New distributional records of free-living marine nematodes from Indian waters I. Chromadorids

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1 Indian Journal of Geo-Marine Science Vol. 44(5), May 2015 pp New distributional records of free-living marine nematodes from Indian waters I. Chromadorids K.G.M.T. Ansari*, P.S. Lyla & S. Ajmal Khan Centre of Advanced Study in Marine Biology, Faculty of Marine Sciences Annamalai University, Parangipettai , Tamil Nadu, India *[ Received 12 June 2014; revised 25 June 2014 Totally 192 species of free-living marine nematodes were identified in the southeast continental shelf of India during Cruise no. 260 of FORV Sagar Samada. Among these free-living marine nematodes following nine of these Chromadorids species: Comesa cuanensis, Chromaspirina inglisi, Chromaspirina parapontica, Desmadora (Desmadora) schulzi, Metachromadora (Bradylaimus) suecica, Pseudonchus northumbriensis, Epsilonema pustulatum, Draconema claparedii and Tricoma longirostris which happen to be first record from Indian waters are described. [Key words: Meiofauna, nematodes, Chromadorids, continental shelf, India] Introduction Due to the higher density and fast turnover rates meiobenthic organisms occupies major component in benthic ecosystem 1. In all type of sedimentary habitats (intertidal to deep sea) meiobenthic production is equal or higher than macrobenthic organisms 2. Free-living marine nematodes inhabit marine benthic ecosystems, often representing more than 60% of the benthic meiobenthos 3. They play a significant role in the energy fluxes of food chain by way of degradation and mineralization of organic matter 4. Nematodes have short life span, high fecundity 5, represent several trophic levels (herbivores, bacterial feeders and carnivores), and at least some species can be easily cultured 6,7. They remain poorly understood, however, despite the fact that they are extremely abundant and diverse, often numbering millions per square meter in sediments and occur in diverse habitats than any other metazoan group 6. Free-living marine nematodes are tiny (few millimeters) in nature and taxonomically difficult to distinguish species level 8,9. Along Indian coasts, only few studies have been undertaken on meiobenthos particularly on free-living marine nematodes mostly qualitative and quantitative aspects 1, 3, and only little information is available on their taxonomy 9, Among the phylum Nematoda, Chromadorida is a largest order in class Adenophorea and its population also higher in around the globe as well as India 1, 14. Present study describes nine nematode species from order Chromadorida are recorded for the first time in Indian waters. Materials and methods The Bay of Bengal continental shelf (southeast coast of India) was taken for consideration of this present study and it extends latitude from 10º 34.03' to 15º 14.48' N and longitude from 79º 52.13' to 80º 53.87'E. Totally seven latitudinal transects (from north to south) Singarayakonda, Tammenapatanam, Chennai, Cheyyur, Cuddalore SIPCOT, Parangipettai and Karaikkal including six different depths sediments were collected for nematode analysis (Fig.1). Fig.1. Study sites of southeast continental shelf of India (Bay of Bengal)

2 ANSARI et al. NEMATODES FROM INDIAN WATERS 757 The samples were collected onboard FORV (Fishery and Oceanographic Research Vessel) Sagar Sampada during Cruise No. 260 (from 7 th to 28 th December 2008). Two sediment samples were collected using a Smith McIntyre grab (having a bite area of 0.2m 2 ) at each depth range. Immediately after the grab was hauled to the deck, sub-samples were taken from undisturbed grab samples using a glass corer (having an internal diameter of 2.5 cm and a length of 15 cm) from the middle of grab sample 27. Samples were fixed in buffered formalin at a concentration of 4%. Replicate core samples were processed separately in the laboratory and data were pooled for analyses. The samples were washed through a set of 0.5 mm and mm sieves. Sediment retained in the mm sieve was decanted to extract meiofauna following the standard method by Pfannkuche and Thiel 28. Sorting of meiofauna from sediment was done by flotation technique. The efficiency of this technique is around 95% 29. The meiofaunal organisms were stained with Rose Bengal. Sorting and enumeration were under a stereomicroscope (Meiji, Japan). Sorted nematodes were mounted onto glass slides, using the formalin-ethanolglycerol method 30. Identification of nematodes was done to the lowest taxonomic level possible using the compound microscope (Olympus CX 41 under