European Journal of Taxonomy 94: 1-12

http://dx.doi.org/10.5852/ejt.2014.94

This work is licensed under a Creative Commons Attribution 3.0 License.

ISSN 2118-9773

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2014 • Leduc D.

Research article

urn:lsid:zoobank.org:pub:39B7B89B-AACB-4BE0-807B-lBlDAAD913F3

Are juveniles of the enigmatic deep-sea nematode Rhaptothyreus

(Rhaptothyreida: Rhaptothyreidae) parasitic?

Daniel LEDUC

National Institute of Water and Atmospheric Research, Private Bag 14-901, Wellington, New Zealand.

Email: [email protected]

urn:lsid:zoobank.org:author:9393949F-3426-4EE2-8BDE-DEFFACE3D9BC

Abstract. Rhaptothyreus is arguably the most enigmatic nematode taxon due to a combination

of unusual morphological features (e.g., large feather-like amphids, vestigial mouth, trophosome,

single spicule), unclear phylogenetic relationships (possible affinities with the Enoplida, Mermithida

and Benthimermithida) and a distribution restricted to the deep sea. Here I provide the first record

of the genus in the Western Pacific Ocean and describe new morphological features of a moulting

juvenile. This specimen is characterised by features that differ markedly from those of the adults, the

most prominent being the absence of cephalic sensillae and amphids and the presence of a stylet-like

structure in the buccal cavity. Similar contrasts in morphology are found between adults and juveniles

of the order Benthimermithida, which is characterised by free-living adults and parasitic juveniles.

Other morphological (large body size, presence of trophosome) and distributional characteristics

(predominantly deep-sea distribution, juveniles rare / absent in sediments) are also common to both

groups. Published records show that Rhaptothyreus is commonly found in oligotrophic environments

(e.g., abyssal plain) where organisms bearing symbiotic bacteria are not typically found, which makes

the presence of endosymbiotic bacteria inside the trophosome unlikely. These observations are consistent

with the existence of a parasitic juvenile life stage in Rhaptothyreus.

Keywords. Benthimermithida, continental slope, ontogeny, Rhaptothyreus typicus, New Zealand

Leduc D. 2014. Are juveniles of the enigmatic deep-sea nematode Rhaptothyreus (Rhaptothyreida: Rhaptothyreidae)

parasitic? European Journal of Taxonomy 94: 1-12. http://dx.doi.org/10.5852/eit.2014.94

Introduction

The deep-sea nematode Rhaptothyreus typicus Hope & Murphy, 1969 is characterised by several unusual

morphological features, including a vestigial mouth and pharynx, presence of a trophosome, large

feather-lilce amphids and a single spicule. The phylogenetic relationships of this enigmatic taxon remain

unclear, but affinities with the Enoplida (Hope & Murphy 1969; Miljutin 2014b), Mermithida (Hope

1977; Petter 1980) and Marimermithidae or Benthimennithidae (Inglis 1983) have been suggested. In the

original description of the species, Hope & Murphy (1969: 72) state that “... the possibility of a change

in the structure of the amphid during development, suggest that younger juveniles may possess certain

morphological features that would provide a clue to the phylogenetic relationships of this species.” All

specimens that have been collected since, however, are either specimens with a heavily cuticularized

spicule (usually referred to as males) or late-stage moulting juveniles with a lightly cuticularized spicule

European Journal of Taxonomy 94: 1-12 (2014)

(but otherwise similar to the males); no females have yet been observed. It has also been suggested

that males may in fact be juveniles due to the lack of well-defined testes in specimens with a strongly

cuticularized spicule (Miljutin et al. 2006).

