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New genus and two new species of the family

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DOI: 10.11646/zootaxa.3692.1.4

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 Zootaxa 3692 (1): 007–027 ISSN 1175-5326 (print edition)
www.mapress.com / zootaxa /
Copyright © 2013 Magnolia Press
Article ZOOTAXA
ISSN 1175-5334 (online edition)
http://dx.doi.org/10.11646/zootaxa.3692.1.4
http://zoobank.org/urn:lsid:zoobank.org:pub:F9EC43F2-F82E-4E8C-A735-ECA4DFF7CA00

New genus and two new species of the family Ethmolaimidae (Nematoda:
Chromadorida), found in two different cold-seep environments

BEZERRA TANIA NARA1*, PAPE ELLEN1, HAUQUIER FREIJA1, VANREUSEL ANN1 & INGELS
JEROEN1,2
1
Ghent University, Department of Biology, Marine Biology Section, Krijgslaan 281/S8, 9000 Ghent, Belgium
2
Plymouth Marine Laboratory, Prospect Place, The Hoe, Plymouth, PL1 3DH, United Kingdom
*
Corresponding author. E-mail: tania.campinasbezerra@ugent.be

Abstract

This study describes a new genus Dystomanema gen. nov. with two new species, D. cadizensis sp. nov. and D. brandtae
sp. nov. within the family Ethmolaimidae, subfamily Neotonchinae, based on specimens from two low-activity cold-seep
environments at distant geographical locations. The new genus was first identified in samples from the Darwin mud vol-
cano (1100 m depth) in the Gulf of Cádiz and later on also found in samples from a low-activity seep in the Larsen B
embayment (820m depth) off the eastern Antarctic Peninsula. Until now, the family Ethmolaimidae contained nine genera:
Ethmolaimus and Paraethmolaimus in the subfamily Ethmolaiminae, and Comesa, Filitonchoides, Filitonchus,
Gomphionchus, Gomphionema, Nannolaimus, and Neothonchus in the subfamily Neotonchinae. The most important fam-
ily characteristics are: an annulated cuticle bearing transverse rows of dots, cephalic sensilla arrangement of 6+6+4, a spi-
ral amphid, an oesophagus with muscular posterior bulb, paired gonads and males with cup-shaped precloacal
supplements. The new genus resembles Comesa and Neotonchus, but is typified by a ventrally displaced oral opening with
three very small teeth that are easily overlooked. D. cadizensis gen. nov. sp. nov. is characterized by the 1401–2123 µm
long body; cuticle transversally striated with fine punctation; head conical; low lips; amphid spiralled 3 turns, oral opening
ventrally displaced, male with outstretched testes; spicules of equal size; gubernaculum plate-like and ten to twelve con-
spicuous cup-shaped precloacal supplements with external longitudinal articulated flange. D. brandtae gen. nov. sp. nov.
can be distinguished by the 2438–3280 µm long body; cuticle transversally striated with fine punctuation; head conical;
low lips; amphid spiraled 3+ turns; oral opening ventrally displaced; male with anterior testes outstretched and posterior
one smaller and reflexed; spicules of equal size; gubernaculum plate-like and twenty conspicuous cup-shaped precloacal
supplements with external longitudinal articulated flange. Notes on the ecology and habitat of the new genus are provided
in light of its discovery in cold-seep environments.

Key words: Antarctic, Larsen, Southern Ocean, Gulf of Cádiz, Northeast Atlantic, Dystomanema gen. nov., Dystomane-
ma cadizensis gen. nov. sp. nov., Dystomanema brandtae gen. nov. sp. nov., cold seep

Introduction

The nematode family Ethmolaimidae has two subfamilies: (1) Ethmolaiminae Filipjev & Stekhoven, 1941,
containing the two genera Ethmolaimus de Man, 1880 (syn. Trichethmolaimus, Jensen 1994) and Paraethmolaimus
Jensen, 1994, and (2) Neotonchinae Wieser & Hopper, 1966, which, until now, contained seven genera: Comesa
Gerlach, 1956 Filitonchoides Jensen, 1985, Filitonchus Platt, 1982, Gomphionchus Platt, 1982, Gomphionema
Wieser & Hopper, 1966, Nannolaimus Cobb, 1920, and Neothonchus Cobb, 1933. The genus Ethmodora Khera,
1975 is here not considered as a valid one.
Dystomanema gen. nov. was found at the Darwin mud volcano, Gulf of Cádiz in the Northeast Atlantic at 1100
m water depth and at a low-activity cold seep in the Larsen B area, Weddell Sea at 820 m water depth. Both
locations are comparable in that they show the presence (Darwin mud volcano) or remnant signs (Larsen B) of
cold-seep activity. Cold seeps are ecosystems that derive their primary metabolic energy from chemical processes
instead of depending on settling phytodetrital matter from euphotic waters (Van Dover et al. 2002, Domack et al.

