Marine Biodiversity

, Volume 48, Issue 1, pp 327–355 | Cite as

New species of Semnoderidae (Kinorhyncha: Cyclorhagida: Kentrorhagata) from the Gulf of Mexico

Original Paper

Abstract

Two new species of Semnoderidae from the Gulf of Mexico are described, and the presence of Antygomonas cf. gwenae and a yet undescribed species of Antygomonas is reported. Sphenoderes aspidochelone nov. sp. is recognized by the presence of a first segment forming a closed ring with deep middorsal and midventral incisions, stout, middorsal acicular spines on segments 1 to 11, lateroventral acicular spines on segments 3 to 9, sexually dimorphic laterodorsal spines on segment 10 and minute cuspidate spines in lateroventral positions on segment 5. Semnoderes lusca nov. sp. is characterized by its first segment forming a closed ring with deep, wedge-shaped middorsal and midventral incisions, acicular middorsal spines on segments 1 to 9 and 11, acicular lateroventral spines on segments 2 to 9, crenulated middorsal and midlateral spines on segment 10 and well-developed cuspidate spines on segments 2 (more lateral than acicular spines), 5 (more ventral than acicular spines), 8 (lateral accessory positions) and 9 (ventrolateral positions). A discussion of the diagnostic characteristics of Antygomonas, Sphenoderes and Semnoderes is included. A comparison of these three genera with the specimens recorded in the present study indicates that Antygomonas should be considered as closely related with Sphenoderes and Semnoderes, but it also suggest that A. gwenae could represent a separate lineage within Semnoderidae, and that the species should be reassigned to a new genus.

Keywords

Antygomonas Kinorhynchs Meiofauna Semnoderes Sphenoderes Taxonomy 

Introduction

Currently, twelve named kinorhynch species from the Gulf of Mexico are known. The first kinorhynch species from the Gulf of Mexico (GoM), Echinoderes steineri (Chitwood, 1951), was described from Aransas Bay near Corpus Christi, Texas (Chitwood 1951), but the simplicity of the description does not follow present day standards, and the species is in need of a redescription. Much more recently, a collaborative initiative between the authors of the present contribution prompted the description of several new kinorhynch species collected along the northern shelf of the GoM. The species described so far include Echinoderes augustae Sørensen and Landers, 2014, E. skipperae Sørensen and Landers, 2014, E. joyceae Landers and Sørensen, 2016, E. romanoi Landers and Sørensen, 2016, E. charlotteae Sørensen et al., 2016 and Paracentrophyes sanchezae Sørensen and Landers, 2017 (Sørensen and Landers 2014, 2017; Landers and Sørensen 2016; Sørensen et al. 2016). The surveys furthermore revealed the presence of additional known species, including E. bookhouti Higgins, 1964, E. spinifurca Sørensen et al., 2005, Centroderes barbanigra Neuhaus et al., 2014 and C. readae Neuhaus et al., 2014 (Sørensen et al. 2016; Landers et al. 2017). Additionally, Fleeger et al. (2015) reported the South Carolinian species Echinoderes coulli Higgins, 1977 from Louisiana salt marshes.

The present contribution focuses on species from the GoM belonging to the genera Antygomonas, Sphenoderes and Semnoderes. All three genera are part of the Kentrorhagata (Sørensen et al. 2015), and the two latter are usually united in the family Semnoderidae, whereas Antygomonas is assigned to the monogeneric family Antygomonidae (Adrianov and Malakhov 1999; Sørensen and Pardos 2008; Neuhaus 2013). The genera Semnoderes and Sphenoderes are mainly distinguished by the morphology of segment 1. Both genera are characterized by having a clamshell-like closing mechanism of the head opening, where segment 1 closes the opening through lateral contraction (Higgins 1969; Neuhaus 2013). However, species of Semnoderes show a head opening with deep, wedge-shaped middorsal and midventral incisions, and with the middorsal and midventral placids accordingly being very narrow in order to fit into the pointed wedge-shape (Sørensen et al. 2009). The head opening in species of Sphenoderes also have middorsal and midventral incisions, but they are broader at the bottom, giving the incisions a truncate appearance, and the middorsal and midventral placids are therefore broader proximally and appear triangular (Higgins 1969; Sørensen et al. 2010). Species of Antygomonas also have middorsal and ventral incisions in the anterior margin of segment 1, but these incisions are broadly concave, and not as deep as in Semnoderes and Sphenoderes (Nebelsick 1990; Bauer-Nebelsick 1996; Sørensen 2007; Dal Zotto 2015). One exception is Antygomonas gwenae Herranz et al., 2014, that shows deeper incisions, especially on the ventral side (Herranz et al. 2014). Currently, Antygomonas accommodates five species (Sørensen 2013; Herranz et al. 2014; Dal Zotto 2015), whereas Sphenoderes and Semnoderes accommodate two and three, respectively (Sørensen 2013).

Materials and methods

Samples were taken along the northern GoM continental shelf during 2007 to 2015 (Fig. 1). From 2007 to 2012, samples were taken with a box corer (WildCo©) or a Shipek® sediment grab, and subsequently with an Ocean Instruments® multi-corer. All samples were collected on the National Oceanic and Atmospheric Administration (NOAA) ships Gordon Gunter, Pisces, or Oregon II, in collaboration with the National Marine Fisheries Service Laboratory in Pascagoula, Mississippi. Specimens of Antygomonas, Sphenoderes and Semnoderes were recorded in samples from 2007, 2011 and 2013 to 2015 (Table 1).
Fig. 1

Map showing the collection sites in the northern Gulf of Mexico

Table 1

Summary of data on stations, species identities and catalog numbers (KIN- or NHMD-) for species deposited at the Natural History Museum of Denmark. Boldfaced recordings are new; recordings with regular font are from previous contributions about the Gulf of Mexico kinorhynch fauna (Landers and Sørensen 2016; Sørensen et al. 2016; Sørensen and Landers 2017; Landers et al. 2017)

Station

Date

Position

Depth

Species

Mounting

Type status and catalog numbers

094–2007

Nov. 1, 2007

290 33 56″ N

860 17′ 34″ W

(29.56560, −86.29260)

113 m

Sphenoderes aspidochelone sp. nov.

SEM

1 ♂ Non-type in Sørensen collection

115–2007

Nov. 4, 2007

280 21′ 13″ N

850 53′ 6″ W

(28.35370, −85.88510)

377 m

Sphenoderes aspidochelone sp. nov.

SEM

1 ♂ Non -type in Sørensen collection

154–2011

Nov. 13, 2011

250 29′ 55″ N

840 30′ 02″ W

(25.49850, −84.50050)

436 m

Antygomonas sp.

SEM

1 Non-type in Sørensen collection

055–2013

Nov. 3, 2013

280 20′ 18″ N

900 00′ 52″ W

(28.33830, −90.01450)

107 m

Sphenoderes aspidochelone sp. nov.

Echinoderes augustae

Echinoderes bookhouti

Echinoderes romanoi

Echinoderes skipperae

SEM

LM

LM

SEM

SEM

1 ♀ and 1 ♂ non-type in Sørensen collection

1 non-type: KIN-873

1 non-type: KIN-898

6 non-types in Sørensen collection

1 ♂ non-type in Sørensen collection

074–2013

Nov. 14, 2013

290 49′ 13″ N

860 59′ 6″ W

(29.82020, −86.98490)

186 m

Sphenoderes aspidochelone sp. nov.

Echinoderes charlotteae

SEM

LM

1 ♀ Non-type in Landers collection

1 non-type in Sørensen collection

079–2013

Nov. 15, 2013

290 48′ 21″ N

860 36′ 03″ W

(29.80570, −86.60070)

125 m

Sphenoderes aspidochelone sp. nov.

Centroderes readae

Echinoderes bookhouti

Echinoderes charlotteae

Paracentrophyes sanchezae

SEM

SEM

SEM

LM

SEM

SEM

1 ♀ and 1 ♂ non-type in Sørensen collection

5 non-types in Sørensen collection

1 non-type in Landers collection and 3 non-types in Sørensen collection

2 unmounted non-types in Sørensen collection

1 non-type in Sørensen collection

1 ♂ non-type in Sørensen collection

1 ♂paratype: KIN-1082

134–2013

Nov. 24, 2013

290 46′ 11″

860 51′ 52″ W

(29.76960, −86.86440)

180 m

Sphenoderes aspidochelone sp. nov.

Echinoderes charlotteae

LM

LM

1 ♀ Paratype: NHMD-115837

3 non-types in Sørensen collection

004–2014

Nov. 2, 2014

280 8′ 31″ N

900 57′ 05″ W

(28.14190, −90.95150)

97 m

Sphenoderes aspidochelone sp. nov.

Centroderes barbanigra

Echinoderes bookhouti

SEM

SEM

LM

SEM

1 ♂ Non-type in Landers collection

1 non-type in Sørensen collection

1 non-type in Landers collection

2 non-types in Landers collection

012–2014

Nov. 13, 2014

290 15′ 10″ N

880 18′ 24″ W

(29.25280, −88.30660)

90 m

Sphenoderes aspidochelone sp. nov.

Centroderes barbanigra

Centroderes readae

Echinoderes augustae

Echinoderes bookhouti

Echinoderes romanoi

SEM

SEM

SEM

LM

SEM

SEM

LM

SEM

1 ♂ Non-type in Landers collection

1 ♀ non-type in Landers collection

1 ♀ non-type in Landers collection

15 non-types in Landers collection

2 non-types in Landers collection

3 non-types in Landers collection

1 ♂ holotype, KIN-962, 2 ♀ paratypes, KIN-963 to KIN-964

1 ♂ non-type

025–2014

Nov. 16, 2014

280 07′ 07″ N

910 49′ 34″ W

(28.11850, −91.82620)

88 m

Sphenoderes aspidochelone sp. nov.

Echinoderes bookhouti

Echinoderes charlotteae

Echinoderes romanoi

SEM

LM

LM

SEM

1 ♀ Non-type in Sørensen collection

1 non-type in Landers collection

1 ♀ paratype: KIN-918

1 non-type in Sørensen collection

029–2014

Nov. 19, 2014

(290 58′ 29″ N

860 48′ 02″ W 29.97470, −86.80060)

125 m

Sphenoderes aspidochelone sp. nov.

Centroderes readae

Echinoderes bookhouti

Echinoderes charlotteae

Echinoderes joyceae

LM

LM

LM

LM

LM

♀ Holotype: NHMD-115833; 1 ♀ paratype: NHMD-115834; 1 ♂ paratype: NHMD-115835

2 non-types in Sørensen collection

2 non-types in Sørensen collection

3 non-types in Sørensen collection

1 non-type in Sørensen collection

031–2014

Nov. 20, 2014

290 39′ 35″ N

860 34′ 58″ W

(29.65980, −86.58280)

163 m

Sphenoderes aspidochelone sp. nov.

Echinoderes charlotteae

Echinoderes joyceae

LM

LM

SEM

LM

1 ♀ Paratype: NHMD-115836

1 ♂ paratype: KIN-917

1 ♂ non-type in Sørensen collection

1 ♂ paratype KIN-867

033–2014

Nov. 20, 2014

290 32′ 32″

860 11′ 33″

(29.54230, −86.19260)

98 m

Semnoderes lusca sp. nov.

Echinoderes charlotteae

Echinoderes joyceae

LM

SEM

SEM

1 ♂ Paratype: NHMD-115840

1 ♂ non-type in Landers collection

1 ♀ non-type

035–2014

Nov. 21, 2014

280 54′ 30″ N

121 m

Sphenoderes aspidochelone sp. nov.

SEM

1 ♀ Non-type in Sørensen collection

850 27′ 40″ W

(28.90830, −85.46100)

038–2014

Nov. 22, 2014

290 30′ 59″ N

50 m

Semnoderes lusca sp. nov.

SEM

1 ♂ Non-type in Sørensen collection

870 49′ 36″ W

(29.51640, −87.82660)

101–2015

Oct. 28, 2015

280 09′ 08″ N

77 m

Semnoderes lusca sp. nov.