The absence of a mouth and alimentary canal indicates that Rhaptothyreus does not feed, and the

trophosome is thought to serve either as a food reserve or as an organ housing endosymbiotic

bacteria (Miljutin et al. 2006). A detailed morphological study using transmission and scanning

electron microscopy did not unequivocally demonstrate the presence of bacteria in the trophosome of

Rhaptothyreus typicus (Miljutin et al. 2006). The absence of bacterial symbionts would suggest that

the trophosome acts as a food reserve for the non-feeding adults, as in the mouthless adults of the

order Benthimermithida (Miljutin 2014a). Juveniles of benthimermithid nematodes parasitize a range of

invertebrate hosts and emerge as free-living adults in the sediments. Rhaptothyreus may have a similar

life cycle, but no parasitic juveniles have yet been found, perhaps due to pronounced morphological

divergence (as was suggested to explain the apparent absence of females; Hope & Murphy 1969).

Rhaptothyreus is exclusively found in the deep sea and is widely distributed on the continental slope

and abyssal plain of the North and South Atlantic Oceans, as well as in the Eastern Pacific Ocean on

the continental margin of South America (see summary by Miljutin et al. 2006). Here the first record of

the genus in the Western Pacific Ocean is provided, and new evidence for a parasitic life cycle similar

to that found in benthimermithids is presented based on morphological differences between male and

juvenile specimens.

Material and methods

Samples were obtained from New Zealand’s southern Hikurangi margin, Southwest Pacific. They

were collected during National Institute of Water and Atmospheric Research (NIWA) cruise TAN1004

(1046 m water depth) on 15 April 2010 using an Ocean Instruments MC-800A multicorer (MUC; core

internal diameter = 9.5 cm). The top five cent im etres of sediment were fixed in 10% formalin and

stained with Rose Bengal. The sample was rinsed on a 1 mm sieve to remove large particles and on a

45 pm sieve to retain nematodes. Nematodes were extracted from the remaining sediments by Tudox

flotation and transferred to pure glycerol (Somerfield & Warwick 1996). Observations were made from

glycerol mounts using differential interference contrast microscopy and drawings were made with the

aid of a camera lucida. Specimens for scanning electron microscopy (SEM) were transferred to a 2%

glutaraldehyde solution with sodium cacodylate buffer overnight and then transferred to a 4% osmium

tetroxide solution for 2 hours. Specimens were gradually transferred to pure ethanol using a graded

ethanol series, critical point dried, and mounted onto stubs before coating with gold using a sputter

coater. Observations were made using a Hitachi TM3000 tabletop SEM at high vacuum mode.

All measurements are in pm, and all curved structures are measured along the arc. Type specimens are

held in the NIWA Invertebrate Collection (NIC), Wellington, New Zealand. Abbreviations in the text

are as follows:

a = body length / maximum body diameter

abd = anal body diameter

c = body length / tail length

cbd = corresponding body diameter

Miljutin et al. (2006) questioned whether specimens with a well-developed spicule are indeed male, as

they do not possess obvious testes. For the purpose of this study, specimens with a heavily cuticularized

spicule are referred to as males; all other specimens are referred to as juveniles.

LEDUC D., Are Rhaptothyreus juveniles parasitic?

Results

Order Rhaptothyreida Tchesunov, 1995

Family Rhaptothyreidae Hope & Murphy, 1969

Rhaptothyreus Hope & Murphy, 1969

Rhaptothyreus typicus Hope & Murphy, 1969

Figs 1-4, Table 1

Material examined

NEW ZEAFAND: 3 SS (NIWA 88370; two specimens processed for SEM after observations under

light microscopy), 15 Apr. 2007, NIWA cruise TAN 1004, st. 4, southern Hikurangi margin, 175.6642° E,

4E6837° S, open slope habitat, 1046 m, mean particle size (geometric) 12 pm, silt / clay content 94.7%,

CaC0 3 content 2.1%, organic carbon content 1.0%. One juvenile (processed for SEM after observations

under light microscopy), same data as

Description

Male

Body cylindrical, tapering slightly towards anterior and posterior ends. Cuticle with light striations

1-2 pm apart, confined to innermost cuticle layer (Fig. 2B), but also visible on SEM micrographs

(Fig. 4A, D), 2.0-2.5 pm thick in mid-body, thickening gradually towards head and tail regions (up to

5 pm thick) due to expansion of median layer (Fig. 1A). Eight longitudinal rows of short somatic setae,

~1 pm long, beginning from anterior edge or mid-level of amphid and extending -2 cbd posterior to

nerve ring; each seta in small pit; anteriormost setae with conspicuous ducts; rest of body devoid of

somatic setae (confirmed using SEM). Chords consisting of two longitudinal rows of cells, often poorly

defined, with clear round inclusions (Figs IE, 2C). Longitudinal muscle fibres 2-5 pm thick, beginning

at level of amphids and most conspicuous in anterior body region. Metanemes not observed.