Accepted by M. Schueller: 24 Apr. 2013; published: 25 Jul. 2013 7

2005; Van Gaever et al. 2009). These remarkable habitats are inhabited by typical meiofauna (Vanreusel et al.
2009) whereby nematodes are generally the predominant metazoan taxon (Van Gaever et al. 2006). Diversity is
usually quite low in these habitats, which has been attributed to the toxic conditions, created by high sulphide and
low oxygen levels (Levin 2005). Mud volcanoes are geologically driven by fluid flow, characterized by a high
patchiness of food sources and biogeochemical and physical characteristics (Levin et al. 2003; Pape et al. 2011).
This patchiness is often reflected by the nematode communities in terms of differences in density, biomass and
composition (Pape et al. 2011). The Gulf of Cádiz is a tectonically active region and one of the largest cold-seep
areas on the European margins. In contrast, no cold seep ecosystem had been reported in the Antarctic until some
years ago, when Domack et al. (2005) discovered a possible methane seep in the area formerly covered by the
Larsen B ice shelf at the eastern Antarctic Peninsula (Hauquier et al. 2011). Later, re-investigation of the site
indicated the presence of a low-activity seep there (Niemann et al. 2009).
Ethmolaimidae species occur globally. In most ecological investigations, the family Ethmolaimidae represents
only a small proportion of the total nematode fauna, which can explain the lack of recent information on the family
(Platt, 1982). Whereas members of the subfamily Ethmolaiminae are mainly described from freshwater and
brackish environments, genera of the subfamily Neotonchinae are exclusively found in marine sediments,
particularly in fine sand, silt and mud with a relatively high organic content (Platt, 1982). Members of
Ethmolaimidae are regularly found in association with chemosynthetic ecosystems and in the thiobios, living in
deep sediment layers, where oxygen availability is generally low and sulphide concentration usually high (Jensen
1985, Shirayama and Ohta 1990, Zeppilli and Danovaro 2009). This paper gives an update on the taxonomical and
ecological information of the subfamily Neotonchinae, with notes on the relationships among its members. The
new genus is characterized by a wide geographical distribution, with each of two species located in geographically
distant areas. However, both new species occur at sites that show remnant signs of seep activity, implying they are
associated with chemosynthetic habitats.

Material and methods

Samples were collected at two sites, one in the Gulf of Cádiz and one at the eastern Antarctic Peninsula at the
Larsen B site. Both areas are characterized by present or remnant cold seep activity.
Gulf of Cádiz. The Gulf of Cádiz (34°–37°15’ N, 9°–6°45’ W) is situated west of the Strait of Gibraltar, at the
boundary between the European and African plates. Therefore, it is a tectonically active region. Moreover, it is one
of the largest cold-seep areas on the European margins with over 30 mud volcanoes (MV) between 200 and 4000 m
deep (Pinheiro et al. 2003, Somoza et al. 2003, Van Rensbergen et al. 2005). The MV studied here is the Darwin
MV, situated at 35°23.51’ N 7°11.48’W (Fig. 1A). At the time of sampling, its summit (at ~1100 m depth) was
covered with a large carbonate crust on top of which, mostly empty, Bathymodiolus mauritanicus shells were
accumulated (Genio et al. 2008). A small area of dark-colored sediment (± 100 cm²) was present which emitted gas
when disturbed. Around this ‘seep site’, small carbonate blocks and white sediments, indicating bacterial activity,
were present (Vanreusel et al. 2009).
The Darwin MV was sampled during the JC10 expedition in May 2007 onboard the RRS James Cook.
Sediment cores were collected with push cores (25.5 cm² surface area), using ROV Isis, along a 10 m transect at 0,
2, 5 and 10 m from the active ‘seep site’ (Fig. 1B). Replicate sampling was not possible due to high heterogeneity
of the habitat and the small size of the ‘seep site’. At each sampling location, one push core was sliced into 1 cm-
layers until 10 cm depth and fixed in 4% formalin for meiofauna and nematode analysis. Next to these 4 locations
nearby the active ‘seep site’, 2 additional sites were sampled at ~100 m and ~1100 m from the seep site with a
megacorer (MC; 75.4 cm² surface area). According to Pape et al. (2011), the new genus was subdominant (8 % of
total nematode abundance) at the seep site and at 2 m away from the seep site. However, the genus was also
observed (but less frequently) in cores taken further away from the seep site.
Larsen B seep area. The second area of interest for this study is the Larsen B area at the eastern Antarctic
Peninsula, where a large part of the previously permanent ice shelf calved off in 2002. After this ice-shelf collapse,
indications of cold seep activity were observed in 2005 during a first videographic survey of the region (Domack et
al. 2005) at a particular site within the Larsen B embayment (hereafter referred to as Larsen B Seep). However,
during another visit in 2007, it was shown that seep activity strongly diminished over time (Niemann et al. 2009).

8 · Zootaxa 3692 (1) © 2013 Magnolia Press BEZERRA ET AL.

FIGURE 1. (A) Bathymetric map of the Darwin MV with the core locations on the MV indicated (adapted from Vanneste et al.
2011) (B) Schematic representation of the sampling strategy. PUC: push core, sampled for pore-water geochemistry and
meiofaunal community analyses; MC: megacorer, sampled for meiofaunal community analyses (Pape et al. 2011).

The Larsen B Seep site (65°26.07’–65°26.10’S; 61°26.48’–61°26.53’W; Fig.2) is located centrally in the
Larsen B embayment at a depth of ~820m, in a trough formed by two glaciers (Domack et al. 2005; Niemann et al.
2009). Sediment cores were collected during the ANT-XXIII/8 expedition onboard RV Polarstern in 2007.
Undisturbed cores were retrieved with a multicorer (MUC) device with each core having a 25.5 cm² cross-sectional
surface area. Four replicated MUC deployments were analyzed based on the presence or absence of a clear
sulphidic layer in the 3rd–10th centimeter, corresponding with a grey-black color and hydrogen-sulphide smell (Raes
& Rose 2007). For each deployment, one core was sliced into different layers for meiofauna and nematode
analysis: the upper 5 cm were sliced per cm, followed by two slices of 5 cm (5–10 cm, 10–15 cm). All slices were
fixed separately in 4% buffered formalin. Within the Larsen B Seep replicates, the new genus of Ethmolaimidae

NEW GENUS AND TWO NEW SPECIES OF ETHMOLAIMIDAE Zootaxa 3692 (1) © 2013 Magnolia Press · 9
was only found in relative abundance higher than 1% in replicate 706/5, where it was the most abundant genus in
the 10–15 cm slice (71% of total nematode abundance in this slice). Occasionally, the genus was also present in
shallower layers and/or other replicates.
Nematodes were then mounted on glass slides and identified to genus level with a Leica DMLS compound
microscope (1000x magnification), using a pictorial key to nematode genera (Warwick et al. 1998) and the NeMys
database (Deprez et al. 2005); the latter and other primary literature was used to identify the relevant specimens to
species level. Species descriptions were made from glycerol slides using interferential contrast microscopy (Leica
DMLS); drawings were made with a camera lucida; images of the specimens were taken with a Leica DFC420
digital mounted camera and processed with Leica LAS 3.3 imaging software. All measurements are in µm and all
curved structures were measured along the arc. Type specimens have been deposited in Ghent University’s
Museum voor Dierkunde (UGMD), K.L. Ledeganckstraat 35, 9000 Ghent, Belgium.

