycerin on a glass slide, and deposited at the
Natural History Museum
of
Denmark
under accession number NHMD-678720.
Allotypic
paratype
(
Fig 4
). Adult female collected on
15 May 2013
at the type locality at ca.
50 m
water depth, mounted in glycerol on a glass slide, and deposited at the
Natural History Museum
of
Denmark
under accession number NHMD-678736
.
Paratypes
.
27 adults
(
5 males
,
21 females
, 1 of unkown gender) and 6 tentatively assigned postlarvae collected at the type locality between
12 July 1985
and
15 May 2013
at 43–55 m water depths.
The
33 paratypic specimens are mounted in glycerin,
Vectashield
or Fluoromount-G on glass slides, and deposited at the
Natural History Museum
of Denmark under the access numbers NHMD-677708 to NHMD-677713, NHMD-677716 to NHMD-677719, NHMD-677721 to NHMD-677734 and NHMD-677737 to NHMD-677744.
The
specimen registered with access number NHMD-677725 is shown in
Fig 5
.
In
addition
,
three adult
males collected at the type locality on
12 July 1985
at ca.
55 m
water depth, and mounted on
SEM
stubs (NHMD-866002 to NHMD-866004) were analyzed for comparative purposes (
Fig 7
)
.
Additional reference material
(
Fig 6
). In addition to the fixed material examined, 11
non-type specimens
(one tentatively assigned postlarva,
four males
and
six females
), collected at the
type
locality in
April 2019
and
August 2020
, were observed and photographed alive.
Habitat and distribution
. Marine sediments composed of clean shell gravel at
type
locality.
Type locality
. Trezen ar Skoden, Roscoff,
France
, (48˚45’55”N, 04˚06’45”E).
Etymology
. The species is named after Valdemar MØbjerg Boslev Kristensen, who is grandson and nephew to the middle author and last author, respectively.
Fig 1. Light micrographs of the holotypic adult male of
Nanaloricus valdemari
sp. nov.
Anterior faces up in all aspects. (A) Ventral view of the extended specimen. Note that the mouth tube is not fully extended. (B) Dorsal view of the specimen. Note the pair of longitudinal stripes (ls) spanning the anterior two thirds of the dorsal plate of the lorica. (C) Anterior region of the specimen, dorsal view. (D) Close-up of the posterior region of the introvert and neck, ventral view. White arrowhead points to the small, midventral anterior spike. Arrows point to trichoscalid sensory organs. Abbreviations: af, anal field;
bpa/b
, basal plate of type a or b; cs, clavoscalid; dp, dorsal plate; fu, oral furca; in, introvert; lo, lorica; mc, mouth cone; mt, mouth tube; sp (and black arrowheads), anterior spike; sr, spinoscalid of 8
th
or 9
th
row; ss, spinoscalid; tp, trichoscalid plate; tr, trichoscalid; vlp, ventrolateral plate; vp,
8/9
ventral plate.
https://doi.org/10.1371/journal.pone.0250403.g001
Fig 2. Line art drawing of the adult male habitus of
Nanaloricus valdemari
sp. nov.
Ventral view of the body, anterior faces up. Note that only a selected number of scalids from rows 1 to 8 are represented for clarity. Abbreviations: af, anal field;
bpa/b
, basal plates of type a and b; bu, buccal tube; cs, clavoscalid; dlp, dorsolateral plate; fu, oral furca; gl?, putative gland outlet; in, introvert; lo, lorica; mc, mouth cone; mo, mouth aperture; mt, mouth tube; mvs, midventral anterior spike; ne, neck; or
1/2
, oral ridges of type 1 and 2; sr
2–9
, spinoscalids of 2
nd
to 9
th
row (including sr, i.e. type a and b spinoscalids of the 4
th
row); sp (and black arrowheads), anterior spike; to, trichoscalid
4a/b
sensory organ; tp, trichoscalid plate; tr
1
, single trichoscalid; tr
2
, double trichoscalid; vlp, ventrolateral plate; vp, ventral plate. https://doi.org/10.1371/journal.pone.0250403.g002
Fig 3. Line art drawing of the adult male partial habitus of
Nanaloricus valdemari
sp. nov.
Dorsal view of the lorica, anterior faces up. Abbreviations: ac, anal cone; dlp, dorsolateral plate; dp, dorsal plate; fl, flosculum; go?, putative gonopore; ls, longitudinal stripe; sp (and arrowhead), anterior spike.
https://doi.org/10.1371/journal.pone.0250403.g003
The following description will solely focus on adult specimens, as postlarvae have only been tentatively assigned to species (see section below:
"Notes on the postlarvae found at Trezen ar Skoden"
).