Remnant of oral aperture pore-like or not discernible. Six inner and six outer labial papillae in pairs and in

one circle (presence of paired inner and outer labial papillae difficult to observe with light microscopy),

~1 pm long and 5-7 pm from anterior end, each pair of setae in small pit with conspicuous duct; second

circle of four submedian papilliform sensillae of similar length and structure to setae of first circle,

12-14 pm from anterior end. Amphid large, oblong, ~1.3 cbd in height and 0.5-0.6 cbd wide, with

strongly cuticularized outline (Fig. 2A). Amphideal fovea covered by a thin layer of cuticle with central

longitudinal rib tapering anteriorly; thin layer of cuticle with transverse rows of minute perforations.

Amphideal canal strongly cuticularized, splitting into two ducts directly underneath amphideal fovea

(Fig. 2A). No clear buccal cavity present; pharynx with indistinct contours, remnant of pharyngeal

lumen sometimes visible as continuous, longitudinal slit extending from oral region to slightly posterior

to nerve ring. Nerve ring conspicuous. Secretory-excretory system not observed.

Trophosome present, tapering anteriorly, beginning 169-183 pm from anterior end, filled with numerous

small, rod-shaped structures, 0.7-1.4 x 1.2-2.3 pm. No cellular structure discernible in anterior portion

of trophosome; one specimen with clear globular inclusions, possibly remnant of cell nuclei. Four or

five longitudinal rows of nucleated, oval-shaped turgescent cells, 7-17 x 17-25 pm, situated dorsally

and subdorsally and extending from anterior end of trophosome to slightly anterior to spicules (Figs

IE, 2B). At -90% of body length from anterior, trophosome appearance changes abruptly to rows of

large, strongly stained, nucleated cells with minute round inclusions, -1 pm in diameter (Fig. 3B). Cells

decrease in size slightly posteriorly and form a short duct (possibly vas deferens) anterior to spicule.

European Journal of Taxonomy 94: 1-12 (2014)

Fig. 1. Rhaptothyreus typicus Hope & Murphy, 1969. Line drawings. A. Lateral view of male head.

B. Lateral view of moulting juvenile head, with details of surface striations on outer cuticle and outline

of amphid under moulting cuticle. C. Anterior body region of male. D. Anterior body region of juvenile.

E. Lateral view of male mid-body region. F. Posterior body region of male. G. Posterior body region

of juvenile. Arrows show the position of the chord (c) and turgescent cells (t). Scale bar: A-B = 50 pm,

C-D = 75 pm, E = 60 pm, F-G = 70 pm.

LEDUC D., Are Rhaptothyreus juveniles parasitic?

Fig. 2. Rhaptothyreus typicus Hope & Murphy, 1969. Light micrographs (c?)- A. Lateral view of head

showing amphid. B. Mid-body region showing cuticle, turgescent cells and portion of anterior tropho-

some with rod-shaped structures. C. Cells of lateral chord with clear, round inclusions. D. Posterior

body region. Arrows show the position of the two small ducts apparently joining just prior to the cloacal

opening. Scale bar: A, C = 20 pm, B = 18 pm, C = 30 pm.

European Journal of Taxonomy 94: 1-12 (2014)

Fig. 3. Rhaptothyreus typicus Hope & Murphy, 1969. Light micrographs (moulting juvenile). A. Lateral

view of head, showing stylet-like structure. B. Sharp transition between anterior (left) and posterior

trophosome (right). C. Lateral chord, mid-body region. D. Posterior body region. Scale bar: A = 20 pm,

B = 40 pm, C = 28 pm, D = 25 pm.