higher magnification of 1000x) following the standard pictorial keys 27, Results Totally 192 species were identified belonging to 96 genera and 33 families from the southeast coast of India 16. Order Chromadorida is the largest order followed by Monhysterida (63 species), Enoplida (34 species) and Trefusiida (4 species) 1. Overall Chromadorida order 91 species belonging to 53 genera and 15 families were recorded. Among these, nine species from five family (Comesa cuanensis from family Ethomolaimidae; Chromaspirina inglisi, Chromaspirina parapontica, Desmadora (Desmadora) schulzi, Metachromadora (Bradylaimus) suecica, Pseudonchus northumbriensis from family Desmadoridae; Epsilonema pustulatum from family Epsilonematidae; Draconema claparedii from family Draconematidae and Tricoma longirostris from family Desmoscolecidae) were found to be new distributional records for the Indian waters. Detailed systematic account, material examined (number of specimens, place of collection, depth range and date of collection), brief description, feeding type, habitat and geographical distribution besides remarks of the above nine species are presented here. 1. Comesa cuanensis (Platt, 1982) Phylum: Nematoda Rudolphi, 1808 Class : Adenophorea von Linstow, 1905 Order : Chromadorida Filipjev, 1929 Family : Ethmolaimidae Filipjev and Stekhoven, 1941 Genus : Comesa Gerlach, 1956 Species: Comesa cuanensis (Platt, 1982) Synonym:Oncholaimus glaber Bastian, 1865 :Viscosia micoletzkyi Chitwood, 1951 Material examined: 3 males collected from Parangipettai 51-75m depth ( ) and Karaikkal 30-50m depth ( ). Male : 61.17± ± ±0.06 ( ) ( ) ( ) Body length mm. Maximum diameter 21-26µm. Cuticle with transverse rows of fine dots, rows more numerous in oesophageal region but in the latter become more numerous posterior to the oesophageal region: without lateral differentiation. Small lateral cuticle pores throughout the body, regularly spaced but difficult to detect except in head and tail regions. Six short (2-3.5µm) and four long (4-5.5µm) cephalic setae. Dorso-sublateral subcephalic setae situated posterior to each amphid. Short stout subventral somatic setae throughout body. Multi-spiral amphids12-14µm wide in male and 6-7µm wide in 4 turns and middle of amphids situated behind posterior cephalic setae. Buccal cavity wide; a pointed dorsal tooth and subventral ridges. Tail conical ( a.b.d.) with characteristic ventral bend at tip. Spicules 29-43µm measured as a curve, relatively straight. Gubernaculum simple, rod-like (Fig. 2). Feeding type: The specimens showed buccal cavity armed with small. According to the classification of buccal cavity by Wieser 34, this species is an epigrowth feeder (2A). Habitat: Sandy sediments. India: Parangipettai and Karaikkal. Elsewhere: England 31, Northeast England, European waters and Irish Sea 35.

3 758 INDIAN J. MAR. SCI. VOL. 44, NO. 5, MAY 2015 Fig.2. Comesa cuanensis A) entire male B) male head, C) male tail the earlier description, except for the larger body size. The total body length described by Platt and Warwick 31 was mm and tail length a.b.d in male. The body length of the specimen studied at present was found larger being mm and the tail length a.b.d. This is the first record of the species from the Indian waters. 2. Chromaspirina inglisi Warwick, 1970 Family : Desmodoridae Filipjev, 1922 Genus : Chromaspirina Filipjev, 1918 Species: Chromaspirina inglisi Warwick, 1970 Material examined: Single male collected from Cheyyur 30-50m depth ( ). Male : Body length 0.8mm. Maximum diameter 13µm. Cuticle covered uniformly with fine hair which commence a short distance posterior to the head: probably cuticular in origin but may be epizoic bacteria. Six short 4-6µm and four longer 12-15µm cephalic setae. Scattered somatic setae extended about one-third of the way down the oesophagus, middle region of the body virtually devoid of setae, but fairly numerous on tail. Spiral amphid 5µm. Buccal cavity with a prominent heavily cuticlarised dorsal tooth opposed by a pair of minute subventral projections. Oesophagus with elongated posterior bulb (95µm), the cuticular lining of which is not markedly thickened. Tail conical with an unstriated tip (5.8a.b.d.). Spicules 23µm measured as a curve, accurate, triangular proximal cephalization, Fig.3. Chromaspirina inglisi A) male head B) entire male, C) male tail prominent ventral ala. Gubernaculam 12µm, crescentic, closely applied to spicules. Supplements absent (Fig. 3). Feeding type: The specimen showed large teeth. According to the classification of buccal cavity by Wieser 34, this species is a predator (2B). Habitat: Sandy sediments. India: Cheyyur. Elsewhere: West Scotland and Southeast England 35 and England 31. the earlier description, except for the smaller body size. The total body length described by Platt and Warwick 31 was mm and tail length a.b.d. The body length of the specimen studied at present was found smaller being 0.8mm and the tail length 5.8a.b.d. This is the first record of the species from the Indian waters. 