Marine Arthrotardigrada and Echiniscoidea (Tardigrada, Heterotardigrada) from the Indian Ocean

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Marine Arthrotardigrada and Echiniscoidea(Tardigrada, Heterotardigrada) from the IndianOceanSusanna Grimaldi de Zio a , Maria D'Addabbo Gallo a , Maria Rosaria Morone de Lucia a

& Luciana Daddabbo aa Istituto di Zoologia ed Anatomia Comparata, Università di Bari, via Amendola 165/A,I‐70126, Bari, ItalyVersion of record first published: 28 Jan 2009.

To cite this article: Susanna Grimaldi de Zio , Maria D'Addabbo Gallo , Maria Rosaria Morone de Lucia & LucianaDaddabbo (1987): Marine Arthrotardigrada and Echiniscoidea (Tardigrada, Heterotardigrada) from the Indian Ocean,Bolletino di zoologia, 54:4, 347-357

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Boll. Zool. 4: 347-357(1987)

Marine Arthrotardigrada andEchiniscoidea (Tardigrada,Heterotardigrada) from the IndianOcean

SUSANNA GRIMALDI DE ZIOMARIA D'ADDABBO GALLOMARIA ROSARIA MORONE DE LUCIALUCIANA DADDABBOIstituto di Zoologia ed Anatomia Comparata, Università di Bari,via Amendola 165/A, I-70126 Bari (Italy)

INTRODUCTION

Three new species of marine Heterotardigrada be-longing to Stygarctidae (Arthrotardigrada) and Echin-iscoididae (Echiniscoidea) families are described. Thephylogenetic importance of Stygarctidae was suggestedwhen the first species were described (Schulz, 1951;Renaud-Debyser, 1965), and was confirmed by thediscovery of new genera. The known species belong tothe genera Stygarctus Schulz, 1951; Mesostygarctus Ren-aud-Mornant, 1979; Parastygarctus Renaud-Debyser,1965; Pseudostygarctus Me Kirdy et al., 1976, and Mega-stjgarctides Me Kirdy et al., 1976. Recently, the newfamily Neostygarctidae (Grimaldi de Zio et al., 1987)was instituted. The exoskeleton shape and articulatedclaws of this family, which has only one species N.acanthophorus, suggest it is more primitive than Stygarc-tidae. Stygarctidae, Neostygarctidae and Renaudarcti-dae Kristensen & Higgins, 1984 have yielded the mostimportant data on the relationship between Arthrotar-digrada and Echinoscoidea and within Arthrotardigra-da, among the different families.

The two new species described here that belong tothe genera Stygarctus and Parastygarctus, contribute toour knowledge about Stygarctidae. The new species ofthe genus Anisonyches demonstrates that the relationshipbetween Arthrotardigrada and Echiniscoidea should bere-examined.

ABSTRACT

Three new species of marine Heterotardigrada, Arthrotardigradaand Echiniscoidea from a sandy shore of the Island of Mauritius,are described. They are two species of Stygarctidae: Parastygarctusrenaudae and Stygarctus lambertii, and a species of Echiniscoididae:Anisonyches mauritianus. The evolution of the cephalic plate in P.renaudae during post-embryonal development is somewhat peculiar.A. mauritianus has an evident medial cirrus and sense organs on thefirst three pairs of legs but both the clavae and the sense organs onthe fourth pair of legs are indistinguishable.

KEY WORDS: Marine Tardigrada; Heterotardigrada.

AKNOWLEDGEMENTS

Our acknowledgements to Prof. Franco Lamberti who collectedfor us a sample of sand on the Island of Mauritius. We thank alsoProf. Jeanne Renaud Mornant for her critical reading of themanuscript and for valuable advice.

(Accepted 23 October 1987)

MATERIAL AND METHODS

Specimens of the three new species were found in a sample ofsand collected by Prof. F. Lamberti on the Island of Mauritius inMay 1985 from the «Belle Mer» beach which faces a coral-reef. Inaddition to the above-mentioned species were: Halechiniscus remaneiSchulz, 1955, and Florarctus hulingsi Renaud-Mornant, 1976. On thesame beach, in May 1986, no Stygarctidae, but only Florarctushulingsi and Halechiniscus remanei were found. This confirms thatsingle data are not reliable for the study of the ecology of intersti-tial species, particularly Tardigrada, or for the ecological definitionof a species. In this paper, the words «interstitial» and «intertidal»are used only to indicate the kind of habitat where the species havebeen found: in the sand of the intertidal zone. A sample of 1000 ccof sand was collected on the shore line. It was washed in fresh-water and filtered through a 64 ßm mesh sieve. Specimens collect-ed were examined both living and fixed in TAF. Specimens weremounted in Polyvinyl-lactophenol.