LEDUC D., Are Rhaptothyreus juveniles parasitic?

Table 1. Morphometries (pm) of specimens of Rhaptothyreus typicus from New Zealand’s southern

Hikurangi margin, a = body length/maximum body diameter; abd = anal body diameter; c = body length

/ tail length; cbd = corresponding body diameter; L = body length.

Males

Juvenile

5578

6010

4484

4931

119

140

118

Head diameter at level of mid-amphid

Amphid height

Amphid width

—

Amphid width / cbd (%)

—

Amphid from anterior end

Nerve ring from anterior end

111

112

101

111

Nerve ring cbd

Maximum body diameter

Spicule length

Anal body diameter

Tail length

Tail length / abd

1.1

1.0

0.9

1.2

Single unpaired spicule, 1.5-1.8 abd long, strongly cuticularized, tapering distally and with sharp

bend at ~l/5 of spicule length from distal tip; distal tip slightly swollen (Fig. 2D). Proximal part of

spicule contains several small glandular cells; longitudinal structures along spicule length may be ducts

connecting glands and small pores (discontinuities in cuticle) near distal tip of spicule (Fig. IF). Spicule

almost completely surrounded by muscular tissue (sheath); at least three pairs of muscles attached to

dorsal and ventral body wall. Two small ducts, apparently joining before cloacal opening, visible in

two specimens (Fig. 2D). Tail short, conical, with conspicuous terminal cap (Figs 2D, 4D). Terminal or

subterminal pore present; caudal glands not observed.

Moulting juvenile

Similar to males in general appearance. Striations of innermost cuticle layer not discernible except in

posterior body region; surface of cuticle with fine striations. Small granules separating outer and inner

layers of head cuticle (Fig. 3A). A few sparse somatic setae present in pharyngeal region, each with a

small pit, not in obvious rows. Chords consist of two rows of well defined oval-shaped, nucleated cells

without inclusions (Fig. 3C).

Cephalic sensillae not observed. No amphideal aperture visible on moulting cuticle (Fig. 4C); amphid

of similar size and shape as male amphid, located underneath moulting cuticle, barely visible, not

cuticularized (Fig. IB). Oral aperture minute. Small, cuticularized, stylet-like structure, 10 pm long,

narrowest in middle region, situated directly underneath oral aperture; may be remnants of narrow,

cuticularized buccal cavity (Fig. 3A). Outline of vestigial pharynx with anterior portion of lightly

cuticularized pharyngeal tubes visible, with small anterior bulb surrounding stylet-like structure and

with posterior bulb immediately posterior to a conspicuous nerve ring.

European Journal of Taxonomy 94: 1-12 (2014)

Fig. 4. Rhaptothyreus typicus Hope & Murphy, 1969. Scanning electron micrographs. A-B. Male

head. C. Juvenile head. D. Male posterior body region. Scale bar: A = 20 pm, B = 8 pm, C = 12 pm,

D = 16 pm.

LEDUC D., Are Rhaptothyreus juveniles parasitic?

Intestine modified into trophosome; anterior and posterior parts of trophosome similar in structure to that

of males, but with globular, not rod-shaped, structures (Fig. 3B). Four rows of turgescent cells present

dorsally and subdorsally. Spicule similar in shape to that of male specimens, but lightly cuticularized

(Fig. 3D). Tail short, conical, without terminal cap. Terminal pore present.