3. Chromaspirina parapontica Luc and De Coninck, 1959 Species: Chromaspirina parapontica Luc and De Coninck, 1959 Material examined: 4 males collected from Cheyyur 30-50m, m depths ( ) and Parangipettai 30-50m depth ( ). Male : 24.78± ± ±0.08 ( ) ( ) ( ) Body length mm. Maximum diameter 57-72µm. Cuticle covered uniformly with fine hair which commence a short distance posterior to the head: probably cuticular in origin but may be

4 ANSARI et al. NEMATODES FROM INDIAN WATERS 759 epizoic bacteria. Six conical labial papillae present. Six short 5-6µm and four longer 12-17µm cephalic setae. Eight files of short setae throughout the length of the body. Spiral amphids 6-7µm. Buccal cavity with a large strongly cuticlarised forward-pointing dorsal tooth and two much smaller subventral teeth. Oesophagus with a weakly developed posterior bulb. Tail conical ( a.b.d.). Spicules 33-52µm measured as a curve, accurate and strongly cephalate proximally. Gubernaculam crescentic. Small ventral precloacal papilla with stout seta and eight very fine tubular precloacal supplements more or less equally spaced (Fig. 4). 4. Desmodora (Desmodora) schulzi Gerlach, 1950 Family : Desmodoridae Filipjev, 1922 Genus : Desmodora Filipjev, 1922 Species: Desmodora (Desmodora) schulzi Gerlach, 1950 Synonym: Desmodora hirsuta Chitwood Material examined: 5 males and 3 females collected from Singarayakonda m and m depths ( ). Male : 30.99± ± ±0.10 ( ) ( ) ( ) Female : 23.05± ± ±0.11 ( ) ( ) ( ) Fig.4. Chromaspirina parapontica A) male head, B) entire male, C) male tail Feeding type: The specimens showed large teeth. According to the classification of buccal cavity by Wieser 34, this species is a predator (2B). Habitat: Sandy sediments. India: Cheyyur and Parangipettai. Elsewhere: England 31 ; Southwest England and European waters 35. the earlier description, except for the smaller body size. The total body length described by Platt and Warwick 31 was mm and tail length a.b.d. The body length of the specimen studied at present was found smaller being mm and the tail length a.b.d. This is the first record of the species from the Indian waters. Fig.5. Desmodora (Desmodora) schulzi A) entire male, B) male head, C) entire female, D) female head, E) male tail, F) female tail Body length mm in male and mm in female. Maximum diameter 49-57µm in male and 54-61µm in female. Cuticle with coarse striation and longitudinal files of fine setae. Six small (4-7µm) and four long (6-9µm) cephalic setae. Eight pairs of subcephalic setae posterior to amphids. Amphids loop-shaped longitudinally oval 9-12µm long in male and 10-12µm long in female. Buccal cavity with a hollow forwardly directed dorsal tooth, opposed by a pair of very much smaller subventral teeth. Oesophagus with elongated posterior bulb ( µm in male and µm in female) with cuticular lining not markedly thickened. Tail conical ( a.b.d. in male and 2.6-3a.b.d. in female). Spicules 57-59µm, arcuate and slender. Gubernaculam projects dorsally, away from the spicules. Two large supplementary organs, one just postcloacal and the other precloacal level with proximal end

5 760 INDIAN J. MAR. SCI. VOL. 44, NO. 5, MAY 2015 of spicules. Ovaries paired, opposed and reflexed. Vulva present at 68-71% of body length (Fig. 5). Feeding type: The specimens showed buccal cavity armed with small. According to the classification of buccal cavity by Wieser 34, this species is an epigrowth feeder (2A). Habitat: Silty sediments. India: Singarayakonda. Elsewhere: England 31 ; Southeast England 35 ; European waters 36 ; North Sea, Biscay and Mediterranean 35. the earlier description of Platt and Warwick 31 except for the larger body size. The total body length described was mm in male and in female these were not recorded. The body length of the specimen studied at present was found larger being mm and the tail length a.b.d. in male and in female mm body length and tail length 2.6-3a.b.d. This is the first record of the species from the Indian waters. 