FIGURE 2. (A) location of the Larsen B area (B) and the stations sampled during ANT-XXIII/8. For this study, only Larsen B
Seep is of interest, indicated with the red dot (map modified after Gutt 2008).

Abbreviations used:

a, b, c: ratios of de Man (1880)

a: body length divided by maximum body diameter;
b: body length divided by pharyngeal length;
c: body length divided by tail length;
c’: tail length divided by body width at level of anus or cloacal opening;
cbd: corresponding body diameter;
mbd: maximum body diameter

10 · Zootaxa 3692 (1) © 2013 Magnolia Press BEZERRA ET AL.

Observation on the measurements:

Sub-lateral setae: length of short dorso-sublateral subcephalic setae;

Amphid from ant. end: distance from the amphid to the anterior end, measured from the anterior edge of the
amphid;
Amphid % of cbd: amphid diameter as a percentage of the corresponding body diameter;
Excretore pore: position of secretory-excretory pore from the anterior end;
Excretore pore cbd: corresponding body diameter at secretory-excretory pore level;
Nerve ring: distance of the nerve ring from the anterior end;
Pharyngeal bulb: measurement of bulb diameter;
Spicule length: measured along the median line;
Spicule/abd: spicule length divided by the anal body diameter

Systematics

Class Chromadorea Inglis, 1983

Subclass Chromadoria Pearse, 1942

Order Chromadorida Chitwood, 1933

Suborder Chromadorina Filipjev, 1929

Superfamily Chromadoroidea Filipjev, 1917

Family Ethmolaimidae Filipjev & Schuurmans Stekhoven, 1941

Diagnosis. Chromadoroidea. Characterized by an annulated cuticle bearing transverse rows of fine punctation,
sometimes with lateral differentiation of fewer rows and rows of pores. Cephalic sensilla arranged in three circles
of 6+6+4. Sensilla of the anterior circlet papilliform and both outer circlets setiform. Amphideal fovea uni- or
multi-ventrally spiral. Buccal cavity with three equal teeth. Pharynx ending with a posterior muscular bulb of
which the degree of development is correlated with the size of the dorsal tooth. Males have paired spicules of equal
size and a slightly cuticularized rod-like gubernaculum. Conspicuous precloacal cup-shaped supplements with an
external articulated flange are present as well as a ventral precloacal spine. Ovaries are paired, opposed, reflexed
and of equal size; testes paired, laying on different sides of the intestine, the posterior one being smaller in most
species. In most genera, the tail is conical, usually with a rounded tip (Platt, 1982; Jensen, 1994; Decraemer &
Smol, 2006).

Subfamily Neotonchinae Wieser & Hopper, 1966

Diagnosis. Ethmolaimidae (originally Cyatholaimidae): buccal cavity elongate, depth greater than width; armed
with very small to medium or large dorsal tooth located midway in the buccal cavity and with or without small
subventral teeth. Cephalic sense organs 6+6+4. Pharynx with well-developed terminal bulb. Spicula of highly
characteristic shape, proximal two-thirds fairly straight and nearly uniform thickness, distal third narrowed,
cylindroid and with a slight S-shaped curvature. Precloacal supplements large, well-developed, cup-shaped. Tail
plump, conoid, with bluntly rounded terminus.
Marine. (Platt, 1982; Lorenzen 1994) (Type genus: Neotonchus Cobb, 1933)
Genera belonging to Neotonchinae: Comesa Gerlach, 1956, Dystomanema gen. nov., Filitonchoides Jensen,
1985, Filitonchus Platt, 1982, Gomphionchus Platt, 1982, Gomphionema Wieser & Hopper, 1966, Nannolaimus
Cobb, 1920, and Neothonchus Cobb, 1933. (Fig 3)

NEW GENUS AND TWO NEW SPECIES OF ETHMOLAIMIDAE Zootaxa 3692 (1) © 2013 Magnolia Press · 11
FIGURE 3. Genera of the family Ethmolaimidae. Adapted from Warwick et.al. (1998), Jensen (1985, 1994). Subfamily
Ethmolaiminae: A—Ethmolaimus, B—Paraethmolaimus; Subfamily Neotonchinae: C—Comesa, D— Dystomanema, E—
Filitonchoides, F—Filitonchus, G—Gomphionchus, H—Gomphionema, I—Nannolaimus, J—Neotonchus.

12 · Zootaxa 3692 (1) © 2013 Magnolia Press BEZERRA ET AL.

Genus Dystomanema Bezerra, Pape, Hauquier, Ingels & Vanreusel gen. nov.