Diagnosis.
Adults
. (1) mouth cone with 8 oral ridges of different length and characterized by posterior sclerotized oral furcae, a telescopic mouth tube, and a well-defined honeycomb sculpture; (2) introvert with 9 rows of scalids; (3) first row with eight clavoscalids that differ between males (multiform, broad or slender, all branched except for the midventral pair) and females (four-segmented, slender, unbranched); (4) second row with 9 four-segmented, leg-like spinoscalids; (5) third row with 7 two-segmented, feather-like scalids; (6) fourth row with 16 spinoscalids of
two types
: 8 two-segmented, leg-like scalids (
type
A) alternate with 8 two-segmented spinoscalids with feather-like distal segment (
type
B); (7) fifth to seventh rows all similar, each row with 30 leg-like, three-segmented scalids; (8) eighth row with 30 very long unsegmented spinoscalids with a small bulbous base; (9) ninth row with 30 small, teeth-like scalids characterized by three cuspid-like protrusions; (10) neck with 8 single trichoscalids alternating with 7 double trichoscalids, with both the single and each of the double trichoscalids protruding from a single, trapezoid trichoscalid plate; (11) trichoscalid plates of the upper appendages of ventrally situated trichoscalids characterized by a short sensory organ with serrated margins and a small, anteroproximal pore; (12) lorica composed of six cuticular plates,
Fig 4. Light micrographs of the allotypic adult female of
Nanaloricus valdemari
sp. nov.
Anterior faces up in all aspects. (A) Overview of the specimen, dorsal view. Note that the mouth tube is not fully extended. Note also the pair of longitudinal stripes (ls) spanning the anterior two thirds of the dorsal plate of the lorica. (B) Close-up of the anterior region of the specimen, dorsal view. Arrow points to the two most distal segments of a clavoscalid.(C) Close-up of the introvert, neck and anterior region of the abdomen, dorsal view. (D) Posterior region, ventral view. Double-headed arrows point to large pores (gland outlets?) situated on the posterior region of the ventral plate. (E) Posterior region, dorsal view. Note the putative gonopores (go?) located on the
posteriormost region of the dorsolateral plates. Abbreviations: af, anal field; bu, buccal tube; cc, cuticularized crest; cs, clavoscalid; dlp, dorsolateral plate; dp, dorsal plate; lo, lorica; mc, mouth cone; or, oral ridge; sp (and black arrowheads), anterior spike; ss, spinoscalid; tr, trichoscalid; vp, ventral plate.
https://doi.org/10.1371/journal.pone.0250403.g004
with honeycomb sculpturing and bearing 14 large anterior spikes and a small midventral spike; (13) dorsal plate characterized by two narrow, longitudinal stripes spanning laterally along its anterior two thirds; (14) 9 flosculi (4 laterodorsal pairs and 1 dorsal) present posteriorly on the dorsal side of the lorica (dorsolateral and dorsal plates); (15) posterior region of the lorica characterized by a small anal cone, a pair of putative gonopores located postero-dorsally and a pair of ventrally located pores (gland outlets?).
Description.
Body (
Figs 1–7
)
. Divided into head (mouth cone and introvert), neck, thorax, and abdomen. The holotypic adult male (
Fig 1
) is 235 μm long, including the mouth cone, and 74 μm wide.
Mouth cone (mc
,
Figs 1
,
2
,
4
,
5
and
7
)
. Long (ca. 60 μm in length), and with three distinct sections. The proximal section is broad, short and with eight conspicuous, sclerotized oral
Fig 5. Light micrographs of a paratypic adult female of
Nanaloricus valdemari
sp. nov.
Anterior faces up in both aspects, dorsal view. (A) Overview of the specimen with extended introvert and fully extended mouth tube. (B) Close-up of the anterior region of the body. Abbreviations: bu, buccal tube; cs, clavoscalids; in, introvert; lo, lorica; ls, longitudinal stripe; mc, mouth cone; mt, mouth tube; or, oral ridge; sp, anterior spike; ss spinoscalid; tr, trichoscalid.
https://doi.org/10.1371/journal.pone.0250403.g005
Fig 6. Light micrographs of three live specimens of
Nanaloricus valdemari
sp. nov.