LM

1 ♂ Holotype: NHMD-115839

920 55′ 04″ W

(28.15230, −92.91770)

111–2015

Oct. 29, 2015

280 36′ 15″ N

37 m

Antygomonas cf. gwenae

LM

1 ♂ Non-type: NHMD-115841

920 20′ 50″ W

(28.60430, −92.34710)

The collected sediment was fixed immediately in 2–5% formaldehyde, and meiofauna was extracted by Ludox centrifugation (Burgess 2001). The extracted meiofauna was sorted under a dissecting microscope, and the specimens were transferred to 70% isopropanol and stored until prepared for light microscopy (LM) or scanning electron microscopy (SEM). Specimens for LM were dehydrated through a graded series of glycerin, mounted in Fluoromount G®, and examined and photographed with an Olympus BX51 microscope using an Olympus DP27 camera. Line art illustrations were based on combined observations from LM and SEM, and composed in Adobe Illustrator® CS6. Measurements were made with CellSens software. All dimensions reported in the tables are based on LM measurements. Specimens for SEM were prepared and examined either at the Natural History Museum of Denmark (NHMD) or at the Auburn University Research Instrumentation Facility (AURIF). Specimens for SEM were transferred from 70% isopropanol to 100% ethanol through a graded series. Some were postfixed in osmium tetroxide vapor, and all specimens were critical point dried, mounted on aluminum stubs, and sputter coated with gold or platinum/palladium. Specimens photographed at NHMD were examined with a JEOL JSM-6335F field emission scanning electron microscope, and specimens photographed at AURIF were examined with a Zeiss EVO 50 scanning electron microscope. All type material is deposited at NHMD.

Material used for comparison included the following: Sphenoderes poseidon, holotype (LM) from NHMD, catalog numbers ZMUC KIN-273, and three specimens (SEM) from the personal collection of the first author. Sphenoderes indicus type material was re-examined (see Sørensen et al. 2010), but the specimens’ condition had deteriorated; hence, all information was extracted from the species’ original description (Higgins 1969). Semnoderes armiger type material is no longer available; instead, non-type specimens from Sweden (see also Sørensen et al. 2009), deposited at NHMD, catalog numbers ZMUC KIN-208 to KIN-219 (LM) and in the personal collection of the first author (SEM), were examined. Semnoderes ponticus type material is no longer available; all information was extracted from the species’ original description (Băcescu and Băcescu 1956). Semnoderes pacificus holotype and allotype (LM) were loaned from the Smithsonian Institution, United States National Museum of Natural History (USNM), catalog numbers USNM-33181 and USNM-33182; the slide with the holotype was completely crystallized and the specimen could no longer be examined, whereas the allotype was still useful for a few observations and photo documentation (see Fig. 12). Antygomonas incomitata non-types from Italy (see also Sørensen et al. 2009), deposited at NHMD, catalog numbers ZMUC KIN-220 to KIN-231 (LM) and in the personal collection of the first author (SEM) were examined. Antygomonas caeciliae: all information was extracted from the species’ original description (Dal Zotto 2015). Antygomonas gwenae: holotype and allotype (LM) were loaned from USNM, catalog numbers USNM-1196402 and USNM-1196403. Antygomonas paulae: holotype and paratypes (LM) were from from NHMD, catalog numbers ZMUC KIN-191 to KIN-204, and numerous specimens (SEM) from the personal collection of the first author. Antygomonas oreas: LM images taken of the type specimens during a previous visit at the Natural History Museum of Vienna, and otherwise information from the species’ original description (Bauer-Nebelsick 1996).

Systematics

Class Cyclorhagida (Zelinka 1896) Sørensen et al. 2015

Order Kentrorhagata Sørensen et al. 2015

Family Semnoderidae Remane 1929

Genus Sphenoderes Higgins, 1969

Sphenoderes aspidochelone sp. nov.

zoobank.org code: urn:lsid:zoobank.org:act:950364F6-BB3D-4AE6-B31D-4D82B2336DC6.

Type material Holotype Adult female, collected from mud on November 19, 2014, from station 029–2014 (Fig. 1, Table 1), at 125-m depth about 60 km southwest of Pensacola, (29o58’29″N 086o48’02″W), mounted in Fluoromount G, deposited at the Natural History Museum of Denmark, under catalog number NHMD-115833.

Paratypes One adult female and one adult male, collected at same station as the holotype. In addition, one adult female, collected from mud on November 20, 2014, from station 031–2014 (Fig. 1, Table 1), at 163-m depth (29o39’35″N 086o34’58″W), and one adult female, collected from mud on November 24, 2013, from station 134–2013 (Fig. 1, Table 1), at 180-m depth (29o46’11″N 086o51’52″W), both near the station of the holotype. All paratypes were mounted in Fluoromount G and deposited at the Natural History Museum of Denmark, under catalog numbers NHMD-115834 to NHMD-115837.

Additional material 11 specimens mounted for SEM and stored in the authors’ personal reference collections (see Fig. 1 and Table 1 for positions and station data). In addition, one specimen tentatively identified as S. aspidochelone sp. nov. was donated by Dr. M. Rohal, Texas A&M University. The specimen was collected at 1020 m of depth in the very southernmost part of the GoM, 236 km east of Heroica Veracruz, Mexico (19o26’51″N 093o53’13″W). The morphology of the Mexican specimen fits the morphology of the type specimens, but due to the distance to the locality of the holotype, and the considerate difference in depths, it is not designated as a type specimen. The specimen is deposited at the Natural History Museum of Denmark, under catalog number NHMD-115838.

Diagnosis Sphenoderes with smooth cuticle of segment 1; cuticle of segments 2 to 11 with minute scale-like hairs in between secondary fringes and free flaps; free flaps with distinct, intracuticular, longitudinal lines. Stout, acicular middorsal spines present on segments 1 to 9; stout, acicular lateroventral spines present on segments 3 to 9; one additional pair of minute cuspidate spines present in lateroventral positions on segment 5. Segment 10 with acicular spines in middorsal and laterodorsal positions in females; males with crenulated spines in same positions. Segment 11 with midterminal, middorsal, laterodorsal and lateral terminal spines.

Etymology The species is named after the sea monster Aspidochelone. The monsters are enormous—as big as an island—and are known to have large spines on their backs, and skin with scales. The two latter characters fit well with the new species.

Description Adults with head, neck and eleven trunk segments (Figs 2, 3, 5a and b). Segment 1 consists of a closed, clamshell-like ring; segments 2 to 11 of a single tergal plate and two sternal plates; tergosternal junctions are formed by intracuticular fissures only, whereas the cuticle appears continuous on the surface. The species appears stout (Fig. 3) and triangular in cross-section, with a long midterminal spine (130.8% of trunk length in average). For complete overview of measures and dimensions, see Table 2. Distribution of cuticular structures, i.e., sensory spots, glandular cell outlets and spines, is summarized in Table 3.
Fig. 2

Line art illustrations of Sphenoderes aspidochelone sp. nov. a. Female, dorsal view. b. Female, ventral view. c. Female, segments 10 to 11 and terminal spines drawn out in full length, dorsal view. d. Male, segments 10 to 11, dorsal view. e. Male, segments 10 to 11, ventral view. Abbreviations: ff, free flap; ld, laterodorsal sensory spot; ldac, laterodorsal acicular spine; ldcr, laterodorsal crenulated spine; lts, lateral terminal spine; lvac, lateroventral acicular spine; lvcu, lateroventral cuspidate spine; mdac, middorsal acicular spine; mdcr, middorsal crenulated spine; mdp, middorsal placid; ml, midlateral sensory spot; mts, midterminal spine; mvp, midventral placid; sd, subdorsal sensory spot; sl, sublateral sensory spot; vm, ventromedial sensory spot

Fig. 3

Scanning electron micrographs showing overviews of Sphenoderes aspidochelone sp. nov. a. Male, laterodorsal view. b. Female, head retracted, lateral view. c. Male, ventral view

Table 2

Measurements from light microscopy of adult Sphenoderes aspidochelone sp. nov. (in μm), including number of measured specimens (n) and standard deviation (SD). Abbreviations: (ac): acicular spine; (cr): crenulated spine; (f), female condition of sexual dimorphic character; LD: laterodorsal; LTS: lateral terminal spine; LV: lateroventral; (m), male condition of sexual dimorphic character; MD, middorsal; MSW-7: maximum sternal width, measured on segment 7 in this species; MTS: midterminal spine; N/A: not applicable; S: segment lengths; SW-10, standard width, always measured on segment 10; TL: trunk length

Character

n

Range

Mean

SD

TL

4

278–350

319

32.26

MSW-7

1

80

N/A

N/A

MSW-7/TL

1

25.8%

N/A

N/A

SW-10

1

34

N/A

N/A

SW-10/TL

1

11.0%

N/A

N/A

S1

4

45–57

51

5.48

S2

4

25–33

30

3.56

S3

4

31–41

35

4.24

S4

4

33–46

40

5.45

S5

4

33–43

41

5.00

S6

4

35–44

41

3.87

S7

4

44–53

48

4.04

S8

4

43–51

48

3.70

S9

4

42–52

46

4.65

S10

4

36–46

42

4.12

S11

4

29–37

32

3.56

MD1 (ac)

4

20–24

22

1.71

MD2 (ac)

4

25–31

28

2.52

MD3 (ac)

4

25–30

28

2.22

MD4 (ac)

4

30–34

32

1.83

MD5 (ac)

4

33–40

37

3.30

MD6 (ac)

4

38–41

39

1.26

MD7 (ac)

4

39–43

41

1.63

MD8 (ac)

4

43–46

45

1.73

MD9 (ac)

3

45–47

46

1.00

MD10 (ac, f)

3

41–52

48

6.08

MD10 (cr, m)

1

46

N/A

N/A

MD11 (ac)

4

195–237

216

20.62

LV3 (ac)

4

21–24

22

1.26

LV4 (ac)

4

25–29

27

1.91

LV5 (ac)

4

27–32

30

2.08

LV6 (ac)

4

29–32

31

1.50

LV7 (ac)

4

32–34

33

1.00

LV8 (ac)

4

32–34

33

0.96

LV9 (ac)

4

37–44

39

3.37

LD10 (ac, f)

3

33–47

39

7.09

LD10 (cr, m)

1

30

N/A

N/A

LD11 (ac)

4

76–87

81

4.65

LTS (ac)

4

50–80

64

12.34

LD11/LTS

4

98.8–152.0%

128.4%

22.11%

MTS (ac)

4

392–440

416

19.76

MTS/TL

4

119.4–141.0%

130.8%

8.92%

Table 3

Summary of nature and location of sensory spots, glandular cell outlets and spines arranged by series in Sphenoderes aspidochelone sp. nov. Abbreviations: LD: laterodorsal; LV: lateroventral; MD: middorsal; ML: midlateral; PD: paradorsal; SD: subdorsal; SL: sublateral; VM: ventromedial; ac, acicular spine; cr, crenulated spine; cu, cuspidate spine; (f), female condition of sexual dimorphic character; lts, lateral terminal spine; (m), male condition of sexual dimorphic character; mts, midterminal spine; ss2/3, sensory spot type 2/type 3

Position Segment

MD

PD

SD

LD

ML

SL

LV

VM

1

ac

 

ss2

ss2

   

ss2

2

ac

ss2

  

ss2

   

3

ac

ss2

 

ss2

 

ss2

ac

ss2

4

ac

ss2

 

ss2

 

ss2

ac

ss2

5

ac

ss2

 

ss2

  

ac, cu

ss2

6

ac

ss2

 

ss2

 

ss2

ac

ss2

7

ac

ss2

 

ss2

 

ss2

ac

ss2

8

ac

ss2

 

ss2

  

ac

ss2

9

ac

ss2

 

ss2

 

ss2

ac

ss2

10

ac(f), cr(m)

 

ss2

ss2(f), ac(f), cr(m)

 

ss2, ss2(m)

  

11

ac, mts

ss3

ss3

ac

 

ss3

lts

 
The head consists of a retractable mouth cone and an introvert (Figs 4, 6a–c). The mouth cone is equipped with nine outer oral styles, each consisting of two joined units, arranged as one style anterior to each introvert sector, with the exception of the middorsal sector 6 (Figs 4, 6a–b). Basally, each style has a sheath with about 12 marginal and terminally bifurcated fringe tips, and a second fringe with rather long fringe tips attaching basally on the sheath (Fig. 6a). The inner mouth cone armature consists of at least a ring with five inner oral styles and a ring with five helioscalids (Fig. 6b); the exact arrangement of inner oral styles and helioscalids, and the eventual presence of additional inner oral styles could not be examined.
Fig. 4

Diagram of mouth cone (gray area), introvert and placids in Sphenoderes aspidochelone sp. nov., showing distribution of outer oral styles, spinoscalids and trichoscalids. The table below shows the scalid arrangement by sector (S1 to S10), and summarized scalid numbers by rings and sectors. Question marks indicate that the occurrences of eventual inner oral styles are uncertain

The introvert sectors are defined by 10 primary spinoscalids in ring 01 (Figs 4, 6c). Each primary spinoscalid consists of a basal sheath and a long, flexible, distal end piece with a blunt tip. The margins of the basal sheaths terminate into a medial fringe, whereas the end-pieces are completely smooth (Fig. 6c). Spinoscalids of rings 02 to 06 also consist of a sheath and an end-piece. These sheaths also show a distal, marginal fringe, and those of rings 02 and 03 have a proximal fringe. End-pieces are smooth and pointed. Scalids become gradually shorter towards the more posterior rings (Fig. 6c). Rings 02 and 04 each have 10 spinoscalids, and rings 03 and 5 have 20, resulting in spinoscalids forming a quincunx in each sector (Fig. 4). Even numbered sectors have no spinoscalids posterior to ring 05, whereas sectors 3, 5, 7 and 9 have a single spinoscalid in ring 06 (Fig. 4). A total of 14 trichoscalids, without trichoscalid plates, are present. Each introvert sector has a single trichoscalid, except sectors 3, 5, 7 and 9 that have two (Fig. 4).