Diagnosis. Neotonchinae. Body long, cylindrical, tapering anteriorly. Cuticle transversally striated with fine
punctation, more evident in the tail region. No lateral differentiation. Few somatic setae with no fixed distribution
pattern. Anterior sensilla arranged in three circles 6+6+4, first circle papilliform, outer circles setiform. Dorso-
sublateral setae just posterior to the third circle of sensilla at the level of the amphid. Spiral amphid smaller in
females than in males. Oral opening ventrally displaced. Buccal cavity wide, deep, funnel shaped. Gymnostom
followed by well-cuticularized pharyngostom with expanded conical posterior part. Three small teeth, one dorsal
tooth and two smaller subventral teeth, all situated in the pharyngostom. Pharynx cylindrical with a posterior
muscular bulb. Male reproductive system diorchic, spicules of equal size, one ventral precloacal spine and
conspicuous cup-shaped precloacal supplements. Female reproductive system didelphic, ovaries antidromously
reflexed. Tail conical.
Type species. Dystomanema cadizensis sp. nov.; present paper. One other species in genus: Dystomanema
brandtae sp. nov.; present paper
Differential diagnosis. Dystomanema gen. nov. resembles Comesa Gerlach, 1956 and Neothonchus Cobb,
1933 in terms of the body shape, cuticle pattern and shape of supplements, but differentiates from both in having
much smaller dorsal tooth.
In the subfamily Ethmolaiminae, Ethmolaimus de Man, 1880 (syn. Trichethmolaimus, Jensen 1994) and
Paraethmolaimus Jensen, 1994 has long mouth and massive teeth; in the subfamily Neotonchinae, Comesa
Gerlach, 1956 has a distinct dorsal tooth and ventral ridges; Gomphionema Wieser & Hopper, 1966 has a massive
dorsal tooth; Gomphionchus Platt, 1982 and Neothonchus Cobb, 1933 has a big dorsal tooth; Nannolaimus Cobb,
1920 has a small weakly cuticularized dorsal tooth while Filitonchoides Jensen, 1985 and Filitonchus Platt, 1982
has a poorly developed buccal cavity with no sign of a dorsal tooth. Comesa Gerlach, 1956 species with small teeth
also have a developed dorsal tooth. Dystomanema gen. nov. has no developed dorsal tooth but three small teeth
(one dorsal and two subventral) instead. These small teeth are bigger than the ridges mentioned for Comesa
Gerlach, 1956. Dystomanema gen. nov. might represent a transition between no teeth (Filitonchoides Jensen, 1985
and Filitonchus Platt, 1982) and small teeth (some Comesa Gerlach, 1956) to big teeth in this subfamily.
Differs from all genera of the family by the ventrally displaced oral opening (visible at low magnification).
Subterminal oral opening is observed in other nematoda genera, such as Campylaimus Cobb, 1920,
Diplopeltula Gerlach, 1950 and Morlaixia Vincx and Gourbault 1988. Just some Campylaimus (Cobb, 1920) and
Morlaixia Vincx and Gourbault 1988 (genus also found in cold-seeps by Guilini et al., 2012) have a subventrally
displaced oral opening. Diplopeltula Gerlach, 1950 has a dorsal oral opening. The ventral position of the oral
opening, in some Campylaimus, was not accepted by Vincx and Gourbault, 1988 when they described the genus
Morlaixia Vincx and Gourbault, 1988 but Villares et al. (2013) accept this ventral position and provide a key to
species identification.
Etymology. The genus is named after the particular mouth displacement, a characteristic that is unique in the
family.

Dystomanema cadizensis gen. nov. sp. nov.

(Figs 4 A–F, 5 A–H, 6 A–F; Table 1)

Material examined. Holotype male (Inventory No. UGMD 104262), three paratypes males (Inventory No.
UGMD 104263, 104264, 104265), three paratypes females (Inventory No. UGMD 104266, 104267, 104268).
Type habitat and locality. Cold-seep sediments in the Northeast Atlantic, Gulf of Cádiz, Darwin mud volcano
(35°23.51’ N 7°11.48’W).
Description. Males: Body slender, long, uniform in diameters tapering anteriorly and posteriorly. Fixation
shape uncoiled. Cuticle transversally striated with fine punctation more evident on the tail region. No lateral
differentiation. Few somatic setae with no fixed distribution pattern. Head conical, low lips. Inner labial sensilla
papilliform, six outer-labial short setiform sensilla, four cephalic setae 5 µm or 35% of corresponding body
diameter long. Short dorso-sublateral subcephalic setae present. Amphid spiral, ventrally to the centre, 3 turns.
Mouth opening ventrally displaced. Buccal cavity wide, deep (18 µm), funnel shaped. Gymnostom followed by

NEW GENUS AND TWO NEW SPECIES OF ETHMOLAIMIDAE Zootaxa 3692 (1) © 2013 Magnolia Press · 13
FIGURE 4. Dystomanema cadizensis gen. nov., sp. nov. (Holotype male). A: entire body; B: anterior end surface view; C:
anterior end median section; D: posterior end; E: female reproductive system; F: female tail (Scale bars: A, E = 50 µm; B, C, D,
F= 20 µm).

14 · Zootaxa 3692 (1) © 2013 Magnolia Press BEZERRA ET AL.

FIGURE 5. Dystomanema cadizensis gen. nov., sp. nov. Holotype Male. A: entire body; B–C: head; D: pharynx, detail ventral
gland; E: supplements, spicules, caudal glands; F: supplements, detail clear patch. Paratype Male. G: upper view of
supplements; H: clear patch (Scale bars: A= 200 µm; B, C, F, G, H= 20 µm; D, E= 50 µm).

well-cuticularized pharyngostom with expanded conical posterior part. Sclerotized walls of pharyngostom with
three small teeth: a dorsal tooth and two smaller subventral teeth. Pharynx cylindrical with a posterior muscular
bulb. Nerve ring located slightly anterior to middle of pharynx. Secretory excretory pore located immediately after
cephalic setae. Reproductive system with long vas deferens, clear patch of variable position from the level of the 4th
to the 8th supplement from the cloaca. Outstretched testes anteriorly directed, anterior one to the right of intestine
and posterior one, smaller, to the left. Spicules of equal size, about the same length as the cloacal diameter, slightly
cephalated, bent about 1/3 of the distance from the distal end. Gubernaculum plate-like with a sclerotized rod-like
internal structure at the distal half. Ten to twelve conspicuous cup-shaped precloacal supplements with external

NEW GENUS AND TWO NEW SPECIES OF ETHMOLAIMIDAE Zootaxa 3692 (1) © 2013 Magnolia Press · 15
longitudinal articulated flange. Distance between the supplements variable among the males. Prominent ventral
precloacal spine about 16 µm anterior to the cloacal opening. At the opening of the cloaca there is a slightly
sclerotized triangular structure, which seems to be a cuticular projection. Tail conical plump, with bluntly rounded
tip. Three caudal glands opening in a prominent, terminal blunt spinneret, half as wide as the tip of the tail.