Remarks

The Hikurangi margin male specimens agree well with the description of R. typicus by Hope & Murphy

(1969), although a few inconsistencies were noted. The Hikurangi margin specimens are characterised

by short body length relative to the type specimens (4,484-6,010 vs. 6,990-12,800 pm), but within

the range reported by Miljutin et al. (2006) for the same species. The longitudinal rows of turgescent

cells observed in the Hikurangi specimens were not observed in the original description of the species

by Hope & Murphy (1969) or the description by Miljutin et al. (2006); Riemann (1993), however,

described the presence of longitudinal rows of turgescent cells in the dorsal region of the type specimens

of R. typicus. In addition, the ventral transverse ridge observed on the ventral side of the tail of the type

specimens by Hope & Murphy (1969) and mentioned in the description of Miljutin et al. (2006) was

not present in the specimens observed in the present study; furthermore, this feature was not noted in

RiemamTs (1993) description.

Discussion

Some conspicuous differences in morphology were observed between the males and the juvenile

specimen. Most notably, the amphideal aperture, cephalic sensillae and tail terminal cap found in the

males were not observed in the juvenile, whereas a stylet-like structure and relatively well defined

(but vestigial) pharynx were observed in the juvenile specimen but not the males. These and other

morphological differences are consistent with the description of a juvenile by Hope & Murphy (1969),

who noted that the stoma was more evident in juveniles than in males, while the terminal cap on the

tail was absent and the amphids and spicule less strongly cuticularized. It appears that the Hikurangi

margin specimen represents an earlier stage juvenile, as it has retained more juvenile features than those

observed by Hope & Murphy (1969). The latter specimens were referred to as fourth-stage juveniles,

but they may be better described as recently moulted males; the sexual maturity of so-called males

(i.e., specimens with a heavily cuticularized spicule) is yet to be confirmed, however, and it is unclear

what stage the juvenile specimen described here may be. The pronounced morphological differentiation

between male and juvenile Rhaptothyreus is unusual among nematodes (particularly free-living taxa; De

Coninck 1965) and could help explain why juvenile stages have not yet been found.

The new observations on the juvenile described herein may provide some clues as to the life cycle

of Rhaptothyreus. There are similarities between the Hikurangi margin juvenile and juveniles of

benthimermithid nematodes (Hope 1977; Tchesunov & Rozenberg 2011). Species of this family

parasitize a variety of marine invertebrate hosts as juveniles and emerge as non-feeding adults surviving

in the sediments on stored food reserves in the trophosome. Although very little is known about the

biology of juveniles, available morphological data provide a basis for comparisons. For example,

juveniles of Trophomera granovitchi Tchesunov & Rozenberg, 2011 are characterised by the absence

of cephalic sensillae and amphideal aperture, presence of a stylet-like structure in the buccal cavity

region, vestigial pharynx and midgut with internal lumen, whereas adult specimens have well-developed

cephalic sensillae and amphids, while lacking a stylet-like structure, pharynx and intestine. Similar

differences were observed between the R. typicus juvenile and adults, although no intestine was observed

in the juvenile. These contrasts observed between males and juveniles of both species may suggest that

R. typicus juveniles are parasitic, i.e., they are equipped with a feeding apparatus but mostly lacking

sense organs, as they are not necessary inside the host. Adults, on the other hand, are free-living in the

sediments and are presumed to be reproductive; a feeding apparatus is no longer required as they survive

European Journal of Taxonomy 94: 1-12 (2014)

on energy reserves, but sense organs such as cephalic sensillae and amphids are required for finding

a mate. Another morphological similarity between Rhaptothyreus and benthimermithid adults is their

large body length (~4-12 mm) relative to most free-living, deep-sea nematode species (which rarely

exceed 3 mm; D. Leduc personal observations).

A life cycle similar to that of benthimermithids would imply that the rod-shaped structures in the anterior

trophosome of male Rhaptothyreus are not bacteria. Although the size and shape of these structures is

consistent with bacteria, detailed observations with transmission electron microscopy could not confirm

the presence of bacteria in the trophosome of R. typicus (Miljutin et al. 2006). Moreover, the only deep-

sea nematode with bacterial symbionts known to date, Astomonema southwardorum Austen et al ., 2013,

is characterised by bacteria of a different shape (spherical to ovoid vs. rod-shaped in R. typicus ) and

size (7-10 x 3-5 pm vs. -I x 2 pm in R. typicus ) (Tchesunov et al. 2012). Nematodes bearing internal

symbionts are normally found in reducing environments associated with high organic matter input (Ott

et al. 1982) or methane seepage (Austen et al. 1993); they are therefore rare in the deep sea and have

so far only been found in highly productive canyon habitats (Tchesunov et al. 2012; Ingels et al. 2011).