The neck has 16 placids. Middorsal placid narrow; midventral placid trapezoid to triangular. Middorsal and midventral placids located in deep, broad, middorsal and midventral incisions of first trunk segment (Figs 2a–b, 3c, 5c–e, 6d–g). Paradorsal and paraventral placids also elongate, but with curved bases, following the convex shape of the anterior margin of first trunk segment. Other lateral placids short with broad bases; the three most lateral placids are slightly broader than those in subdorsal and ventrolateral positions.
Fig. 5

Light micrographs showing overviews and details of Sphenoderes aspidochelone sp. nov. a–c, e–g. Female holotype, NHMD-115833; d, h. Male paratype, NHMD-115835. a. Dorsal overview. b. Ventral overview. c. Segments 1 to 3, dorsal view. d. Segments 1 to 3, lateral view. e. Segments 1 to 2, ventral view. f. Segments 4 to 8, ventral view. g. Segments 9 to 11, showing female morphology, dorsal view. h. Segments 9 to 11, showing male morphology, lateral view. Abbreviations: ld, laterodorsal sensory spot; ldac, laterodorsal acicular spine; ldcr, laterodorsal crenulated spine; lts, lateral terminal spine; lvac, lateroventral acicular spine; lvcu, lateroventral cuspidate spine; mdac, middorsal acicular spine; mdcr, middorsal crenulated spine; mdp, middorsal placid; ml, midlateral sensory spot; mts, midterminal spine; mvp, midventral placid; sd, subdorsal sensory spot; sl, sublateral sensory spot; sm, anterior segment margin of segment 1; vm, ventromedial sensory spot

Fig. 6

Scanning electron micrographs showing details in head, neck and anterior segments of Sphenoderes aspidochelone sp. nov. a. Mouth cone, middorsal view. b. Mouth cone, polar view, arrow indicates position of missing middorsal outer oral style. c. Introvert, centered at middorsal introvert sector 6. d. Polar view of segment 1 in specimen with retracted head. e. Segments 1 to 2, ventral view. f. Segment 1, subdorsal and middorsal parts. g. Segments 1 to 2, lateral view. Abbreviations: hs, helioscalid; ios, inner oral style; ld, laterodorsal sensory spot; mdp, middorsal placid; ml, midlateral sensory spot; mvp, midventral placid; oos, outer oral style; psp, primary spinoscalid; sd, subdorsal sensory spot; sec 5/6, introvert sectors 5 and 6; sp2–5, spinoscalid followed by introvert ring number; tr, trichoscalid; vm, ventromedial sensory spot

Segment 1 consists of a complete cuticular ring. Anterior margins laterally convex with deep middorsal and midventral incisions, giving the segment a clamshell-like appearance in frontal view (Fig. 6d). Closing of head opening is also clamshell-like, done by bilateral contraction of the two segment halves. Stout acicular middorsal spine, with dense hair covering on exterior surface, present (Figs 2a, 3a–b, 5c); all other acicular spines on segments 2 to 9 have a similar appearance. Sensory spots present in subdorsal, laterodorsal and ventromedial positions (Figs 2a–b, 5d, 6e–g, 7d); all sensory spots on segments 1 to 10 are small and rounded, and belong to type 2 (sensu Nebelsick 1992), i.e., they have numerous micropapillae, a central pore, and a lateral pore with a short tube-like collar (Fig. 7d inset). The segment is completely smooth, without any kind of cuticular hairs (Fig. 6d–g). The only detectable substructures are longitudinal lines on the free flap (Fig. 6e–g). Posterior segment margin without a fringe, but with minute denticles (Fig. 6e); margin with small notch in middorsal position, and extending ventrally into a broad, pointed projection (Fig. 6e, g).
Fig. 7

Scanning electron micrographs showing details in trunk morphology of Sphenoderes aspidochelone sp. nov. a. Segments 3 to 5, dorsal view. b. Segments 4 to 6, ventral view; inset shows lateroventral reduced cuspidate spine, scale = 2 μm. c. Segments 10 to 11 in female, dorsal view. d. Segments 1 to 5, lateral view; inset shows type 2 sensory spot from midlateral position on segment 2, with its characteristic collar around its lateral pore, scale = 1 μm. m. Segments 10 to 11 in male, ventral view. e. Segments 10 to 11 in male, lateral view. Abbreviations: ff, free flap; ld, laterodorsal sensory spot; ldac, laterodorsal acicular spine; ldcr, laterodorsal crenulated spine; lts, lateral terminal spine; lvac, lateroventral acicular spine; lvcu, lateroventral cuspidate spine; mdac, middorsal acicular spine; mdcr, middorsal crenulated spine; ml, midlateral sensory spot; mts, midterminal spine; pd., paradorsal sensory spot; sd, subdorsal sensory spot; sl, sublateral sensory spot; ss3, sensory spot type 3; vm, ventromedial sensory spot

Segment 2 with stout middorsal acicular spine. Sensory spots are present in paradorsal and midlateral positions (Figs 2a, 5d, 6g, 7d). At least one secondary fringe is present on the anterior segment margin, partly covered by a free flap of segment 1, and the segment is covered with minute scale-like hairs between the secondary fringe and the free flap. Posterior segment margin with substructure forming longitudinal lines, weak incisions in lateroventral positions, and a deep incision in the middorsal position.

Segment 3 with stout middorsal and lateroventral acicular spines. Sensory spots present in paradorsal, laterodorsal, sublateral and ventromedial positions (Figs 2a–b, 5d, 7a, d). Hairless patches framed by minute denticles like those in the secondary pectinate fringe, suggest the presence of midlateral and paraventral muscle attachment sites. Secondary fringe, cuticular hairs, free flap and posterior segment margins as on preceding segment. Lateroventral incisions in posterior margin are much deeper though.

Segment 4 similar with preceding segment (Figs 2a–b, 5f, 7a–b, d).

Segment 5 with stout middorsal and lateroventral acicular spines (Figs 2a–b, 5f, 7a–b). In addition, it has a pair of minute (8 μm in length from SEM), flexible lateroventral cuspidate spines located inferior to the much stouter lateroventral acicular spines. The minute spines are very minute, but have otherwise the shape of regular cuspidate spines, i.e., divided into a swollen proximal part with smooth surface, and a thinner distal part covered with minute hairs, and we therefore interpret them as being reduced or modified cuspidate spines (Fig. 7b inset). Sensory spots are present in paradorsal, laterodorsal and ventromedial positions (Figs 2a–b, 7a–b). Secondary fringe, glandular cell outlets, cuticular hairs, free flap and posterior segment margins as on the preceding segment.

Segments 6 and 7 are similar to segments 3 and 4.

Segment 8 is similar to preceding segments, except for the lack of sublateral sensory spots.

Segment 9 is similar to segments 3, 4, 6 and 7.

Segment 10 with middorsal and laterodorsal spines (Figs 2, 5g–h, 7c, e–f). Spines in females are acicular, but less stout than those on preceding segments (Figs 2a–b, 5g, 7c); spines in males are crenulated (Figs 2c–d, 5h, 7f). Sensory spots are present in subdorsal positions in both sexes. Females furthermore with a pair of laterodorsal sensory spots, anterior to laterodorsal spines; males with two pairs of sublateral sensory spots (Fig. 7f). Posterior segment margin still with deep middorsal incision, whereas lateroventral incisions are less deep. Secondary fringe, glandular cell outlets, cuticular hairs and free flap as on preceding segment. Male with deep laterodorsal incisions.

Segment 11 with long, acicular middorsal and midterminal spines, and considerably shorter lateral terminal and laterodorsal spines (Figs 2, 3b–c, 7f; laterodorsal spines are obviously homologous with lateral terminal accessory spines, but they are clearly displaced to a laterodorsal position). Pairs of triangular extensions with terminal sensory spots type 3 are present in paradorsal and sublateral positions (Fig. 7c, e–f). One additional pair of sensory spots type 3 is located in subdorsal positions, but they do not emerge from triangular extensions. Secondary fringe and glandular cell outlets not present. Cuticular hairs still minute and scale-like, lightly scattered over the segment. Posterior segment margin of tergal plate without free flap; posterior margin of sternal plates with free flap, showing an even more prominent substructure of longitudinal lines that almost form palisade-like extensions (Fig. 7e).

Notes on diagnostic features in Sphenoderes aspidochelone sp. nov.

The presence of a clamshell-like closing apparatus in segment 1 (Higgins 1969) assigns the new species to Semnoderidae, and the presence of deep and broad (opposed to wedge-shaped) incisions in the anterior margin of segment 1, and a trapezoid midventral placid (Sørensen et al. 2010), assigns it to Sphenoderes. Currently, Sphenoderes accommodates only two species. The first, Sphenoderes indicus Higgins, 1969, was described from several localities along the east coast of the Indian peninsula (Higgins 1969). The second species, Sphenoderes poseidon Sørensen et al., 2010, was described from the Korea Strait (Sørensen et al. 2010), and was subsequently also recorded from Okinawa, Japan (Yamasaki et al. 2013).

Sphenoderes aspidochelone nov. sp. can be recognized by its low number of cuspidate spines, present on segment 5 only. S. indicus has lateroventral cuspidate spines on segment 5 (more ventral than acicular spine), segment 8 (more ventral than acicular spine) and segment 9 (more lateral than acicular spine), whereas S. poseidon has lateroventral cuspidate spines on segment 5 and 9 (both more ventral than acicular spines; Higgins 1969; Sørensen et al. 2010). Furthermore, even though the cuspidate spines of S. indicus and S. poseidon are rather small, e.g., compared to the very large ones in species of Antygomonas, the cuspidate spines in S. aspidochelone nov. sp. are even smaller and so reduced that it hard to identify them as true cuspidate spines. Furthermore, S. aspidochelone nov. sp. differs from S. indicus by having segment 1 composed as a closed ring, as opposed to having a small dorsal, a small ventral and two large lateral plates, as described in S. indicus (Higgins 1969). The composition of segment 1 in S. aspidochelone nov. sp. is identical with the one found in S. poseidon. S. aspidochelone nov. sp. also differs from its two congeners in regard to its secondary sexual characters. S. indicus and S. poseidon do not show any particular sexual dimorphism in their spines on segment 10. S. aspidochelone nov. sp. has females with regular acicular middorsal and laterodorsal spines, while these spines are crenulated in males. A similar sexual dimorphism is quite common among other kentrorhagid species, such as species of Zelinkaderes (Higgins 1990; Bauer-Nebelsick 1995; Sørensen et al. 2007; Altenburger et al. 2015), Centroderes (Neuhaus et al. 2013, 2014), Triodontoderes anulap (Sørensen and Rho 2009), Tubulideres seminoli (Sørensen et al. 2007) and Wollunquaderes majkenae (Sørensen and Thormar 2010; see also the new species of Semnoderes described below). S. indicus may potentially have a secondary sexual dimorphic character that would make it differ from its congeners. In the description, Higgins (1969) reports the presence of “keyhole-shaped muscle scars?” lateroventrally on segment 8 and ventromedially on segment 9. He does not mention though whether this character is restricted to females only. This may be the case. From their positions and the way they are illustrated, these keyhole-shaped structures show great resemblance with the minute female papillae that have been reported from various species, e.g., Antygomonas gwenae (Herranz et al. 2014), Wollunquaderes majkenae (Sørensen and Thormar 2010) and species of Campyloderes (Neuhaus and Sørensen 2013). If this interpretation is correct, this would be the first only example of female papillae in a species of Sphenoderes.