5. Metachromadora (Bradylaimus) suecica (Allgen, 1929) Family : Desmodoridae Filipjev, 1922 Genus : Metachromadora Filipjev, 1918 Species: Metachromadora (Bradylaimus) suecica (Allgen, 1929) Material examined: Single male collected from Singarayakonda ( ). Male : Body length 1.3mm. Maximum diameter 38µm. Cuticle conspicuously but finely striated with the striations frequently anastomosing. Six short 3µm and four long 8µm cephalic setae. Subcephalic and somatic setae very small. Loopshaped amphids (3µm) in wide and a single loop. Buccal cavity with hollow dorsal tooth opposed by small subventral projections. Oesophagus with well-developed elongate posterior bulb (186µm) with heavily cuticularised lining. Tail conical with a relatively long unstriated tip (3.8a.b.d.). Spicules 37µm, arcuate, proximally cephalic with ventral ala. Gubernaculam 16µm parallel to spicules.11 inconspicuous tubular precloacal supplements and a postcloacal ventral unstriated cuticular pad (Fig. 6). Fig.6. Metachromadora (Bradylaimus) suecica A) entire male B) male head, C) male tail Feeding type: The specimen showed buccal cavity armed with small. According to the classification of buccal cavity by Wieser 34, this species is an epigrowth feeder (2A). Habitat: Silty sediments. India: Singarayakonda. Elsewhere: Northeast Ireland, West Scotland, East Scotland, Essex, Biscay and Netherland 35 ; England 31 ; European waters 37 ; Norway, Skagerrak, Oresund, Kattegatt, Baltic Sea and Kieler Buchat 35. the earlier description of Platt and Warwick 31 except for the larger body size. The total body length described was mm and tail length a.b.d in male and in female these were not recorded. The body length of the specimen studied at present was found larger being 1.3mm and the tail length 3.8a.b.d. This is the first record of the species from the Indian waters. 6. Pseudonchus northumbriensis Warwick, 1969 Genus : Pseudonchus Cobb, 1920 Species: Pseudonchus northumbriensis Warwick, 1969 Material examined: 4 males collected from Parangipettai 51-75m and m depths ( ). Male : 60.12± ± ±0.11 ( ) ( ) ( ) Body length mm. Maximum diameter 16-24µm. Cuticle striation commences at posterior edge of amphids. Six minute rounded

6 ANSARI et al. NEMATODES FROM INDIAN WATERS 761 labial papillae. Six short 2-2.5µm and four long 4-5µm cephalic setae. Smooth without any striation and dots. Six rounded lips. Cephalic sense organs represented by six small papillae only. Loopshaped amphids (12-14µm) wide and a single open loop. Buccal cavity with about 14 teeth anteriorly and junction of sections with eight ridged structures subventrally. Oesophagus with indistinct posterior bulb ( µm).Tail conical ( a.b.d.) with unstriated tip. Spicules 21-36µm measured as a curve, with thin ventral alae; large double-jointed precloacal papilla and two ventral papillae on tail each with a pair of stout conical setae. Gubernaculum (10-12µm), parallel to spicules (Fig. 7). the tail length a.b.d. This is the first record of the species from the Indian waters. 7. Epsilonema pustulatum (Gerlach, 1952) Family: Epsilonematidae Steiner, 1927 Genus: Epsilonema Steiner, 1927 Species: Epsilonema pustulatum (Gerlach, 1952) Material examined: Single male collected from Cuddalore SIPCOT at 30-50m depth ( ). Male : Fig.7. Pseudonchus northumbriensis A) entire male B) male head, C) male tail Feeding type: The specimens showed large teeth. According to the classification of buccal cavity by Wieser 34, this species is a predator (2B). Habitat: Sandy sediments. India: Parangipettai. Elsewhere: England 31 ; Northeast England and European waters 35. The specimens examined conformed well with the earlier description of Platt and Warwick 31 except for the smaller body size. The total body length described was 2.4mm and tail length 2.4a.b.d in male and in female these were not recorded. The body length of the specimen studied at present was found smaller being mm and Fig.8. Draconema claparedii A) entire male B) male head, C) male tail Body first with a sharp ventral curvature and then a sharp dorsal curvature giving it a characteristic epsilon-shape and length mm. Maximum body diameter 37-40µm. Cuticle very thick includes erratically arranged vesicles; four cephalic setae (6-10µm) and eight subcephalic setae (10-14µm) are present. Four rows of ventral ambulatory setae (12-14µm) situated just posterior to the dorsal curvature. Circular amphids present in dorsal side (8µm wide). Small very narrow tubular buccal cavity and well developed posterior oesophageal bulb, rounded with cuticular lining. Well-developed ovaries paired, opposed and reflexed situated posterior to the dorsal curvature of the body. Tail conical ( a.b.d.) with unstriated spinneret. Spicules 45-53µm as a curve, strongly arcuate.