Anterior faces up in all aspects. (A) Overview of a female adult with head almost fully retracted. Internally, note the presence of the large ovaries (ov) in the abdomen. (B) Overview of a female adult (different from that shown in A). Note the pair of longitudinal stripes (ls) spanning the anterior two thirds of the dorsal plate of the lorica. (C and D) Overview of a male adult with head almost fully retracted. Note the presence, within the abdomen, of a testis (te) containing spermatozoa (sz). Note also the relative position of the pharyngeal bulb (pb) in this retracted animal. Abbreviations: af, anal field; bu, buccal tube; cs, clavoscalid; dp, dorsal plate; lo, lorica; sp, anterior spike; ss spinoscalid; tr, trichoscalid.
https://doi.org/10.1371/journal.pone.0250403.g006
Fig 7. Scanning electron micrographs of three paratypic adult males of
Nanaloricus valdemari
sp. nov.
(A) Overview of extended specimen, ventral view, anterior faces up. Same specimen as in C and D. Note the multiform clavoscalids: the ventralmost pair is unbranched (and similar to the eight female clavoscalids), while the others are divided into three branches. (B) Close up of the mouth tube (mt). Same specimen as in E. Note the honeycomb sculpture (hs) of the cuticle. (C) Anterior region of the body, ventral view. Note the difference between single (tr
1
) and double trichoscalids (tr
2
). White arrowhead points to the small midventral anterior spike. White
arrows point to lorical pores. (D) Close up of the midventral pair of single trichoscalids, each of which protrudes from a plate characterized by a large pore (white double-headed arrow). The inset shows a magnification of the double trichoscalid sensory organ (to), which possesses a small pore (black arrows). (E) Close up of spinoscalids of 9
th
row (sr
9
) and basal plates, one of each
type
(
bpa
and
bpb
). Note the long hairs (ha) scattered along the length of the distal segments of a spinoscalid of 7
th
(?) row. (F) Detail of a cluster of flosculi arranged in a rectangular pattern on the dorsolateral plate. Same specimen as in G. (G) Overview of the posterodorsal region of the lorica. Note the pair of longitudinal stripes (ls) that span the anterior two thirds of the dorsal plate (dp). Black double arrowheads indicate the clusters of flosculi situated on the dorsolateral plates (dlp), while the white double arrowheads point to the small flosculum situated on the dorsal plate. Abbreviations: ac, anal cone; cs, clavoscalid; dlp, dorsolateral plate; fu, oral furca; lo, lorica; mc, mouth cone; or, oral ridge; ss, spinoscalid; sp, anterior spike; tp, trichoscalid plate; tr, trichoscalid; vlp, ventrolateral plate; vp, ventral plate.
https://doi.org/10.1371/journal.pone.0250403.g007
furcae (fu) arranged radially (
Figs 2
and
7C
). These eight furcae are of identical structure and they each extend into an oral ridge (
Fig 7A–7C
). The middle section is long, conical and characterised by the eight oral ridges of different lengths (
Fig 2
). Four primary oral ridges (or
1
) are long and span the whole middle section, while four secondary oral ridges (or
2
) are short and span only the posterior three quarters of the middle section (
Figs 2
,
4
and
7A and 7B
). Both the proximal and middle sections are characterized by a well-defined honeycomb sculpture of the cuticle (
Figs 2
and
7B
). The distal section consists of a seemingly short mouth tube (mt), which is slightly bulbous posteriorly and ends with a terminal mouth aperture. However, the mouth tube is telescopic and can extend outside of the mouth cone, significantly increasing its total length (
Fig 5
). There are no oral stylets.
Introvert (in
,
Figs 1
,
2
,
4
,
5
and
7
)
. Round in shape and characterized by nine rows of scalids arranged radially (
Figs 1
,
2
,
4
and
5–8
).
First row (sr1,
Fig 8
) with eight clavoscalids (cs) that differ between males and females. In females (
Figs 4
and
5
), the clavoscalids are divided into four segments. The first, most proximal segment is relatively short and consists of a conical base that protrudes from the introvert and extends distally into a curved, cylindrical shape with many small papillae arranged anteriorly. The second segment, which is the longest segment of the clavoscalid, is club-shaped and slightly serrated anteriorly. The third segment is very short and thin (
Figs 2
and
4B
). The fourth segment is also very short and ends as a spinose tip (
Figs 2
and
4B
). In males (
Figs 1–3
and
7
) the clavoscalids are multiform. The most ventral pair is exactly as those of the female. The other six clavoscalids possess a robust base and are divided into primary, secondary and tertiary branches. Both the secondary and tertiary branches are broad and flat. However, the former has a thin base and is slightly broader than the latter. The primary branch is three-segmented and very similar to the three most distal segments of the ventral pair of clavoscalids. Indeed, the primary branch possesses distally two short, slightly curved segments: a thin one followed by a terminal spine-like segment.