Information from SEM is not available for S. indicus, so eventual similarities or differences in the detailed cuticular surface morphology can only be provided for S. poseidon and S. aspidochelone nov. sp. The two species both show the same general trunk shape and cuticle of medium thickness. The very stout middorsal and lateroventral acicular spines, each with an exterior area of densely set minute hairs, are also common for both species. S. indicus appears to have some stout spines (Higgins 1969), but the hairs are not visible in LM. Also, the cuticular ornamentation of segments 2 to 11 is identical in both species, as they both have a dense covering of small, triangular scale-like hairs between the secondary fringes and the free flap, and free flaps with longitudinal lines. Such longitudinal lines are also illustrated on the free flaps of S. indicus (Higgins 1969). Cuticular ornamentation differs on segment 1 though, which is completely naked in S. aspidochelone nov. sp., as opposed to S. poseidon that has well-developed leaf-like hairs (Sørensen et al. 2010). Another interesting similarity is the morphology of the sensory spots on segments 1 to 10, that all seem to belong to type 2 (sensu Nebelsick 1992), i.e., the lateral pore has a small tube-like protrusion or collar.

Genus Semnoderes Zelinka, 1907.

Semnoderes lusca sp. nov.

zoobank.org code: urn:lsid:zoobank.org:act:3C946426-D97B-46BE-B343-EB00B84648C5.

Type material Holotype Adult male, collected from mud on October 28, 2015, from station 101–2015 (Fig. 1, Table 1), at 77 m of depth, 175 km south of the Louisiana coast line, and 220 km southeast of Galveston, TX (28o09’08″N 092o55’04″W), mounted in Fluoromount G, deposited at the Natural History Museum of Denmark, under catalog number NHMD-115839.

Paratypes One adult male, collected from mud on November 20, 2014, from station 033–2014 (Fig. 1, Table 1), at 98 m of depth 82 km southwest of Panama City, FL (29o32’32″N 086o11’33″W), mounted in Fluoromount G, deposited at the Natural History Museum of Denmark, under catalog number NHMD-115840.

Additional material One adult male, collected from mud on November 22, 2014, from station 038–2014 (Fig. 1, Table 1), at 50 m of depth 143 km east northeast of the Mississippi River outlet, south of Mobile, AL, (29o30’59″N 087o49’36″W), mounted for SEM and stored in the personal collection of the first author.

Diagnosis Semnoderes with primary spinoscalids with one septum, forming single distal chamber. Tergal plates of all segments with scattered leaf-like cuticular hairs; free flaps with distinct, intracuticular, longitudinal lines. Acicular middorsal spines present on segments 1 to 9 and 11, getting progressively stronger towards the posterior segments; acicular lateroventral spines present on segments 2 to 9, small and flexible on segment 2, much more well-developed on segments 3 to 9; lateroventral series also with well-developed cuspidate spines on segments 2 and 5, more lateral than acicular spines on segments 2, and more ventral on segments 5, lateral accessory cuspidate spines on segment 8, and ventrolateral cuspidate spines on segment 9. Segment 10 with crenulated middorsal and midlateral spines in males; female morphology unknown. Segment 11 with midterminal, midlateral and lateral terminal spines.

Etymology The species is named after the Caribbean sea monster Lusca—a monster sometimes described as a gigantic octopus, or a hybrid between a shark and an octopus, sometimes simply as a dragon-like creature or evil sea spirit.

Description Adults with head, neck and eleven trunk segments (Figs 8, 9a, 10a). Segment 1 consists of a closed, clamshell-like ring; segments 2 to 11 of a single tergal plate and two sternal plates. The species has a relatively soft cuticle and appears triangular in cross-section, with long midterminal spine (134% to 147% of trunk length). For complete overview of measures and dimensions, see Table 4. Distribution of cuticular structures, i.e., sensory spots, glandular cell outlets and spines, is summarized in Table 5.
Fig. 8

Line art illustrations of male Semnoderes lusca sp. nov. a. Dorsal view. b. Ventral view. c. Segment 11 and midterminal spine drawn out in full length, dorsal view (midlateral spines are omitted). Abbreviations: ff, free flap; lacu, lateral accessory cuspidate spine; ld, laterodorsal sensory spot; lts, lateral terminal spine; lvac, lateroventral acicular spine; lvcu, lateroventral cuspidate spine; mdac, middorsal acicular spine; mdcr, middorsal crenulated spine; mdp, middorsal placid; ml, midlateral sensory spot; mlac, midlateral acicular spine; mlcr, midlateral crenulated spine; mts, midterminal spine; mvp, midventral placid; sd, subdorsal sensory spot; sl, sublateral sensory spot; ss3, sensory spot type 3; vl, ventrolateral sensory spot; vlcu, ventrolateral cuspidate spine

Fig. 9

Light micrographs showing overviews and details of Semnoderes lusca sp. nov., male holotype, NHMD-115839. a. Lateral overview. b. Segment 1, lateral view, focused at anterior segment margin. c. Dorsal half of segment 1, lateral view, focused at middorsal wedge-shaped incision (arrow). d. Ventral half of segment 1, lateral view, focused at midventral wedge-shaped incision (arrow). e. Segments 2 to 4, lateral view. f. Segments 4 to 7, lateral view, note the dense covering of minute cuticular hairs. g. Segments 9 to 11, showing male morphology, lateral view. h. Segments 9 to 11, showing male morphology, lateral view, note the sperm cells that fill up segments 9 and 10. Abbreviations: lacu, lateral accessory cuspidate spine; ld, laterodorsal sensory spot; lts, lateral terminal spine; lvac, lateroventral acicular spine; lvcu, lateroventral cuspidate spine; mdac, middorsal acicular spine; mdcr, middorsal crenulated spine; ml, midlateral sensory spot; mlac, midlateral acicular spine; mlcr, midlateral crenulated spine; mts, midterminal spine; pl, placid; psp, primary spinoscalid; sd, subdorsal sensory spot; sl, sublateral sensory spot; sm, anterior segment margin of segment 1; ss3, sensory spot type 3; tr, trichoscalid; vl, ventrolateral sensory spot; vlcu, ventrolateral cuspidate spine

Fig. 10

Scanning electron micrographs showing overviews and details head, neck and anterior segments of Semnoderes lusca sp. nov. a. Lateroventral overview. b. Introvert, centered at midventral introvert sector 1. c. Mouth cone, centered above midventral introvert sector 1. d. Segments 1 to 2, laterodorsal to middorsal parts of left segment half. e. Segments 1 to 3, ventral view. Abbreviations: ff, free flap; ld, laterodorsal sensory spot; lvac, lateroventral acicular spine; lvcu, lateroventral cuspidate spine; mdp, middorsal placid; mdac, middorsal acicular spine; mvp, midventral placid; oos, outer oral style; pd., paradorsal sensory spot; psp, primary spinoscalid; sec 1, introvert sector 1; sp2–6, spinoscalid followed by introvert ring number; tr, trichoscalid; vl, ventrolateral sensory spot

Table 4

Measurements from light microscopy of adult male holotype and paratype of Semnoderes lusca sp. nov. (in μm). Abbreviations: (ac): acicular spine; (cr): crenulated spine; (cu): cuspidate spine; LA: lateral accessory; LTS: lateral terminal spine; LV: lateroventral; MD, middorsal; ML: midlateral; MTS: midterminal spine; S: segment lengths; TL: trunk length; VL: ventrolateral; − missing data

Character

Holotype

Paratype

TL

474

396

S1

64

56

S2

47

38

S3

50

45

S4

54

51

S5

51

52

S6

60

57

S7

59

58

S8

66

62

S9

71

66

S10

60

67

S11

57

49

MD1 (ac)

46

34

MD2 (ac)

51

38

MD3 (ac)

57

45

MD4 (ac)

68

47

MD5 (ac)

72

52

MD6 (ac)

57

MD7 (ac)

82

60

MD8 (ac)

84

65

MD9 (ac)

84

69

MD10 (cr)

72

52

MD11 (ac)

201

148

LV2 (cu)

22

20

LV3 (ac)

38

29

LV4 (ac)

38

40

LV5 (cu)

22

21

LV5 (ac)

53

43

LV6 (ac)

57

50

LV7 (ac)

58

65

LA8 (cu)

22

24

LV8 (ac)

56

56

VL9 (cu)

20

LV9 (ac)

76

82

LD10 (cr)

48

39

ML11 (ac)

185

140

LTS (ac)

108

87

ML11/LTS

171.3%

160.9%

MTS (ac)

697

531

MTS/TL

147.0%

134.1%

Table 5

Summary of nature and location of sensory spots, glandular cell outlets and spines arranged by series in Semnoderes lusca sp. nov. Abbreviations: LA: lateral accessory; LD: laterodorsal; LV: lateroventral; MD: middorsal; ML: midlateral; PD: paradorsal; SD: subdorsal; SL: sublateral; VL: ventrolateral; ac, acicular spine; cr, crenulated spine; cu, cuspidate spine; lts, lateral terminal spine; mts, midterminal spine; ss2/3, sensory spot type 2/type 3

Position Segment

MD

PD

SD

LD

ML

SL

LA

LV

VL

1

ac

ss2

 

ss2

    

ss2

2

ac

ss2

  

ss2

gco

 

cu, ac

 

3

ac

ss2

 

ss2

 

ss2

 

ac

ss2

4

ac

ss2

   

ss2

 

ac

ss2

5

ac

ss2

 

ss2

   

ac, cu

ss2

6

ac

ss2

 

ss2

 

ss2

 

ac

ss2

7

ac

ss2

 

ss2

 

ss2

 

ac

ss2

8

ac

ss2

 

ss2

  

cu

ac

ss2

9

ac

ss2

 

ss2

 

ss2

 

ac

cu, ss2

10

cr

 

ss2

 

cr, ss2

    

11

ac, mts

ss3

ss3

 

ac

  

lts

ss3

The head consists of a retractable mouth cone and an introvert (Fig. 10b–c). The mouth cone is equipped with nine outer oral styles, each consisting of two joined units, arranged as one style anterior to each introvert sector, except the middorsal sector 6. Basally, each style has a sheath with about seven marginal and terminally bifurcated fringe tips, and a second fringe with two or three rather long fringe tips attaching basally on the sheath (Fig. 10c). Inner mouth cone armature includes inner oral styles and helioscalids, but their exact arrangement could not be examined.

The introvert sectors are defined by 10 primary spinoscalids in ring 01. Each primary spinoscalid consists of a basal sheath and a long, flexible, distal end piece with a blunt tip (Fig. 10b). The basal sheaths have a basal spike, flanked by a pair of more flexible spikes. These spikes overlays a second triplet of spikes, where the median one is longest and strongest, and the lateral ones are more flexible and bifurcating. The distal margins of the sheaths terminate laterally into paired, brush-like fringes. The distal end pieces are covered with minute hairs, and have a single internal septum, forming a distal chamber (Figs 9b, 10b). Spinoscalids of rings 02 to 06 also consist of a sheath and an end piece. These sheaths also show a proximal pair of lateral fringes, a row of densely set hairs on the exterior surface, and terminate distally into a fringed margin. End pieces are covered with minute hairs and pointed. Scalids become gradually shorter towards the more posterior rings. Scalid arrangements could only be examined in introvert sectors 1 (Fig. 10b), and 8 to 10. Sectors 8 and 10 have a single spinoscalid in rings 02 and 04, and paired spinoscalids in rings 03 and 5. Sectors 1 and 9 are similar but have in addition a single spinoscalid in ring 06. Single trichoscalids are present in sectors 1 and 8 and 10, whereas sector 9 has two trichoscalids; trichoscalid plates are not present.