7 762 INDIAN J. MAR. SCI. VOL. 44, NO. 5, MAY 2015 Vulva present at 62 65% of the total body length (Fig. 8). Feeding type: The specimen showed a narrow tubular buccal cavity. According to the classification of buccal cavity by Wieser 34, this species is a selective deposit feeder (1A). India: Cuddalore SIPCOT Elsewhere: England 31 ; Arcachon, Biscay, Mediterranean 35. Epsilonema pustulatum generally occurs in sandy beaches and shallower depth 31. In general, the present specimens (two females) corresponded well with the earlier description of Platt and Warwick 31 except for the larger body size. The total body length described was mm and tail length a.b.d. The body length of the present specimen was found greater being mm and the tail length a.b.d. This is the first report of the species in Indian waters. 8. Draconema claparedii (Metchnikoff, 1867) Family: Draconematidae Filipjev, 1918 Genus: Draconema Cobb, 1913 Species: Draconema claparedii (Metchnikoff, 1867) Synonym: Draconema hibernicum (Southern, 1914); Kreiss, 1938 :Draconema armatum (Giard & Barrois, 1874); Filipjev, 1918 :Draconema macrocephalum (Schepotiff, 1907); Filipjev, 1918 :Netochaetosoma claparedii (Mechinikov, 1867); Cobb, 1929 :Netochaetosoma armatum (Giard & Barrois, 1874); Cobb, 1929 : Netochaetosoma macrocephalum (Schepotiff, 1907); Cobb, 1929 :Netochaetosoma hibernicum (Southern, 1914); Cobb, 1929 :Drepanonema claparedii (Mechinikov, 1867); Cobb, 1933 : Drepanonema armatum (Giard & Barrois, 1874); Cobb, 1933 : Drepanonema hibernicum (Southern, 1914); Cobb, 1933 : Netochaetosoma haswelli (Irwin-Smith, 1918); Cobb, 1929 Material examined: Two males collected from Tammenapatanam at 30-50m depth ( ). Male: ( ) ( ) ( ) Body S-shaped and length mm. Cuticle very thick with coarsely striated except on head region; numerous cephalic stilt setae present in dorsal and subventral side of cephalic region; numerous somatic stilt setae present throughout the body. Ω-shaped amphids present in the middle of rostrum. Very small buccal cavity and the posterior oesophageal bulb are well developed with cuticular lining. Numerous ambulatory stilt setae situated posterior to dorsal curvature. Tail more slender and fine tipped (2.3 a.b.d.). Spicules 71-75µm as a curve, arcuate. Gubernaculum short, 20-22µm, rod shaped (Fig. 9). Feeding type: The specimens showed a narrow tubular buccal cavity. According to the classification of buccal cavity by Wieser 34, this species is a selective deposit feeder (1A). India: Tammenapatanam Elsewhere: North Atlantic, Ireland and England 31, 35 ; English Channel, Norway and Mediterranean 35. Draconema claparedii generally occurs in sublittoral, littoral and shallower depths 31. In general, the present specimens (2 males) corresponded well with the description of Platt and Warwick 31 except for the smaller body size. Total body length described was mm and tail length 4.5 a.b.d. The body length of the specimen studied at present was found lesser being mm and the tail length 2.3 a.b.d. This is the first report of the species in Indian waters. 9. Tricoma longirostris (Southern, 1914) Family : Desmoscolecidae Shipley, 1896 Genus : Tricoma Cobb, 1894 Species: Tricoma longirostris (Southern, 1914) Material examined: 16 males and 19 females collected from Singarayakonda m, m depths ( ); Chennai 30-50m, m, >176m depths ( ); Cuddalore SIPCOT 30-50m depth ( ); Parangipettai 30-50m, m, >176m depths ( ) and Karaikkal 30-50m, 51-75m, m, >176m depths ( ).