Rhaptothyreus , however, has been found at low productivity abyssal sites (see summary in Miljutin et

al. 2006). The distribution of Rhaptothyreus is similar to that of benthimermithids, i.e., they are rare

and found mostly (or exclusively in the case of Rhaptothyreus) in the deep sea. Rhaptothyreus juveniles

are rarely encountered and juvenile specimens collected to date are all near maturity and/or presumably

undergoing their final moult, which is consistent with a life cycle where only adults are free-living (as

in benthimermithids). Finally, the nematode community at the southern Hilcurangi margin sampling site

was dominated by Mudwigglus Leduc, 2013, Paramonohystera Steiner, 1916 and Aegialoalaimus de

Man, 1907, genera that are widespread in the open slope habitats of New Zealand and without particular

affinity for chemosynthetic or highly productive environments (D. Leduc unpublished data; Leduc et

al. 2012).

It is possible that the trophosome of R. typicus is, in fact, a testis. This structure, in some of the specimens

from New Zealand, is characterised by a hollow, vas deferens-like posterior portion which appears to be

connected to the cloacal opening (although this could not be confirmed with certainty). If this were the

case, however, it is unclear where food reserves would be stored.

Rhaptothyreus shows some similarities with mermithid nematodes, which are usually parasites of

freshwater or terrestrial invertebrates, but are also found in the deep sea (Tchesunov & Hope 1997). The

amphideal fovea in adults of the marine mermithid Thalassomermis megamphis Tchesunov & Hope,

1977 is large, whereas the amphideal aperture is minute, as in Rhaptothyreus. In addition, juvenile

mermithids have a protrusible stylet that is absent in adults. Finally, several mermithid genera have only

one spicule (e.g., Thalassomermis Tchesunov & Hope, 1977 and Limnomermis Daday, 1911), a feature

that they share with Rhaptothyreus but otherwise is rare in nematodes.

In conclusion, new morphological observations of a juvenile R. typicus , as well as the distributional pattern

of the genus, suggest that Rhaptothyreus has a life cycle similar to that of benthimermithids. Further

tests of this hypothesis will require either determining the identity of the rod-shaped structures inside

the trophosome (i.e., are they bacteria or not?), or, more significantly, finding juvenile Rhaptothyerus

specimens inside a host (if they are indeed parasitic). Comparisons with adult specimens may be difficult

due to the different morphologies of adults and juveniles, and molecular tools will be required to confirm

the identity of juvenile specimens.

LEDUC D., Are Rhaptothyreus juveniles parasitic?

Acknowledgments

Funding was provided by NIWA’s Coasts and Oceans Centre Research Programme 2 (2013/14 SCI)

and the programme ‘Impact of resource use on vulnerable deep-sea communities’ (CO 1X0906). I am

grateful to Norliana Rosli for processing TAN1004 samples. I also acknowledge the other participants of

NIWA cruise TAN 1004 and the officers and crew of the RV Tangaroa. I thank two anonymous referees

who provided constructive criticisms of the manuscript.

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Manuscript received: 31 March 2014

Manuscript accepted: 25 June 2014

Published on: 25 August 2014

Topic editor: Rudy Jocque

Desk editor: Danny Eibye-Jacobsen

Printed versions of all papers are also deposited in the libraries of the institutes that are members of

the EJT consortium: Museum National d’Histoire Naturelle, Paris, France; Botanic Garden Meise,

Belgium; Royal Museum for Central Africa, Tervuren, Belgium; Natural History Museum, London,

United Kingdom; Royal Belgian Institute of Natural Sciences, Brussels, Belgium; Natural History

Museum of Denmark, Copenhagen, De nm ark