FIGURE 6. Females of Dystomanema cadizensis gen. nov., sp. nov. A: entire body; B: head; C: anterior end, median section;
D: reproductive system, vulva; E: vulva and perivulvar glands; F: tail. (Scale bars: A= 200 µm; B, C, D= 50 µm; E, F= 20 µm).

16 · Zootaxa 3692 (1) © 2013 Magnolia Press BEZERRA ET AL.

NEW GENUS AND TWO NEW SPECIES OF ETHMOLAIMIDAE Zootaxa 3692 (1) © 2013 Magnolia Press · 17
 Females: Females are similar to males in most respects, in general longer. Amphids do not show dimorphism
in shape or number of turns but in females they occupy just 36% of the correspondent diameter, while in males this
proportion is 45%. Vulva at 54% of the body; two perivulvar glands present, opening of perivulvar gland cells not
clear; vagina transverse; ovejector sclerotized; vagina vera separated from vagina uterine by sphincter; uteri paired
opposed; two cells (glands?) at the junction of vagina and uteri visible; spermatheca occupying about one third of
each uterus; oviduct indistinct; ovaries antidromously reflexed, flexion at the junction of ovary and uterus. Anterior
ovary to the left side of the intestine, posterior ovary to the right. Female tail conical, longer than in males.
Terminal spinneret with same morphology than in males but slightly elongated.
Juveniles: similar to adults in most morphological aspects.
Differential diagnosis. Dystomanema cadizensis gen. nov. sp. nov. is characterized by its body size, number
of supplements, both testes directed anteriorly and has the diagnostic features of the genus. The condition of both
testes directed anteriorly was unknown within the family until now. Size of testes changes with male development
but the posterior one always remains smaller than the anterior one. It is very close to Dystomanema brandtae gen.
nov. sp. nov. but differs by the body size. Males about 70% smaller than males of D. brandtae gen. nov. sp. nov.
Among females this difference is reduced to about 40%. The amount of precloacal supplements is also smaller: D.
cadizensis gen. nov. sp. nov. has 10 to 12 cup-shape supplements while D. brandtae gen. nov. sp. nov. has 20.
Etymology. The species is named after the sampling location – Gulf of Cádiz.

Dystomanema brandtae gen. nov. sp. nov.

(Figs. 7 A–F, 8 A–F, 9 A–F, Table 1)

Material examined. Two males and 3 females. Holotype male (Inventory No. UGMD 104269), paratype male
(Inventory No. UGMD 104270), three paratypes females (Inventory No. UGMD 104271, 104272, 104273)
Type habitat and locality. Remnant cold-seep sediments in the Larsen B area off the Eastern Antarctic
Peninsula (65°26.07’–65°26.10’S; 61°26.48’–61°26.53’W)
Description. Males: Body slender, long, uniform in diameter, tapering anteriorly and posteriorly. Fixation shape
mostly coiled. Cuticle transversally striated with fine punctation more evident on the tail region. No lateral
differentiation. Few somatic setae with no fixed distribution pattern. Head conical, low lips. Inner labial sensilla
papilliform, six outer-labial short setiform sensilla, four cephalic setae 4 µm or 25% of corresponding body
diameter long. Short dorso-sublateral subcephalic setae present. Amphid spiral 3+ turns. Oral opening ventrally
displaced. Buccal cavity wide, deep (21 µm), funnel shaped. Gymnostom followed by well-cuticularized
pharyngostom with expanded conical posterior part. Sclerotized walls of pharyngostom with three small teeth, a
dorsal tooth and two smaller subventral teeth. Pharynx cylindrical with a posterior muscular bulb. Nerve ring
located about 20% of pharynx length from anterior end. Secretory excretory pore located immediately after
cephalic setae. Reproductive system with long vas deferens, with clear patch from the level of the 7th to the 11th and
5th to the 10th supplement from the cloaca. Anterior testis outstretched and anteriorly directed, posterior one smaller
and reflexed. Anterior testis to the right of intestine and posterior one to the left. Spicules of equal size, about the
same length as the cloacal diameter, slightly cephalated, bent about 1/3 of the distance from the distal end.
Gubernaculum plate-like with a sclerotized rod-like internal structure at the distal half. Twenty conspicuous
cup-shaped precloacal supplements with external longitudinal articulated flange. Prominent ventral precloacal
spine anterior to the cloacal opening. Tail conical plump, with bluntly rounded tip. Three caudal glands opening in
a terminal blunt spinneret.
Females: Females are similar to males in most respects, in general longer. Amphids do not show dimorphism
in shape or number of turns but in females amphids occupy just 40% of the correspondent diameter, while in males
this proportion is 50%. Vulva at 53% of the body; four perivulvar gland cells present; vagina transverse; ovejector
without special sclerotization; vagina vera inconspicuous, no sphincter present; uteri paired opposed; spermatheca
developed as outpocketing of each uterus; oviduct indistinct; ovaries antidromously reflexed, flexion at the
junction of ovary and uterus; ovary position in relation to the intestine not clear. Female tail conical, longer than in
males. Spinneret terminal, elongated.
Juveniles: Similar to adults in most morphological aspects.

18 · Zootaxa 3692 (1) © 2013 Magnolia Press BEZERRA ET AL.

FIGURE 7. Dystomanema brandtae gen. nov., sp. nov. (Holotype male). A: entire body; B: anterior end surface view; C:
anterior end median section; D: posterior end; E: female reproductive system; F: Female tail. (Scale bars: A= 100 µm; E, F= 50
µm; B, C, D= 20 µm).