The neck has 16 placids. Middorsal placid narrow and pointed; midventral placid rather narrow and rod-shaped, but with a somehow rounded proximal end (Fig. 10b). Middorsal and midventral placids located in deep, middorsal and midventral wedge-shaped incisions of first trunk segment (Figs 8a–b, 9c–d, 10d–e). Paradorsal and paraventral placids also elongate, but with curved bases, following the convex shape of the lateral anterior margins of the first trunk segment (Figs 9b, 11a). Other lateral placids short with broad bases.
Fig. 11

Scanning electron micrographs showing overviews and details in trunk morphology of Semnoderes lusca sp. nov. a. Segments 1 to 3, lateral view. b. Segments 8 to 11, lateral view. c. Segments 6 to 11, dorsal view. d. Segments 6 to 9, ventral view. e. Segments 9 to 11, ventral view. Abbreviations: ff, free flap; gco, glandular cell outlet; lacu, lateral accessory cuspidate spine; ld, laterodorsal sensory spot; lts, lateral terminal spine; lvac, lateroventral acicular spine; lvcu, lateroventral cuspidate spine; mdac, middorsal acicular spine; mdcr, middorsal crenulated spine; ml, midlateral sensory spot; mlac, midlateral acicular spine; mlcr, midlateral crenulated spine; mts, midterminal spine; pd., paradorsal sensory spot; sd, subdorsal sensory spot; ss3, sensory spot type 3; vl, ventrolateral sensory spot; vlcu, ventrolateral cuspidate spine

Segment 1 consists of a complete cuticular ring. Anterior margins laterally convex with deep middorsal and midventral wedge-shaped incisions, giving the segment a clamshell-like appearance in frontal view (Figs 8a–b, 9b–d, 10d, 11a). Closing of head opening is also clamshell-like, done by bilateral contraction of the two segment halves. Short and relatively flexible acicular middorsal spine present (Figs 8a, 10d). Sensory spots present in paradorsal, laterodorsal and ventrolateral positions (Figs 8a–b, 9b, 10d–e, 11a); all sensory spots on segments 1 to 10 are relatively large and oval, and those that could be examined in detail belong to type 2 (sensu Nebelsick 1992). The segment is covered by short, bamboo leaf-like hairs (Fig. 11a). Free flap with intracuticular longitudinal lines. Posterior segment margin without a fringe, but with deep ventrolateral incisions, and slightly serrated edge.

Segment 2 with middorsal acicular spines, being slightly stronger than the one on the preceding segment. In addition with rather small and flexible acicular lateroventral spines (9 μm from SEM), and a pair of well-developed cuspidate spines (Figs 8b, 9e, 10e). Sensory spots are present in paradorsal and midlateral positions (Figs 8a, 10d, 11a). Secondary fringes could not be detected on this or any of the following segments. Hairless patches framed by minute denticles suggest the presence of sublateral glandular cell outlets. The middorsal area, anterior to the middorsal spine is covered by a triangular area of densely set minute hairs (Fig. 10d); remaining tergal plate is covered with minute leaf-like hairs that extend onto the free flap; sternal plates with minute scale-like hairs only. Posterior segment margin as preceding segment.

Segment 3 with middorsal acicular spines, being slightly stronger than the one on the preceding segment, and with well-developed lateroventral acicular spines (Fig. 8a–b). Sensory spots present in paradorsal, laterodorsal, sublateral and ventrolateral positions (Figs 8a–b, 9e, 11a). Glandular cell outlets as on preceding segment present, but in midlateral positions (Fig. 9e). Cuticular hairs, free flap and posterior segment margins as on preceding segment.

Segment 4 with middorsal acicular spine, being distinctively stronger than the one on the preceding segment, and with a well-developed lateroventral acicular spine (Fig. 8a–b). Sensory spots present in paradorsal, sublateral and ventrolateral positions (Figs 8a–b, 9e–f). Cuticular hairs, glandular cell outlets, free flap and posterior segment margins as on preceding segment.

Segment 5 with strong acicular middorsal spine, well-developed lateroventral acicular spines, and, closer to the ventral side, well-developed lateroventral cuspidate spines (Figs 8a–b, 9f). Sensory spots are present in paradorsal, laterodorsal and ventrolateral positions. Cuticular hairs, glandular cell outlets, free flap and posterior segment margins as on preceding segment.

Segments 6 and 7 are similar with segment 3, but with considerably stronger middorsal and lateroventral spines (Figs 8a–b, 11c).

Segment 8 with well-developed middorsal and lateroventral acicular spines, and lateral accessory cuspidate spines (Figs 8a–b, 11c). Sensory spots are present in paradorsal, laterodorsal and ventrolateral positions (Figs 8a–b, 9g, 11b, 11d). Cuticular hairs, glandular cell outlets, free flap and posterior segment margins as on preceding segment.

Segment 9 with well-developed middorsal and lateroventral acicular spines, and ventrolateral cuspidate spines (Figs 8a–b, 9g, 11b–e). Sensory spots are present in paradorsal, laterodorsal, sublateral and ventrolateral positions (Figs 8a–b, 9g, 11b, 11d–e). Cuticular hairs, glandular cell outlets, free flap and posterior segment margins as on preceding segment.

Segment 10 with middorsal and midlateral crenulated spines in the three male specimens available for the description (Figs 8a–b, 9g–h, 11b–c); female spine morphology is unknown. Sensory spots are present in subdorsal and midlateral positions (Figs 8a, 9g, 11g). Posterior segment margin with middorsal incision and midlateral incisions at spines, and with more broadly concave incisions in ventrolateral positions. Cuticular hairs more scale-like than leaf-like, especially on posterior segment half. Otherwise, glandular cell outlets, cuticular hairs and free flap as on preceding segment.

Segment 11 with very long, acicular midterminal spines (Figs 8c, 9a), and shorter middorsal, lateral terminal and midlateral spines (midlateral spines are obviously homologous with lateral terminal accessory spines, but they are clearly displaced to a midlateral position); midlateral spines are considerably stronger than middorsal and lateral terminal spines. Pairs of cone-shaped extensions with terminal sensory spots type 3 are present in paradorsal positions, dorsal to midterminal spine (Figs 8a, 11b). Additional pairs of sensory spots type 3 are located in subdorsal and ventrolateral positions, but they do not emerge from cone-shaped extensions. Glandular cell outlets not present. Cuticular hairs very minute and scale-like, lightly scattered over the segment. Posterior segment margin of tergal plate without free flap; posterior margin of sternal plates with free flap, with intracuticular longitudinal lines.

Notes on diagnostic features in Semnoderes lusca sp. nov.

The clamshell-like closing apparatus in segment 1 (Higgins 1969) assigns the new species to Semnoderidae, and the presence of deep, wedge-shaped middorsal and midventral incisions in the anterior margin of segment 1, and a rod-shaped midventral placid (Sørensen et al. 2009), assigns it to Semnoderes.

Currently, Semnoderes accommodates three species: Semnoderes armiger Zelinka, 1928, Semnoderes ponticus Băcescu and Băcescu, 1956 and Semnoderes pacificus Higgins, 1967. Semnoderes armiger is widely distributed in the Mediterranean Sea and throughout Western Europe and the eastern North Atlantic. It was originally described from two localities in the Adriatic Sea, and near Barcelona in the Western Mediterranean (Zelinka 1928), and has subsequently been reported from several Mediterranean localities along the Spanish east coast (Sánchez et al. 2012), around the Italian Peninsula (Dal Zotto and Todaro 2016), from the Black Sea (Sheremetevskij 1974), the Cantabric Sea (Sørensen and Pardos 2008), the North Sea, east of Scotland (McIntyre 1962), the Faroe Islands (Sørensen and Pardos 2008), the Swedish east coast (Nyholm 1947; Sørensen et al. 2009) and off Bergen in Norway (Sørensen et al. 2015; see Neuhaus 2013, p. 280 for additional references). This species is easily distinguished from S. lusca nov. sp. by the spine formula, in that S. armiger has a cuspidate lateroventral spine on segment 6 that is not present in S. lusca. Additionally, the arrangement of the trichoscalids differs in that S. armiger has two trichoscalids in sector 8, while S. lusca has two in sector 9, and S. armiger does not have septa on the primary spinoscalids whereas S. lusca nov. sp. has a single distal septum on that structure.

Another interesting difference can be found in the cuticular ornamentation of the two species. Whereas S. lusca nov. sp. has minute, leaf-like cuticular hairs on the tergal plates of all segments, S. armiger has leaf-like hairs on segment 1 only, and these are even so narrow that they resemble acicular hairs. On the following segments, S. armiger has very minute acicular hairs. The morphology of cuticular hairs should of course only be used with caution in morphological comparison, because the appearance of the hairs could be different in recently molted specimens, but at least for S. armiger the morphology is constant for all nineteen specimens examined with SEM, from both Espegrend (Norway) and Tjärnö (Sweden; Sørensen, unpubl. obs.). This could indicate that hair morphology and patterning also plays a significant role in semnoderid taxonomy.

The distribution pattern of acicular spines are identical in S. lusca nov. sp. and S. armiger (as well as the two additional congeners), but the spines in S. armiger all appear slightly stronger, and less flexible than those in S. lusca nov. sp. The middorsal spines especially of S. armiger appear much more rigid than the middorsals in S. lusca nov. sp. In traditional cyclorhagid taxonomy, characters like spinoscalid morphology, cuticular ornamentation and spine morphology are usually not considered to be of very great taxonomic value, but with the discovery of new species showing identical spine patterns, this necessitates a need for exploring new morphological characters. This issue will be addressed further in the general discussion below, since species with identical spine patterns will be a future challenge within other kentrorhagid genera as well.

The second species, Semnoderes ponticus Băcescu and Băcescu, 1956 is known from its type locality at the Romanian Black Sea coast only, and with lateral cuspidate spines on segments 2, 4, 5, 6, 8 and 9, this species is also easily distinguished from S. lusca nov. sp. Otherwise, very little information is available for S. ponticus. Besides the spine pattern, the only useful information provided by Băcescu and Băcescu (1956) is the trunk length of 450 μm and midterminal spine length of 520 μm (mistakenly printed in Băcescu and Băcescu (1956) as 45 μm and 52 μm, respectively, but the scale on the line art illustration indicate the correct dimensions). These measures indicate that S. lusca nov. sp. and S. ponticus pretty much have the same sizes.

The third species, Semnoderes pacificus Higgins, 1967 was described from New Caledonia in the southwest Pacific, and in the same contribution reported from California as well (Higgins 1967). The spine formula of Semnoderes lusca nov. sp. is basically identical with the one of S. pacificus, and due to the limited information provided in the description of S. pacificus, it is extremely challenging to point out differential characters. To complicate things further, examination of the S. pacificus types (Fig. 12) provided very little new information because they were in such a poor condition. The slide with the holotype was heavily crystalized and it was impossible to locate the specimen. For the allotype, it was possible to get a rough outline of the anterior 2/3 of the trunk (Fig. 12a), but cuticular details were only visible on segment 8 (Fig. 12c), due to severe dirt and bleaching. Sensory spots were not visible on any segment.
Fig. 12

Light micrographs showing overviews and details of Semnoderes pacificus, female allotype, USNM 33182. a. Segments 1 to 9, lateral overview. b. Segments 1 to 4, lateral view. c. Segment 8, lateral view, note cuticular ornamentation. Abbreviations: lvcu, lateroventral cuspidate spine; mdac, middorsal acicular spine

In the description of S. pacificus, Higgins (1967) provides information about the spine arrangements, and segment and spine measures. He furthermore notes that the scalids of the first row of the introvert, i.e., the primary spinoscalids, have eight joined distal units, and that the surface of the trunk segments shows a “spinulate sculpture pattern”. Additionally, Higgins (1967) illustrated the holotypic male with regular acicular spines on segment 10 (Fig. 12 in Higgins 1967). Although subtle, these characters may provide hints to distinguish S. lusca nov. sp. and S. pacificus. The eight, distal joined units in the primary spinoscalids of S. pacificus obviously refers to the presence of internal septa, giving the distal ends of the primary spinoscalids an annulated appearance. As opposed to S. pacificus, the new species has a single distal septum only, which can be considered a differential character. Furthermore, the cuticular sculpturing appears to differ between the species. The tergal plates of S. lusca nov. sp. are covered by minute leaf-like cuticular hairs (as known from Sphenoderes aspidochelone nov. sp. and Antygomonas paulae and A. incomitata, see Sørensen 2007; Sørensen et al. 2009), that forms a homogenous surface sculpturing on each segment (see, e.g., Fig. 9f). The hair pattern of S. pacificus appears to be different. It is not exactly clear what is meant with “spinulate sculpture pattern”, but “spinulate” could refer to the presence of scale-like hairs, and the sculpture pattern that Higgins (1967) by the time of the description was able to observe on all segments, could be the highly characteristic one that today is retained only on segment 8 of the allotype (Fig. 12c). This segment shows a sculpturing with minute scale-like hairs arranged in very conspicuous lines, which differs considerably from the homogenous sculpturing in S. lusca nov. sp. Finally, the secondary male characters differ between the species. Males of S. lusca nov. sp. have crenulated spines on segment 10, whereas males of S. pacificus according to Higgins (1967) show regular acicular spines.