The second row (sr
2
,
Fig 8
) consists of nine leg-like spinoscalids (ss) divided into four segments (
Fig 2
). The first, most proximal segment has a semiround base with a row of papillae arranged laterally on the most proximal region. The base narrows distally to form a cylindrical, short region. The second segment is short and cylindrical with many small papillae. The third segment is slightly thinner and long, representing approximately one half of the spinoscalid. The most distal segment, which represents one quarter of the spinoscalid, is slightly curved and terminates as a spinose tip. Noteworthy, the two midventral and the two ventrolateral spinoscalids of the second row are thinner than all other spinoscalids of the same row. Their bases are characterized by 1–3 small spikes.
The third row (sr
3
,
Fig 8
) is composed of seven short, two-segmented feather-like spinoscalids (
Fig 2
). The proximal segment is a small, conical base with several large papillae (up to eight?) arranged anteriorly. The distal segment is relatively long and possesses numerous short, curved hairs.
Fig 8. Schematic diagrams of the distribution of introvert and neck appendages in adult forms of
Nanaloricus valdemari
sp. nov.
and
Nanaloricus mathildeae
sp. nov.
Note that for sake of clarity clavoscalid sexual dimorphism is not depicted.
Note also that the shaded area indicates the neck region. (A) Polar diagram. (B) Planar projection. Abbreviations:
bpa/b
, basal plates of type a or b; cs, clavoscalid; MD, middorsal line; MV, midventral line; sr, scalids of 1
st
to 9
th
row; ss, spinoscalid; tp,
1–9
trichoscalid plate; tr
1
, single trichoscalid; tr
2
, double trichoscalid.
https://doi.org/10.1371/journal.pone.0250403.g008
The fourth row (sr
4
,
Fig 8
) consists of 16 spinoscalids of
two types
:
8 type
A leg-like spinoscalids (sr
4a
) alternating with
8 type
B feather-like spinoscalids (sr
4b
) with numerous short, curved hairs (
Fig 2
). The
type
A spinoscalids are divided into three segments. The first, most proximal segment has a short, round base with several small papillae distributed in a scattered manner. The base narrows distally into a cylindrical, short region. The second segment is thin, serrated posteriorly and rather long, representing half of the total length of the spinoscalid. The third, most distal segment terminates as a thin tip. The
type
B spinoscalids are two-segmented, each composed of a proximal and a distal segment of similar length. The proximal segment has a round base with several densely distributed papillae. This segment narrows distally to form a cylindrical region with serrated margins. The distal segment has numerous short hairs and, hence, appears feather-like. It terminates in a hook-shaped tip with two short hairs. The fifth to seventh rows (sr
5-7
,
Fig 8
) are each composed of 30 three-segmented, leg-like spinoscalids (
Fig 2
). The most proximal segment has a short, narrow base. The middle segment is thin and very long, representing more than half of the total length of the scalid. The most distal segment is relatively long, thin and terminates as a spine-like tip. The two most distal segments have finely serrated margins and several long hairs (ha,
Fig 7E
) scattered along their length. The hairs are only seen by
SEM
.
The eighth row (sr
8
,
Fig 8
) consists of 30 unsegmented whipe-like spinoscalids with a small bulbous base with a few papillae (
Fig 2
). These spinoscalids have finely serrated margins and several long hairs scattered along their length (only seen by SEM), and they terminate as a thin tip.
The ninth row (sr
9
,
Fig 8
) consists of 30 small, teeth-like scalids (well discernible by SEM,
Figs 2
and
7E
). Each of these scalids possesses an oval anterior edge and three cuspid-like projections that protrude laterally and extend backwards from the posterior edge.