NEW GENUS AND TWO NEW SPECIES OF ETHMOLAIMIDAE Zootaxa 3692 (1) © 2013 Magnolia Press · 19
FIGURE 8. Dystomanema brandtae gen. nov., sp. nov. Male. A: entire body; B: pharynx; C: mouth, pharynx, detail nerve
ring; D: end of anterior testis; E: end of posterior reflexed testis; F: supplements, spicules. (Scale bars: A= 200 µm; B, E, F= 20
µm; C,D= 50 µm).

20 · Zootaxa 3692 (1) © 2013 Magnolia Press BEZERRA ET AL.

FIGURE 9. Females of Dystomanema brandtae gen. nov., sp. nov. A: entire body; B: head; amphid C: anterior end, median
section; D: reproductive system, vulva; E: vulva and perivulvar glands; F: tail. (Scale bars: A= 200 µm; D= 100 µm; C, F= 50
µm; B, E= 20 µm).

Differential diagnosis. Dystomanema brandtae gen. nov. sp. nov. is characterized by its body size, number of
supplements, posterior testis reflexed and has the diagnostic features of the genus. The posterior testis is smaller
than the anterior one. The condition of reflexed posterior testis has not been mentioned for the family until now.
However, the drawing of Filitonchus ewensis description (Platt, 1982), shows a similar situation as observed in D.
brandtae gen. nov. sp. nov. but he does not mention it and just describes it as “two opposed testes; anterior right,
posterior left to the gut”. In addition, Lorenzen (1994) suggested that the posterior testis of Ethmolaimus (Family
Ethmolaimidae, subfamily Ethmolaiminae) is reflexed by describing the position of the testis structure from his
own observations: “the posterior one (testis) proceeds anteriorly for a bit and then folds over to posterior”, although
he doesn’t use the term ‘reflexed’. These observations suggest that the occurrence of a reflexed posterior testis has
been overlooked in the past, and may support the classification of Dystomanema gen. nov. within the family
Ethmolaimidae.
Dystomanema brandtae gen. nov. sp. nov. is very close to D. cadizensis gen. nov. sp. nov. but D. brandtae
gen. nov. sp. nov. is about 70% longer, this difference is reduced to 40% when females of both species are
compared. Unlike D. cadizensis gen. nov. sp. nov., the fixation shape of D.brandtae gen. nov. sp. nov. is mostly
coiled. The punctation of D. brandtae gen. nov. sp. nov. remains fine but is more evident than in D. cadizensis gen.
nov. sp. nov. Both species have very small teeth which can easily be overlooked, but in D. brandtae gen. nov. sp.
nov. they are even smaller. D. brandtae gen. nov. sp. nov. has 20 cup-shaped supplements while D. cadizensis gen.
nov. sp. nov. has 10 to 12.

NEW GENUS AND TWO NEW SPECIES OF ETHMOLAIMIDAE Zootaxa 3692 (1) © 2013 Magnolia Press · 21
 The clear patch of the vas deferens mentioned in the revision of Ethmolaimidae (Platt, 1982) is also recognized
in the two new species of the new genus. A similar structure has been described by Gourbault and Vincx (1988) for
Calomicrolaimus compridus Gerlach, 1956, although they mention “there is a clear patch because of the presence
of only very fine granules in that region (cf. some Ethmolaimidae, Platt 1982)”. In Dystomanema gen. nov. we
didn’t find granules in this region. Muthumbi et al. (1997) also mention a clear patch for Sabatieria pisinna but do
not explain if, like Gourbault and Vincx (1988), it is a region of very fine granules. The drawing of S. pisinna in the
article doesn’t show the patch. Since the description of the patches in those other families does not match with the
structures we identified in Dystomanema gen. nov., we are not able to affirm that the mentioned authors described
the same type of structure.
Etymology. The species is named in honour of Prof. Angelika Brandt, for her valuable contributions to
Antarctic research.

Remarks on the classification of the family Ethmolaimidae and its members

The nematode family Ethmolaimidae has had a confusing taxonomic and classification history, mainly due to the
presence of a spiral amphid and punctated cuticle. In this section we do not aim at giving an exhaustive
chronological overview of the classification of all members of the family Ethmolaimidae, but a concise account of
the relevant changes to situate the Ethmolaimidae and its members in the current classification.
Originally, the genus Ethmolaimus De Man, 1880 was placed in the subfamily Spilipherinae Filipjev, 1918
(family Chromadoridae Filipjev, 1917) until Filipjev & Stekhoven (1941) erected the subfamily Ethmolaiminae,
synonimized with Spilipherinae by Hope and Murphy (1972). De Coninck (1965) and Gerlach & Riemann (1973)
considered Ethmolaimus as a member of the family Chromadoridae, but Lorenzen (1981), in a precursor work for
his well-known 1994 work “A phylogenetic systematic account of free-living nematodes”, recognised the family
Ethmolaimidae in its own right on the account of there being no halopomorphy for the family Chromadoridae when
the genus Ethmolaimus was included.
The genus Neotonchus Cobb, 1933 was originally described as a member of the family Chromadoridae
Filipjev, 1917 but was transferred to the family Cyatholaimidae Filipjev, 1918, by Wieser & Hopper (1966) who
established the subfamily Neotonchinae for this genus. Similarly as done for the Ethmolaiminae, Lorenzen (1981)
raised the subfamily Neotonchinae to family level, the Neotonchidae, on the account of there being no holophyly if
placed within Cyatholaimidae or Chromadoridae on the basis of several cephalic characteristics.
At the time of Lorenzen’s publication of 1981, there were hence the family Ethmolaimidae Filipjev &
Stekhoven, 1941 (with one genus Ethmolaimus de Man, 1880) and the family Neotonchidae (with two genera,
Gomphionema Wieser & Hopper, 1966 and Neotonchus Cobb, 1933).
In an extensive revision of the family Ethmolaimidae, Platt (1982) argued that Lorenzen could not establish
monophyly with the families Ethmolaimidae and Neotonchidae, and so grouped Ethmolaimus and the
Neotonchidae of Lorenzen (1981) in the family Ethmolaimidae Filipjev & Stekhoven 1941. Platt (1982) reinstated
the subfamilies Ethmolaiminae and Neotonchinae within the family Ethmolaimidae, and established the genus
Trichethmolaimus within the Ethmolaiminae, placing it together with the genus Ethmolaimus. Within the
Neotonchinae, he grouped the genera Gomphionema Wieser & Hopper, 1966, Neotonchus Cobb, 1933,
Nannolaimus Cobb, 1920 and created three new genera in the subfamily; Gomphionchus, Neotonchoides, and
Filitonchus. Platt (1982) also synonymised the genus Comesa Gerlach, 1956 with the genus Neotonchoides Platt,
1982. Although Lorenzen in his systematic account of 1994, agreed with the argumentation Platt had put forward
in his 1982 revision, he failed to include the changes, which may have caused confusion with taxonomists using the
work of Lorenzen (1994), because there is one single sentence where he says that the changes proposed by Platt
(1982) haven’t been integrated. In a follow-up of his 1982 revision, Platt (1985) synonymised the genera
Neotonchoides Platt, 1982 and Comesa Gerlach, 1956, the latter being the valid name.
In a revision of the subfamily Ethmolaiminae Filipjev & Stekhoven, 1941, Jensen (1994) described a new
genus, Paraethmolaimus within the Ethmolaiminae and synonymised Trichethmolaimus Platt, 1982 with
Ethmolaimus de Man, 1880. Previously, in 1985, Jensen had described a new genus within the Neotonchinae,
namely Filitonchoides (Jensen, 1985). In his revision, Jensen (1994) did not mention the genus Ethmodora Khera,
1975 described under Cyatholaiminae, based on 5 females. The genus was according to the author (Khera, 1975)