Meristically, it is also possible to detect some differences between S. lusca nov. sp. and S. pacificus, even though meristic data from small sample sizes of course should be used with some caution. In general, middorsal spines appears to be about 50% to 100% longer in S. lusca nov. sp., and the difference in length become more expressed on the more posterior segments. Especially the difference in lengths of middorsal spines on segment 11, 148 μm to 201 μm in S. lusca nov. sp. versus 79 μm in S. pacificus, is quite prominent. Also the lateral terminal spines and midlateral spines of segment 11 (equivalent to lateral terminal accessory spines in S. pacificus) are longer in S. lusca nov. sp., and especially the lateral terminal spines are about twice as long as in S. pacificus (note that measures for LTS and LTAS in Table 2 in Higgins 1967 accidentally have been switched). Hence, based on meristic differences combined with the characters discussed above, it is possible to distinguish S. lusca nov. sp. from other congeners.

Family Antygomonidae Adrianov and Malakhov, 1994

Genus Antygomonas Nebelsick, 1990

In addition to the two new semnoderid species, two species of Antygomonas are reported. One is identified as Antygomonas gwenae Herranz et al., 2014 (Fig. 13a–e, h) whereas the second one most likely represents a new species (Fig. 14) that is not described due to the limited amount of material.
Fig. 13

Light micrographs showing overviews and details of a–e, h Antygomonas cf. gwenae male from the Gulf of Mexico, and f–g Antygomonas gwenae male holotype, USNM 1196402. a. Laterodorsal overview. b. Segments 1 to 3, dorsal view. c. Segments 1 to 3, ventral view. d. Segments 8 to 9, laterodorsal view. e. Segments 10 to 11, focused on laterodorsal spine of segment 10. f. Laterodorsal spine of segment 10. g. Middorsal spine of segment 10. h. Segments 10 to 11, lateral view. Abbreviations: lacu, lateral accessory cuspidate spine; ld, laterodorsal sensory spot; ldac, laterodorsal acicular spine; ltas, lateral terminal accessory spine; lts, lateral terminal spine; lvac, lateroventral acicular spine; mdac, middorsal acicular spine; ml, midlateral sensory spot; mvp, midventral placid; sl, sublateral sensory spot; sm, anterior segment margin of segment 1; vlcu, ventrolateral cuspidate spine; vm, ventromedial sensory spot

Fig. 14

Scanning electron micrographs showing overviews and details in trunk morphology of Antygomonas sp. a. Lateroventral overview. b. Segments 6–11, lateroventral view. c. Ventral overview. d. Segments 4–8, ventral view. Abbreviations: ep, epibiont; lacu, lateral accessory cuspidate spine; lts, lateral terminal spine; lvcu, lateroventral cuspidate spine; lv, lateroventral sensory spot; mlac, midlateral acicular spine; mlcr, midlateral crenulated spine; vl, ventrolateral sensory spot; vlcu, ventrolateral cuspidate spine

Antygomonas cf. gwenae Herranz et al., 2014

Material One adult male, collected from mud on October 29, 2015, from station 111–2015 (Fig. 1, Table 1), at 37 m of depth, south of Lafayette, LA, (28o21’44″N 092o12’30″W), mounted in Fluoromount G, deposited at the Natural History Museum of Denmark, under catalog number NHMD-115841.

Short description Measures of spine and segment lengths and dimensions are provided in Table 6, and the details of the specimen are shown in Fig. 13a–e and Fig. 13h. The specimen generally corresponds well to the original description of A. gwenae (see Herranz et al. 2014) regarding spine pattern, distribution of sensory spots, and the characteristic middorsal and midventral incisions of the anterior margin of segment 1. One noteworthy difference though regards the middorsal and laterodorsal spines of segment 10 (Fig. 13e, h). The spines on this segment are considerably thinner than the otherwise rather stout spines on the remaining segments, but they are clearly acicular and not crenulated as stated in the original description. Also the segment and spine lengths are within or at least close to the ranges provided in the original description. Only two noteworthy deviations were noted. One regards the length of the middorsal spine on segment 11 that is 66 μm in the Gulf specimen, as opposed to 31–49 μm in the type material. The second regards the dimensions of the lateral accessory terminal spines and lateral terminal spines, that are nearly the same length in the Gulf specimen (LTAS/LTS ratio = 89.1%), whereas the lateral terminal accessory spines are about twice as long as the lateral terminal spines in the type material.
Table 6

Measurements from light microscopy of adult male of Antygomonas cf. gwenae (in μm). Abbreviations: (ac): acicular spine; (cu): cuspidate spine; LA: lateral accessory; LTAS: lateral terminal accessory spine; LTS: lateral terminal spine; LV: lateroventral; MD, middorsal; MSW-6: maximum sternal width, measured on segment 6 in this specimen; MTS: midterminal spine; S: segment lengths; TL: trunk length; VL: ventrolateral

Character

A. cf. gwenae

TL

353

MSW-6

69

MSW-6/TL

19.5%

S1

43

S2

27

S3

35

S4

39

S5

38

S6

39

S7

41

S8

43

S9

46

S10

44

S11

32

MD1 (ac)

26

MD2 (ac)

25

MD3 (ac)

27

MD4 (ac)

30

MD5 (ac)

28

MD6 (ac)

33

MD7 (ac)

32

MD8 (ac)

32

MD9 (ac)

35

MD10 (ac)

32

MD11 (ac)

66

LV2 (cu)

22

LV3 (ac)

17

LV4 (ac)

23

LV5 (cu)

21

LV5 (ac)

26

LV6 (ac)

28

LV7 (ac)

32

LA8 (cu)

22

LV8 (ac)

36

VL9 (cu)

26

LV9 (ac)

36

LD10 (cr, m)

35

LTAS (ac)

49

LTS (ac)

55

LTAS/LTS

89.1%

MTS (ac)

398

MTS/TL

112.7%

The tergal plates of all segments appear to be covered with minute acicular or leaf-like hairs, and the free flaps have clear longitudinal lines.

Notes on diagnostic features in Antygomonas cf. gwenae.

Based on the concordant spine formulas and distribution of sensory spots, this specimen, with some hesitation, is identified as Antygomonas cf. gwenae. The hesitation is mostly due to the metric difference mentioned above, regarding the length of the middorsal spine of segment 11, and the LTAS/LTS dimensions. The recorded specimen also differed from the original description by the male morphology of the spines of segment 10, that opposite to the description were thin and acicular, and not crenulated. However, examination of the male A. gwenae holotype revealed that this specimen also has acicular spines on segment 10 (Fig. 13f–g). The spines are clearly thinner than those on the remaining segments, which might have led the authors to misinterpret the spines as crenulated. Further discussion of A. gwenae and its generic assignment are provided below in the general discussion.

Antygomonas sp.

Material One adult male, collected from silty sand on November 13, 2011, from station 154–2011 (Fig. 1), at 436 m of depth off Florida, about 214 km south of Tallahassee and 209 km northwest of Tampa (25o29’55″N 084o30’02″W), mounted for SEM and stored in the first authors reference collection.

Short description Trunk consisting of eleven segments (Fig. 14a, c), with segment 1 forming a closed ring, and segments 2 to 11 composed of one tergal and two sternal plates. Segment 1 with middorsal and midventral incisions, resembling the condition in A. gwenae. Placids of the neck are quite long, with a distinct elongate, trapezoid shape. Due to the shape of the neck opening, the middorsal and midventral placids are the longest. All placids have nearly the same width at their bases, except for the paraventral ones that are narrower. The trunk cuticle appears relatively thin, even though the single available SEM specimen has maintained its shape nicely, and only have moderately collapsed sternal plates. Spines in the lateral series insert in notches, but otherwise, the posterior segment margins show no deep notches. Acicular spines present in middorsal positions on segments 1 to 9 and 11 (Fig. 14a), and in lateroventral positions of segments 2 to 9 (Fig. 14b–d); terminal segment with midlateral, lateral terminal, and midterminal spines. Cuspidate spines present in lateroventral positions on segments 2 and 5, in lateral accessory positions on segment 8, and in ventrolateral positions on segment 9. Segment 10 with crenulated spines (putative sexually dimorphic male condition) in middorsal and midlateral positions. Middorsal spine of segment 11 extends well beyond terminal segment, and midlateral and lateral terminal spines of almost equal lengths, but with midlateral spines being much thicker than lateral terminal ones. Sensory spots could not be mapped completely, but sensory spots type 2 are at least present in paradorsal positions on segments 1 to 10, in laterodorsal positions on segment 1, in midlateral positions on segment 2, in sublateral positions on segments 4, 7, and 9, in lateroventral positions on segment 10, and in ventrolateral positions on segments 1, 3 to 4, 6 and 8. Sensory spots type 3 present on terminal segment in paradorsal, subdorsal and ventrolateral positions. Cuticular hairs formed by very minute scales, arranged in well-spaced and distinct longitudinal rows on tergal and sternal plates from segment 2 to 10 (Fig. 14a–b, d); segment 1 with a few thin acicular hairs, and segment 11 with scattered scale-like hairs on sternal plates only.

Notes on diagnostic features in Antygomonas sp.

Even though the recorded specimen shares its spine formula with five other species, it also shows some uncommon traits, and even its generic assignment was not unambiguous (species with identical spine patterns include Antygomonas caeciliae, A. paulae, A. gwenae, Semnoderes lusca sp. nov., S. pacificus; species with similar spine patterns will be addressed further in the general Discussion). The middorsal and midventral incisions in the anterior margin of segment 1 suggest an assignment to either Antygomonas, Semnoderes or Sphenoderes. Semnoderes can be excluded though, since the incisions are broad and not wedge-shaped. Instead, segment 1 shows much closer resemblance to the condition in species of Sphenoderes, but the placids in the neck region are not as differentiated as in species of Sphenoderes, but appear much more like the placids in species of Antygomonas. The typical Antygomonas species, i.e., A. incomitata, A. oreas, A. paulae and A. caeciliae all show middorsal and midventral incisions in the anterior margin of segment 1, but these are broadly concave (Nebelsick 1990; Bauer-Nebelsick 1996; Sørensen 2007; Dal Zotto 2015), and quite different from the much deeper incisions present in the recorded species. However, the condition in the recorded species shows close resemblance to another atypical species of Antygomonas, A. gwenae (see above and Herranz et al. 2014), hence, with some hesitation, this specimen is assigned to Antygomonas. A. gwenae and the recorded specimen also share the same spine formula, but this specimen is not considered conspecific with A. gwenae. First of all, the general appearance of the trunk segments differs between the two species. A. gwenae has a fairly thick cuticle, resembling the cuticle in, e.g., species of Centroderes or Campyloderes, which prevents the tegumental plates from collapsing during preparation. Oppositely, the cuticle in Antygomonas sp. is much thinner, collapses easily, and resembles the cuticle of typical Semnoderes and Antygomonas species. A character like this is obviously hard to quantify, but the difference in general trunk appearance is distinct. Antygomonas sp. also shows the rather long free flaps that are typical for most other species of Antygomonas, except A. gwenae.

The morphology and arrangement of cuticular hairs are atypical in Antygomonas sp. Most other congeners, inclusive A. caeciliae, A. gwenae, A. incomitata and A. paulae have leaf-like hairs that are scattered over the segments (Nebelsick 1990; Sørensen 2007; Sørensen et al. 2009; Herranz et al. 2014; Dal Zotto 2015), whereas Antygomonas sp. has minute scale-like hairs that are arranged in very distinct longitudinal lines, from segment 2 to 10. This character trait could be shared with one congener though, A. oreas. A similar hair-arrangement is shown in the line-art in the original description of the species (Bauer-Nebelsick 1996), and confirmed in the SEM images as well (Figs. 21–23 in Bauer-Nebelsick 1996). It furthermore resembles the arrangement in S. pacificus (Fig. 12c). Otherwise, this particular hair pattern is mostly known from some species of Zelinkaderes, i.e., Z. klepali, Z. brightae and Z. yong (Bauer-Nebelsick 1995; Sørensen et al. 2007; Altenburger et al. 2015), and probably also Z. submersus (see Higgins 1990), and to a lesser degree in Z. floridensis (see Higgins 1990).