Neck (ne
,
Figs 2
and
8
)
. Composed of at least four rows of neck flat plates, which are divided into columns by several longitudinal folds (
Fig 2
). A row of 15 small basal plates is present in the most anterior region of the neck, immediately under the ninth row of spinoscalids (
Figs 1D
and
7E
). This row consists of seven triangular plates (
bpa
) alternating with eight oval plates (
bpb
), each with two rows of teeth arranged transversely. The two midventral basal plates are of the latter
type
(i.e.,
bpb
). Each basal plate is arranged in the center of the neck flat plates. The posterior region of the neck is characterized by 15 trichoscalids (tr) arranged radially: eight single (tr
1
) alternating with seven double trichoscalids (tr
2
;
Figs 1
,
2
and
7
). The trichoscalids are all flat, with a central ridge, and possess serrated margins with hairs and a blunt tip. The double trichoscalids are composed of two separate appendages, an upper appendage and a lower appendage. The upper appendage is longer (ventrolateral pairs) or slightly longer (lateral pairs) than the lower appendage, which has approximately the same length as a single trichoscalid. Both the single and each of the double trichoscalids protrude from a single trichoscalid plate (tp) with a trapezoid shape; the basal plates of the midventral pair are slightly smaller (
Figs 2
and
7D
). Moreover, each ventrolateral single trichoscalid is further characterized by having two sclerotized plates located anteriorly to their trichoscalid plate. Notably, the basal plates of the upper appendages of the double trichoscalids are characterized by a short sensory organ with serrated (toothed) margins and an anteroproximally situated pore, which is only seen by SEM (to;
Figs 1D
,
2
and
7D
). The trichoscalid sensory organ is situated at the most anterior margin of the upper appendage basal plate. The sensory organs of the ventral double trichoscalid plates are slightly shorter than the ventrolateral ones. The putative sensory organs of the dorsal side could not be observed neither by light nor scanning electron microscopy; their presence/absence remains thus to be determined. In addition, the plate of each midventral single trichoscalid has a large, medially situated pore that is approximately twice the size as the pore on the trichoscalid sensory organs.
Summing up, the number of introvert and neck appendages (cs = clavoscalids,
ss = spinoscalids, tp = trichoscalid plates, tr = trichoscalids) is given in the following formula (
Fig 8
):
Introvert: 8 cs; 9 sr
2
; 7 sr
3
;
8
þ
8 sr
4
; 30 sr
5
; 30 sr
6
; 30 sr
7
; 30 sr
8
; 30 sr
9
;
Neck: 7a
þ
8b bp;
8
þ
14 tp; 8 tr
1
ð
single
Þ þ
7 tr
2
ð
double
Þ:
Thorax
. Short, enclosed in its own cuticle, surrounded externally by the lorica, and without any appendages or segments.
Abdomen
. Enclosed in a lorica (lo;
Figs 1–7
) composed of six cuticularized plates with honeycomb sculpture: one ventral, two ventrolateral, two dorsolateral and one dorsal. Each plate possesses two robust anterior spikes (sp) except for the dorsal plate, which bears four anterior spikes. In total, the anterior edge of the lorica thus has 14 large spikes of equal length, except for one larger spike on each of the dorsolateral plates. In addition, a small midventral spike is present, located between the two large anterior spikes of the ventral plate (
Figs 1D
,
2
,
7C and 7D
). The total number of anterior spikes is thus 15.
Notably, the dorsal plate is characterized by two narrow, longitudinal stripes (ls) spanning laterally along its anterior two thirds (
Figs 1B
and
3–7G
). These longitudinal stripes appear as surface ridges and their presence gives the impression that the dorsal plate is partially subdivided into three subplates.
A cluster of four flosculi (fl), arranged in a rectangular pattern, is present on each of the dorsolateral plates (dlp). These flosculi are characterized by 5–6 microvilli-like structures covered with cuticle (
Fig 7F and 7G
). Additionally, a single smaller flosculum, with only 2–3 microvilli-like structures, is found on the dorsal plate.
The postero-dorsal region of the lorica consists of an anal field (af,
Figs 1A
,
2
,
4A
and
6A
). More specifically, this anus-gonopore region is characterized, both in males and females, by a small anal cone (
Figs 3
and
7G
) and a pair of putative gonopores situated posteriorly on the dorsolateral plates (go?;
Figs 3
and
4E
). Each of the latter plates is furthermore characterized by a cuticularized crest (cc) that spans internally between the putative gonopores and the posterior end of the lorica (
Fig 4A
). On the ventral side, a large pore (gland outlet?) is situated posteriorly on each margin of the ventral plate (gl?;
Figs 2
and
4D
) of both males and females.
Internal anatomy (
Figs 2
and
4–6
)
. A long annulated buccal tube (bu) extends between the mouth aperture (mo) and the pharyngeal bulb (pb;
Figs 2
,
4A, 4B
,
5
and
6D
). Posteriorly, the pre-pharyngeal armature is characterized by the presence of three buccal furcae arranged radially, which anchor retractor muscles (not shown). In females, the abdominal region is characterized by the presence of two ovaries (ov;
Fig 6A
), each of which may contain oocytes. Males have two large testes (te) containing spermatozoa (sz;
Fig 6C
).