22 · Zootaxa 3692 (1) © 2013 Magnolia Press BEZERRA ET AL.

positioned between the genera Achromadora Cobb 1913 and Ethmolaimus De Man 1880 (under the family
Cyatholaimidae by the time of its description). Ethmodora Khera, 1975 was listed by Andrassy (1992) as
Ethmolaimidae (cf. Ethmolaiminae) but since no male has been described so far, we do not accept it as a valid
genus.
Currently, the status of the family Ethmolaimidae and its two subfamilies, the Ethmolaiminae and
Neotonchinae, is generally accepted. De Ley & Blaxter (2002) had raised the Neotonchinae to family level, re-
establishing the family Neotonchidae, but we fail to see the reasons why and there are no solid arguments provided
by De Ley & Blaxter (2002) to deviate from the classification at subfamily level and above as given in Platt (1982);
presumably Platt’s work and/or Lorenzen’s (1994) very brief acknowledgement of Platt’s work (1982) were
overlooked. The Ethmolaimidae Filipjev & Stekhoven, 1941 therefore consists of two subfamilies, (1) the
Ethmolaiminae Filipjev & Stekhoven, 1941, containing the genera Ethmolaimus de Man, 1880 and
Paraethmolaimus Jensen, 1994, and (2) the Neotonchinae Wieser & Hopper, 1966, containing the genera Comesa
Gerlach, 1956, Dystomanema gen. nov., Filitonchoides Jensen, 1985, Filitonchus Platt, 1982, Gomphionchus Platt,
1982, Gomphionema Wieser & Hopper, 1966, Nannolaimus Cobb, 1920, and Neothonchus Cobb, 1933.

Notes on the ecology of Dystomanema gen. nov. and Ethmolaimidae

Ethmolaimid nematodes are usually sparsely represented in nematode studies and hence, information on them is
scant. Despite efforts to clarify their taxonomy and classification, synecological information on this nematode
family is lacking. However, they are regularly mentioned in studies that focus on chemosynthetic environments,
such as cold seeps and hydrothermal vents, and in deeper sediment layers (thiobenthos) where oxygen levels are
usually low and sulphide content usually high, similar to chemosynthetic environments.
Zeppilli and Danovaro (2009) recovered Ethmolaimidae representatives at a meter away from a shallow-water
hydrothermal vent in the Pacific Ocean; Ethmolaimidae represented only 0.9% of the total community, however.
Similar relative abundances of Ethmolaimidae were found in sediments surrounding mud volcano sediments in the
Sicily Channel in the Mediterranean (Zeppilli et al. 2011). In the deep Western Mediterranean, Ethmolaimidae
species were found in the sediments of an inactive pockmark crater of a pockmark field, characterized by active
hydrocarbon expulsions from the seafloor (Zeppilli et al. 2012). In the latter study, a Paraethmolaimus species
contributed significantly to the community differences between the active and inactive pockmark sites.
Interestingly, Jensen (1985) described a new genus, Filitonchoides, belonging to the subfamily Neotonchinae
within the Ethmolaimidae from a sulphide-rich brine seep in the Gulf of Mexico (see also Jensen 1986), and in
1987, he mentions a Nannolaimus species (Ethmolaimidae) from deep anoxic sandy sediment layers of the
Denmark Coast (Jensen 1987).
Shirayama and Ohta (1990) mentioned the presence of the ethmolaimid Gomphionchus (4.9% of the total
nematode community) in a cold seep community off Hatsushima, Central Japan, and another unidentified genus of
Ethmolaimidae close to the seep site. Ethmolaimidae were also recovered from a large pockmark area with active
methane seepage in the North Sea, off the coast of Scotland (Dando et al. 1991), where it co-occurred with the
dominant chemosynthetic nematode Astomonema southwardorum (Austen et al. 1993). Perhaps not coincidently,
the same species was dominant in deeper layers of organically enriched sediment samples from the Whittard
Canyon in the Northeast Atlantic where Ethmolaimidae genera were observed in densities of about 1–2% of the
total nematode community (Ingels et al. 2011; Lins et al. 2013).
So there seems to be an affinity of genera belonging to the family Ethmolaimidae with ecosystems that are
characterized by fauna with the ability to harness chemosynthetic energy. However, Ethmolaimidae nematodes
seem to occur in the patches where chemosynthetic activity is not at its highest, areas where the seep-activity or
methane release has died out or is only reminiscent of what once was a highly active seep habitat. The observation
of Ethmolaimidae’s association with low-activity seep sites is reinforced by the discovery of this family (of which
Dystomanema gen. nov. is described in the present study) in high abundances at the low-activity Darwin mud
volcano in the Gulf of Cádiz, Northeast Atlantic (Pape et al. 2011), and the remnant seep off the Eastern Antarctic
Peninsula in the Larsen B area (Hauquier et al. 2011). At these sites, 8 to nearly 10% of the total nematode
community consisted of the new Ethmolaimidae genus, which translates into densities of nearly 400 ind. 10 cm-2
for the Antarctic low-activity seep, and 58 and 229 ind. 10 cm-2 at the Gulf of Cádiz seep site, and 2 m away from
it, respectively (Hauquier et al. 2011; Pape et al. 2011).