The distribution of sensory spots differ between Antygomonas sp. and A. gwenae, at least on segment 7 where A. gwenae has ventrolateral sensory spots, missing in Antygomonas sp., on segment 10 where Antygomonas sp. has lateroventral sensory spots, missing in A. gwenae. Finally, even though the spine formulas are congruent for the two species, the thickness and dimensions differ. Whereas A. gwenae has rather short and stout spines, the spines in Antygomonas sp. are proportionally much longer, thinner and needle-like. In addition, a characteristic trait for A. gwenae is the rather short middorsal spine of segment 11 that hardly projects beyond the terminal segment. In contrast, Antygomonas sp. has a much longer middorsal spine on the terminal segment that projects well beyond its segment.

Antygomonas sp. likely represents a new species. Due to the very limited material, it is too premature to describe it here, but these diagnostic notes will make it possible to identify the species if more specimens are found in future studies.

Discussion

The extensive sampling along the shelf rim of the northern GoM has offered insights in the morphology and systematics of some of the rarer kinorhynch genera, Antygomonas, Semnoderes and Sphenoderes. Two issues of major interest are the stereotypical spine patterns that exist across genus boundaries, and the apparent need for more precise genus diagnoses with inclusion of new characters for the examined genera. These topics will be addressed in the following.

Stereotypical spine patterns within Kentrorhagata

A great part of the cyclorhagid taxonomy is based on differences in spine patterns, and especially among echinoderids, spine distribution appears to be a good character to distinguish species. However, within Kentrorhagata, a certain spine pattern seems to exist, even across genera.

The presence of middorsal acicular spines on all segments, lateroventral acicular spines on segments 2 to 9 (spines always small on segment 2), and cuspidate spines on segments 2, 5, 8 and 9, with the cuspidate spines being more lateral than the acicular on segments 2 and 8, and more ventral on segments 5 and 9, is shared between no less than six species from two different genera (referred to as the ‘2–5–8–9 pattern’): Antygomonas caeciliae, A. paulae, A. gwenae, Antygomonas sp. from station 154–2011, Semnoderes lusca sp. nov., and S. pacificus (Higgins 1967; Sørensen 2007; Herranz et al. 2014; Dal Zotto 2015; present contribution). In addition, there is one, perhaps two, yet undescribed species of Antygomonas around the Iberian Peninsula that show the same spine pattern (M. Herranz pers. comm.). Furthermore, a very similar spine pattern is found in several other species. For instance, and almost identical spine pattern is found in A. oreas, where the only difference is the positions of the lateral cuspidate and acicular spines on segment 9 that have switched position so the cuspidate ones become most lateral (Bauer-Nebelsick 1996). In other species, the same pattern is found, with just one pair, e.g., Antygomonas incomitata, Semnoderes armiger, Triodontoderes anulap (Nebelsick 1990; Sørensen and Rho 2009; Sørensen et al. 2009), or two pairs of cuspidate spines added, e.g., Semnoderes ponticus (Băcescu and Băcescu 1956). Species of Sphenoderes apparently never form lateral spines on segment 2, so with the exception of this segment, the same spine pattern is also found in Sphenoderes indicus (see Higgins 1969). Traces of this spine pattern are present in Zelinkaderes. Species of Zelinkaderes typically have less acicular spines, compared to other groups of Kentrorhagata, but focusing on cuspidate spines exclusively, this stereotypical ‘2–5–8–9 pattern’ is also present in Z. klepali and Z. yong (Bauer-Nebelsick 1995; Altenburger et al. 2015). In Z. yong the cuspidate spines on segments 2 and 8 are more lateral, whereas those on 5 and 9 are more ventral, which perfectly fits the ‘2–5–8–9 pattern’.

The existence of such a stereotypical spine pattern across several genera obviously leads to speculation about the phylogenetic significance of such character. The phylogenetic analyses of Sørensen et al. (2015) suggest a clade consisting of the genera Condyloderes, Centroderes, Wollunquaderes, Tubulideres, Cateria, Antygomonas, Semnoderes, Sphenoderes, Triodontoderes and Zelinkaderes (= Kentrorhagata). The analyses were unable to clarify the relationships within this clade, but one may speculate if the ‘2–5–8–9 pattern’ could be a basal trait, and hence synapomorphic, for at least some of these genera, and that further modifications, i.e., acquisition or loss of additional pairs of cuspidate spines, happened later in evolution. If this assumption is correct, this could suggest that at least Antygomonas, Semnoderes, Sphenoderes, Triodontoderes and Zelinkaderes might form a clade, since they all show traces of the ‘2–5–8–9 pattern’. Centroderes and Condyloderes would not fit into this clade, since species of Centroderes do not have cuspidate spines (see, e.g., Neuhaus et al. 2013, 2014), and the distribution of cuspidate spines in Condyloderes does not show any particular similarity to the ‘2–5–8–9 pattern’. It is also unlikely that Cateria would fit into this clade with Antygomonas and allies, and as discussed by Dal Zotto et al. (2013) and Sørensen et al. (2015), Cateria may not even belong to Kentrorhagata. The positions of Tubulideres and Wollunquaderes are rather uncertain. Wollunquaderes have cuspidate spines on segments 2, 5 and 8 though, which could point them towards the ‘2–5–8-9 pattern’ clade.

For now, this is speculation, and phylogenetic analyses with improved molecular data are required to solve the relationships within Kentrorhagata. However, the phylogenetic studies of Yamasaki et al. (2013) and Dal Zotto et al. (2013) actually found some evidence for a clade with species displaying the ‘2–5–8–9 pattern’. Yamasaki et al. (2013) recognized a clade consisting of Antygomonas, Sphenoderes, and Zelinkaderes (representatives of Semnoderes and Triodontoderes were not included in the analyses), whereas Dal Zotto (2013) recognized a similar clade with Semnoderes included as well (representatives of Triodontoderes were not included in the analyses).

Distinguishing species of Antygomonas, Semnoderes and Sphenoderes

As mentioned above, cyclorhagid taxonomy has to a great extend been based on the presence of spines and tubes. However, the finding of different species, even across genera, with identical spine patterns, stresses the need to explore other characters that potentially can be used in species diagnoses. One potential character could be the distribution of sensory spots. Sensory spots have previously been used to distinguish the otherwise nearly identical species Centroderes readae and C. drakei (see Neuhaus et al. 2014). During the present study, sensory spots also proved useful in the comparison of specimens, but the character should be used with a word of caution. First of all, sensory spots may be hard to visualize, and especially midlateral sensory spots may be impossible to observe with LM in a perfectly dorso-ventrally orientated specimen. Furthermore, several studies have shown intraspecific variation of sensory spot distributions, or specimens with occasional losses of single sensory spots, resulting in an asymmetrical distribution along the body axis. For instance, all four species of Centroderes described by Neuhaus et al. (2014) showed to some degree intraspecific variations in the occurrence of sensory spots. Neuhaus and Kegel (2015) also pointed out variations in sensory spot distribution between specimens of Cateria gerlachi, and Sørensen et al. (2009) reported a single specimen of Semnoderes armiger with an extra set of sensory spots on segment 3. The authors feel, though, that sensory spots can be used as diagnostic characters at the species level, but they should preferably be used in combination with other diagnostic characters, and if possible, only with a sufficient amount of specimens that could reveal eventual intraspecific variation.

Spine dimensions may also prove useful to distinguish species, especially the relative differences in lengths of lateral spines of the terminal segment that have been used to distinguish species of Centroderes (Neuhaus et al. 2014). In the holotype of Sphenoderes poseidon the sublateral terminal spines are twice as long as the lateral terminal spines (Sørensen et al. 2010), whereas the nearly opposite condition is found in in S. indicus in which the lateral terminal spines are nearly twice the lengths of the sublateral terminal spines (Higgins 1969). In S. aspidochelone nov. sp., the laterodorsal spines of segment 11 are nearly the same length, or up to 50% longer than the lateral terminal spines. Among species of Semnoderes, the relative difference seems to be less conspicuous though, and the midlateral or lateral accessory terminal spines are typically about 50–70% longer than the lateral terminal spines (Higgins 1967; Sørensen et al. 2009; present study). Alternately, as discussed above in the description of S. lusca nov. sp., the relative lengths between the lateral terminal and midterminal spines could be used to distinguish species. Another potentially useful character is the relative dimensions of other spines. For instance, the two undescribed species of Antygomonas from the Iberian Peninsula, mentioned in the previous section, seem to fall into two groups that can be distinguished by lengths of the middorsal spines (M. Herranz pers. comm.). Spine metrics can be used in species diagnoses, but again, the character should be used with caution. When comparing relatively few specimens, some differences may appear to be very distinct, but a more extensive sampling with numerous specimens, may extend the size ranges and eventually lead to overlapping ranges for putatively different species.

Other potential characters that should be considered in the future includes the pattern and type of cuticular hairs segment by segment, development of spines (conspicuously thin versus conspicuously thick spines), and sexual dimorphism such as presence of ventral papillae in females and dimorphism expressed in spines on segment 10.

Distinguishing the genera Antygomonas, Semnoderes and Sphenoderes

The special morphology of segment 1 has traditionally made it very easy to distinguish the genera Antygomonas, Semnoderes and Sphenoderes from other kinorhynchs, and from each other. Species of Antygomonas were characterized by a segment 1 consisting of a closed ring with broadly concave anterior margins on the dorsal and ventral side (Nebelsick 1990). This morphology is very distinct in most species of the genus, including A. incomitata, A. oreas, A. paulae and A. caeciliae (Nebelsick 1990; Bauer-Nebelsick 1996; Sørensen 2007; Dal Zotto 2015). Segment 1 in Semnoderes also consists of a closed ring with dorsal and ventral indentations in the anterior margin, but among these species, the indentations would form deep, wedge-shaped cuts (Zelinka 1928; Băcescu and Băcescu, 1956; Higgins 1967; Sørensen et al. 2009). The genus Sphenoderes was for many years represented by only a single species, S. indicus, and according to the original description the genus, was defined by segment 1 being composed of small middorsal and midventral plates, and two larger bilateral plates (Higgins 1969). These characters initially made it very easy to distinguish the three genera, but more recent discoveries have blurred this picture, and today, examples of species showing intermediate versions of segment 1 are known.

The first problem appeared with the description of the second Sphenoderes species, S. poseidon (see Sørensen et al. 2010). The species showed a morphology that was very close to the one of S. indicus, but segment 1 obviously consisted of a single, closed ring, and not lateral, dorsal and ventral plates as stated in the original genus diagnosis (Higgins 1969). Only a few years later, Herranz et al. (2014) described A. gwenae. The morphology of the species corresponded in different ways with other species of Antygomonas, but the morphology of the key character to the genus, namely the shape of the anterior margin of segment 1 differed. Instead of showing broadly concave dorsal and ventral incisions in segment 1, it showed much deeper incisions that in shape resembled the condition in Sphenoderes, or at least an intermediate condition between the two genera. Herranz et al. (2014) chose with some hesitation to assign the species to Antygomonas, but stressed that its generic assignment was controversial.

In the present contribution the same problems are repeated. Sphenoderes aspidochelone nov. sp. shows obvious similarities with its two putative congeners, but segment 1 is formed by a closed ring, which distinguishes it from S. indicus and hence the original species diagnosis. This leaves the question of whether the original diagnosis for Sphenoderes should be followed (i.e., include only species with segment 1 composed of four plates) and hence have S. poseidon and S. aspidochelone nov. sp. treated as a separate genus, or if the differences on segment composition should be ignored and the three species should remain in the same genus. Furthermore, the questionable generic assignment of A. gwenae became relevant again with the discovery of a second species, here reported as Antygomonas sp., that showed clear Antygomonas affinities, but also an anterior margin of segment 1 with much deeper incisions than those in the typical Antygomonas species. These questions prompted a consideration of various other characters that could be useful to distinguish these three genera.