8 ANSARI et al. NEMATODES FROM INDIAN WATERS 763 Fig.9. Epsilonema pustulatum A) entire male B) male head, C) male tail Male : 19.75± ± ±0.68 ( ) ( ) ( ) Female : 20.18± ± ±0.31 ( ) ( ) ( ) Body length mm in male and 0.7-1mm in female. Maximum diameter 44-49µm in male and 45-57µm in female symmetrical oval desmen, closely spaced with virtually no gaps between them, the number corresponding with the number of body annules. Cephalic setae (21-23µm).Head wedge-shaped, as long as broad, with thickened cuticular walls. Amphids large, kidneyshaped. Tail conical ( a.b.d. in male and 4.3-5a.b.d. in female). Spicules 19-23µm. Ovaries paired and outstretched. Vulva present at 51-58% of body length (Fig. 10). Feeding type: The specimens showed small minute buccal cavity. According to the classification of buccal cavity by Wieser 34, this species is a selective-deposit feeder (1A). Habitat: Sandy, sandy silt sediments. India: Singarayakonda, Chennai, Cuddalore SIPCOT, Parangipettai and Karaikkal. Elsewhere: West Ireland 35 and England 31. the earlier description of Platt and Warwick 31 except for the larger body size. The total body length described was 0.7mm and tail length 4.5a.b.d. The body length of the specimen studied Fig.10. Tricoma longirostris A) entire male B) male head, C) male tail at present was found larger being mm and the tail length a.b.d.in male and in female 0.7-1mm body length and tail length 4.3-5a.b.d. This is the first record of the species from the Indian waters. Discussion In the present study, Comesa cuanensis, Chromaspirina inglisi, Chromaspirina parapontica, Desmadora (Desmadora) schulzi, Metachromadora (Bradylaimus) suecica, Pseudonchus northumbriensis, Epsilonema pustulatum, Draconema claparedii and Tricoma longirostris of free-living marine nematodes belonging to order Chromadorida is reported for the first time in Indian waters from the continental shelf region (southeast coast of India). So far, around 225 species of nematodes have been reported from various regions including estuaries, backwaters, lagoons and mangroves on the east and west coasts of India 13, 15, 18-26, Sajan and Damodaran 14 reported 154 species in the western continental shelf of India. Nevertheless none of these nine species from order Chromadorida have been reported earlier from Indian waters. Therefore, these new recorded species might be useful in future studies especially in the environmental impact assessment (EIA) studies and ecotaxicology studies of Indian waters. Acknowledgements Authors are thankful to Prof. K. Kathiresan, Director, Centre of Advanced Study in Marine Biology for the encouragement and the University authorities for the facilities and Centre for Marine Living Resources and Ecology (CMLRE) of

9 764 INDIAN J. MAR. SCI. VOL. 44, NO. 5, MAY 2015 Ministry of Earth Sciences (MoES), Kochi, Government of India, for helping us with dedicated cruises for collection of benthic samples and financial assistance. References 1. Ansari, K.G.M.T., Manokaran, S., Raja, S., Lyla, P.S & Ajmal Khan, S., Checklist of nematodes (Nematoda: Adenophorea) from southeast continental shelf of India, Checklist, 8(3) (2012a) Schratzberger, M., Warr, K. and & Rogers, S.I., Patterns of nematode population in the southwestern North Sea and their like to other components of benthic fauna. J. Sea Res., 55 (2007) Sajan, S., Joydas T.V. & Damodaran, R., Meiofauna of the western continental shelf of India, Arabian Sea, Estuar. Coast. Shelf Sci., 86 (4) (2010) Soltwedel, T., Metazoan meiobenthos along continental margins: A Review. Prog. Oceanogr., 46 (2000) Vranken, G. & Heip, C., Calculation of the intrinsic rate of natural increase. r m with Rhabditis marina Bastian, 1865 (Nematoda). 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