NEW GENUS AND TWO NEW SPECIES OF ETHMOLAIMIDAE Zootaxa 3692 (1) © 2013 Magnolia Press · 23
 Diminishing abundances of Dystomanema gen. nov. with increasing distance from active seepage or their
presence at near-dormant or remnant seeps suggests that these nematodes are not able to thrive in the unfavorable
conditions associated with highly active seeps, but somehow they must benefit from it in the vicinity of seep
activity or when the seepage has died down.
In contrast with Astomonema southwardorum, a true chemosynthetic nematode which lacks a mouth and
possesses a gut lumen filled with symbiotic prokaryotes (Austen et al. 1993; Ingels et al. 2011; Tchesunov et al.
2012), no ecto- or endosymbiotic microbiota has been observed in association with Dystomanema gen. nov. or any
other Ethmolaimidae species for that matter. It is likely, however, that Dystomanema gen. nov. may benefit from
the influence of seep activity by feeding on bacteria, which are usually highly abundant in these habitats, on
dissolved organic matter released upon bacterial lysis or on particles that are covered with bacteria and hence
provide a great source of nutrition (e.g. Pape et al. 2011). Alternatively, or complementary, reduced feeding
competition as a result of the characteristic deposit-feeding community present at seep sites (Vanreusel et al. 2010;
deposit feeders usually have small buccal cavities and lack teeth) may enable Dystomanema gen. nov. to thrive in
these environments by being able to exploit the larger particles (with or without bacteria attached) that are not
accessible for typical deposit-feeding nematodes. The latter hypothesis does imply, however, that nematodes with
similarly large buccal cavities and teeth may be competing with Dystomanema gen. nov. for the same food sources.
Examples are found within the genera Sabatieria and Desmodora, which have relatively large buccal cavities and
are often abundant or dominant in seep sediments (e.g. Vanreusel et al. 2010; Van Gaever et al. 2009; Pape et al.
2011). These two genera are thought to be adapted to the requirements of suboxic or anoxic environments (in seeps
or deeper sediment layers), but the mechanisms underpinning these adaptations are not well understood (Vanreusel
et al. 2011). There are indications that these and other nematodes exhibit sulphur inclusions close to their cuticle
(Pape et al. 2011), which may be indicative of a thiobiotic life-style, but their significance is ambiguous and their
adaptive value for a thiobiotic lifestyle rather disputed (Vanreusel et al. 2010). There were no indications of sulphur
inclusions for the Dystomanema gen. nov. species described here, but ultrastructural electron-microscopic and
sulphur analysis are warranted to see whether there are any indications for such structures. Complementary further
investigations with electron-microcopy and molecular analysis should be able to resolve whether there are any
bacterial associations to be found with Dystomanema gen. nov. Despite the lack of evidence that indicates the
reasons behind their thiobiotic life style or an ability to harness chemosynthetic energy directly or indirectly, the
high abundance of Dystomanema gen. nov. at the here described seep sites, especially in deeper sediment layers,
suggests that they must thrive in such conditions. Their occurrence in deeper sediment layers and characteristic
long, relatively slender body shape lead us to assume that they may adhere to a thiobiotic life style. Dystomanema
cadenzis gen. nov. sp. nov was found between 1 and 9 cm sediment depth while Dystomanema brandtae occurred
in deeper sediment layers mainly between 10 and 15 cm depth. As Sabatieria and other seep-associated genera,
Dystomanema gen. nov. has a long, slender habitus. Increased body length is considered an adaptation to sulphidic
conditions in that it facilitates nematodes to cover the distance between anoxic, sulphidic and oxic, sulphide-free
sediments (Schratzberger et al. 2004; Soetaert et al. 2002), whilst the associated body surface expansion may
secure sufficient access to oxygen for respiration (Jensen, 1987).
Despite the fact that Dystomanema gen. nov. abundance is high in the here reported seep sediments (especially
in deeper layers), and their slender elongated form is typical for deep-living, thiobiotic nematodes, further
investigations are needed to ascertain the ecological significance of the Dystomanema gen. nov. and
Ethmolaimidae in general in chemosynthetic ecosystems and the ways in which they are adapted to live and feed
successfully under low-activity or remnant seep conditions.

Acknowledgments

This research was funded through the European Commission’s Seventh Framework Programme HERMIONE
project (grant number 226354), the BIANZOII project, financed by the Belgian Science Policy (Scientific
Research Program on Antarctica) and the FWO project 'ColdSeeps' nr.G034607. Jeroen Ingels is currently
supported by a Marie Curie Intra-European Fellowship within the 7th European Community Framework
Programme (Grant Agreement FP7-PEOPLE-2011-IEF No 300879).

24 · Zootaxa 3692 (1) © 2013 Magnolia Press BEZERRA ET AL.

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