One potentially distinguishing character is the thickness of the general body cuticle. Exact measures of body cuticle require TEM sectioning, which is not feasible in standard taxonomic studies, but when examining species of the three genera, it is obvious that the thickness of the cuticle differs. Species of Semnoderes and Antygomonas (except A. gwenae) have a very thin cuticle that easily collapses and can make the sternal plates fold inward. Oppositely, species of Sphenoderes and A. gwenae have a much more rigid cuticle that enables the animal to maintain its trunk shape, as is typically seen in species of Echinoderidae and Campyloderidae. It is extremely difficult to propose a strict and unambiguous definition for a character like this, but the trait is quite distinct when observing the animals, which makes it easy to distinguish putative species of Sphenoderes from Semnoderes and Antygomonas. A second character that appears to be linked to the cuticular thickness, is the morphology of the free flaps that extend from the posterior segment margins. Species of Semnoderes and Antygomonas (excluding A. gwenae) always have rather long and floppy free flaps, with deep notches, whereas Sphenoderes and A. gwenae have more rigid free flaps without notches, except anterior to spine insertions. These characters are useful to get a hint about a species’ generic assignment.

Placids of the neck region could also provide important information. The shape of the placids is obviously tightly linked to the appearance of the neck opening, and hence the shape of the anterior margin of segment 1. In species of Antygomonas, the placids are relatively undifferentiated, and the midventral placid would be slightly broader than the others (Nebelsick 1990; Bauer-Nebelsick 1996; Sørensen 2007). Oppositely, species of Semnoderes have strongly modified placids, to fit the shape of the deep, wedge-shaped incisions in segment 1. Especially the middorsal and midventral placids are very narrow in order to fit into the wedge-shape (Sørensen et al. 2009; Fig. 9e). The placids of Sphenoderes resemble to some extent those in Semnoderes, but since the deep midventral incision in the anterior margin of segment 1 is quite broad, opposed to wedge-shaped, the midventral placid becomes much broader at its base, and gets a conspicuously triangular or trapezoid appearance. The placids of A. gwenae are somewhat in between the condition among other species of Antygomonas and those of Sphenoderes. Its placids are clearly less differentiated than those of Sphenoderes, but still they appear more triangular than those of, e.g., A. paulae (see Sørensen 2007). Nebelsick (1990) pictures the placids of A. incomitata as quite triangular as well, but more detailed SEM of the species shows that the placids of this species are more rectangular than triangular (Sørensen et al. 2009). The placids of the undescribed species, herein reported as Antygomonas sp., are very close in morphology to those of A. gwenae. Hence, morphology of placids also helps to distinguish Antygomonas, Semnoderes and Sphenoderes as three distinct clades, with A. gwenae and Antygomonas sp. in a somewhat intermediate position between Antygomonas and Sphenoderes.

The morphology of the cuspidate spines shows some interesting trends. Species of Semnoderes and Antygomonas (including Antygomonas sp. and to a smaller extent A. gwenae) typically have very thick and well-developed cuspidate spines, that would nearly reach the posterior margin of the following segment, and be as thick or thicker than the acicular spines of the same segment. On the opposite, species of Sphenoderes tend to have rather reduced cuspidate spines. Higgins (1969) pictures the cuspidate spines in S. indicus as quite minute, and they are about the same size in S. poseidon (see Sørensen et al. 2010). In S. aspidochelone, the cuspidate spines are even smaller, and so reduced that it was difficult to identify them as cuspidate. The size reduction of cuspidate spines could be a character that distinguishes species of Sphenoderes from those of other genera.

The development of the acicular spines shows interesting trends. Semnoderes and Antygomonas (including Antygomonas sp., but not A. gwenae) have rather thin and slender acicular spines (Nebelsick 1990; Bauer-Nebelsick 1996; Sørensen 2007; Sørensen et al. 2009; Dal Zotto 2015; present study) whereas the spines of Sphenoderes and A. gwenae are much shorter and stouter (Higgins 1969; Sørensen et al. 2010; Herranz et al. 2014; present study), which make them resemble the middorsal spines in species of Centroderes (see, e.g., Neuhaus et al. 2013, 2014). Again, although the morphology may be difficult to quantify precisely, the difference in appearance is quite striking.

A final character with regard to spines is the apparent lack of lateroventral spines of segment 2 in species of Sphenoderes. All other species that have been discussed in this section show a set of lateroventral cuspidate spines, together with a set of strongly reduced acicular spines on segment 2. The ability to form lateroventral spines on segment 2 has apparently been lost in species of Sphenoderes and this may in fact be the best and most unambiguous character that distinguishes the genus from Antygomonas and Semnoderes. Interestingly, it also distinguishes species of Sphenoderes from A. gwenae, which is important to note, since A. gwenae otherwise share more traits with Sphenoderes than with other species of Antygomonas.

Recognition of families and genera

Species of Antygomonas, Sphenoderes and Semnoderes are all characterized by a modified segment 1 that shows some degree of indentation in the segments’ anterior margin. No other kinorhynchs show this kind of morphology in segment 1, which leads us to speculate if Antygomonidae and Semnoderidae also in the future should be treated as two different families. Comprehensive phylogenetic analyses based on molecular evidence have until now failed to provide unambiguous support for a clade uniting the three genera (Dal Zotto et al. 2013; Yamasaki et al. 2013; Sørensen et al. 2015), but analysis of morphological data only actually suggests monophyletic Antygomonidae + Semnoderidae (Sørensen et al. 2015). The discovery of A. gwenae and Antygomonas sp. (Herranz et al. 2014 and present contribution) only reinforce the bands between the two families, since the shape of the neck openings in these species represents an intermediate stage between the conditions in other species of Antygomonas and in species of Sphenoderes. It is too premature to merge the two families, but future studies should consider the option. Obviously, their relationship should be tested in phylogenetic analyses with improved molecular sampling for the kentrorhagid species, but also morphology, and in particular muscular arrangements and functional morphology in the neck and segment 1 of Antygomonas, Sphenoderes and Semnoderes should be taken into account when evaluating this question.

At the generic level, the morphology of segment 1 is the key to distinguishing the three genera. Species of Antygomonas have broadly concave anterior incisions of segment 1, Sphenoderes has deep truncate incisions, and Semnoderes has deep and broad incisions (Higgins 1969, 1990; Nebelsick 1990; Sørensen and Pardos 2008; Sørensen et al. 2009; Neuhaus 2013). Other characters that have been mentioned in the diagnoses of the three genera, e.g., spindle-shaped trunk, 14 trichoscalids, 16 placids, cuspidate spines and long midterminal spine are common traits among kentrorhagid kinorhynchs (see, e.g., Sørensen et al. 2015) and not useful in genus diagnoses. However, as discussed above, the present study has revealed new character combinations that could prove useful in future genus recognition, and the characters are summarized in Table 7. The table suggests that Sphenoderes is the most easily recognized genus, based on the combination of deep and broad incisions in segment 1, triangular to trapezoid midventral placid, a relatively thick cuticle, stout acicular spines, reduced cuspidate spines and the absence of lateroventral spines on segment 2. However, only the latter character is unique among species of Semnoderidae and Antygomonidae. Semnoderes is also easily recognized by its distinct neck morphology and wedge-shaped incisions in segment 1. This leaves us with Antygomonas as the last, but also the most poorly defined genus. Except for A. gwenae and Antygomonas sp., Antygomonas would be distinguished by its segment 1 morphology. Besides this, some species of Antygomonas sensu stricto share several characters with Semnoderes including a thin cuticle, very well-developed cuspidate spines and thin, needle-shaped acicular spines.
Table 7

Selected characters in species of Antygomonas, Sphenoderes and Semnoderes. The character coding is based on the species’ original descriptions, information from Sørensen et al. (2009) and the present contribution. Parantheses around character traits mark that the trait is less conspicuous or slightly obscure in this species

Character Species

Segment 1 composition

Segment 1 incision

Cuticle thickness

Midventral placid

Cuspidate spines

Acicular spines

Segment 2 LV spines

A. gwenae

Ring

Broad

Thick

(Triangular)

(Long-thick)

Stout

Present

A. caeciliae

Ring

Concave

Thin

Rectangular

Long-thick

Needles

Present

A. incomitata

Ring

Concave

Thin

Rectangular

Long-thick

Needles

Present

A. oreas

Ring

Concave

Thin

Rectangular

Long-thick

Needles

Present

A. paulae

Ring

Concave

Thin

Rectangular

Long-thick

Needles

Present

Antygomonas sp

Ring

Broad

Thin

(Triangular)

Long-thick

Needles

Present

Se. armiger

Ring

Wedge

Thin

Wedge

Long-thick

Needles

Present

Se. lusca sp. nov.

Ring

Wedge

Thin

Wedge

Long-thick

Needles

Present

Se. pacificus

Ring

Wedge

Thin

Wedge

Long-thick

Needles

Present

Se. ponticus

Ring

Wedge

Thin

Wedge

Long-thick

Needles

Present

Sp. aspidochelone sp. nov.

Ring

Broad

Thick

Triangular

Reduced

Stout

Absent

Sp. indicus

4 Plates

Broad

Thick

Triangular

Reduced

Stout

Absent

Sp. pacificus

Ring

Broad

Thick

Triangular

Reduced

Stout

Absent

The two latter species, A. gwenae and Antygomonas sp., do not fit unambiguously into any of the genera. The morphology of segment 1 is closer to (but not identical with) the condition in Sphenoderes, and the stout acicular spines and thick cuticle also points A. gwenae in this direction. However, due to their presence of lateroventral spines on segment 2, the two species would not fit into Sphenoderes. This leaves A. gwenae and Antygomonas sp. somewhere between Antygomonas, Semnoderes and Sphenoderes. When describing A. gwenae, Herranz et al. (2014) mentioned that its assignment to Antygomonas is problematic, and considered the species generic assignment as provisional. Our data from the present study supports this view, and the authors foresee that A. gwenae in the future should be assigned to a new genus, eventually accompanied with Antygomonas sp. Before taking this step, though, it would be preferable to find an additional closely related species and more specimens of Antygomonas sp.

Conclusions

The description of Sphenoderes aspidochelone sp. nov. and Semnoderes lusca sp. nov., and the finding of Antygomonas cf. gwenae, increases the potential number of named kinorhynch species in the GoM to 15. Reexamination of A. gwenae and another yet undescribed species, herein referred to as Antygomonas sp., furthermore suggested that these two species could represent intermediate forms between other Antygomonas and Sphenoderes, which would bring the two genera even closer together and question whether Antygomonidae in the future should be treated as a separate family, or whether the genus Antygomonas should be included in Semnoderidae. The results also questioned the generic assignment of A. gwenae, and indicated that the species more likely should be treated as a separate lineage within Semnoderidae. Comparison of character traits within the three genera demonstrated that within Semnoderidae, the lack of lateroventral spines on segment 2 and a general reduction of cuspidate spines are unique for Sphenoderes, and together with the deep truncate incisions in segment 1, this should be treated as an important part of the genus diagnosis. Until the taxonomy of A. gwenae has been solved, it is very difficult to point out clear diagnostic characters for Antygomonas, but with A. gwenae excluded, the genus would be recognized by its broadly concave incisions in segment 1. Semnoderes can be recognized by its deep wedge-shaped incisions in segment 1, but otherwise, the genus shares many character traits with most species of Antygomonas, such as well-developed cuspidate spines, needle-shaped acicular spines and a thin cuticle.

Notes

Acknowledgements

This research was made possible by a grant from The Gulf of Mexico Research Initiative. Data are publically available through the Gulf of Mexico Research Initiative Information & Data Cooperative (GRIIDC) at https://data.gulfresearchinitiative.org (doi:  10.7266/N74J0C32,  10.7266/N7SB43S2 and  10.7266/N7W66HTS). The authors thank the staff and students of Troy University for help with sediment collection and laboratory work. In addition, our thanks go to the researchers at the NMFS/NOAA Pascagoula lab for their help with sediment collection, to Dr. Steve Ramroop (TU) for providing Fig. 1, to Jon Norenburg, Kathryn Ahlfeld and Courtney Wickel, Smithsonian Institution, for arranging the loan of Antygomonas gwenae and Semnoderes pacificus type material, to Melissa Rohal, Harte Research Institute, Texas A&M University Corpus Christi, for donating her specimen of Sphenoderes aspidochelone from the southern GoM, and to Maria Herranz for providing information about the undescribed Spanish species of Antygomonas. The second author also thanks Troy University for funding through the faculty development committee.

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Copyright information

© Senckenberg Gesellschaft für Naturforschung and Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Section for GeoGenetics, Natural History Museum of DenmarkUniversity of CopenhagenCopenhagenDenmark
  2. 2.Department of Biological and Environmental Sciences, 210A MSCXTroy UniversityTroyUSA

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