RESULTS AND DISCUSSION

Family STYGARCTIDAE Schulz, 1951emended Me Kirdy et al., 1976.

Diagnosis: Arthrotardigrada with a complete set ofcephalic appendages. Anterior clavae either elongatedor hemispherical. Dorsal cuticle forming five thicken-ings: a cephalic plate, three body plates and a caudalplate; ventral plates sometimes present. Feet non-digi-tate; in adults: either four claws on each leg, the centralpair with long filaments, or three claws on each leg, allwith a short dorsal accessory spine, or four claws on

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348 S. GRIMALDI DE ZIO,. AL D'ADDABBO GALLO,. M. R. MORONE DE LUCIA* L. DÁDDABBO

the first three pairs of legs and two claws on the fourthleg, ail with a short accessory spine; claws attachedwith dorsal basal membrane. Bulb-shaped papilla onthe fourth leg.Type genus: Stygarcfus Schulz, 1951.

Genus Parastygarctus Renaud-Debyser, 1965Diagnosis: Stygarctydae with body plates extending

laterally into one or two acute processes. Head dividedinto two parts: the antero-ventral part bearing a mouthcone and internal cirrus;, the deeply incised posteriordorsal plate features external cirri with secondaryclavae, lateral cirri with primary clavae and the un-paired medial cirrus. AH cirri articulated at the base;,primary and secondary clavae of the same shape, gener-ally elongated. Articulated cirri E inserted on the later-al processes of the caudal plate. Ventral plates some-times present. Buccal apparatus as in Sfygarctus. Eachleg with four claws, the central pair of which with along accessory filament. Cuticle punctated.Type species: Parastygarctus higginsi Renaud-Debyser,1965.

Parastygarctus renaudae n . sp.

(Table 1, Figs. 1-2)

Diagnosis: Parastygarctus with lateral cephalic lobesventrally' bent with a prominent dorsal elbow. Bothprimary and secondary clavae pedunculated; Interrneta-meric oval and smooth dorsal plates; three ventralplates; two organdíes (small cavity and flap) on eachventral plate. Dorsal body plates extending laterallyinto one sharp, ventrally bent process.

Type locality. Island of Mauritius, «Belle Mer» beach,20°ll' S, 57° 16' E. Intertidal zone, fine and well sortedsand (105 ßm) with Foraminifera.

Holotypei female, in authors' collection, slide Pa-Ma,3/85.

Deriva fio nominis: Parastygarctus renaudae is dedicatedto Prof. Jeanne Renaud-Mornant of the Museum Na-tional d'Histoire Naturelle, Paris, France.

Holotype description

Body length, from anterior rim between internalcirri to posterior end of caudal plate, 126 ßm. Dorsalcuticle forming three body plates between the cephalicand caudal plates. Head divided into two parts: theantero-ventral part bearing internal cirri (16 ßm); thedorsal part with external cirri (21 ßm) and secondaryclavae (14 ßm). The dorsal part extending laterallyinto two arms bearing lateral cirri (29 ßm) andprimary clavae (17.4 ßm). Medial unpaired cirrus (23ßm) on an evident dorsal prominence. Primary andsecondary clavae of the same shape consisting of apeduncle with a basal inner ring-shaped support (1ßm) and an enlarged terminal portion. Lateral arms ofthe cephalic plate ventrally bent at about half of their

length, where an evident elbow is present. Ventrallyto the insertion of the primary clava and lateral cirrus,a stout and short spike (4 ßm) arising from the distalend of each arm. Cephalic plate width, lateral armsincluded, is 79 ßmr whereas the central portion is only44 ßm. Within the head a wide cerebron innervatingall cephalic appendages and overlapping the pharyngealtube is visible. Mouth opening in the ventral part ofthe head; buccal tube length 50.4 ßm, small pharyngealbulb (13 ßm) at the second body plate level.

Long protrusible buccal cone, connected with thebuccal tube at the level of the stylet sheath and movedby a pair of tape-like muscles arising from the internalcaudal ridge of the cephalic plate and ending with atendon-like thin portion on the stylet sheaths; long thinstylets without furca, but with a very large semilunarapophysis, three short, stout placoids with strong pro-cesses which are antero-lateral in the two latero-dorsal,but antero-ventral in the medial one. The latter work-ing as internal stylet support: the two ends of eachsemilunar stylet apophysis articulating with them, theexternal ones with the antero-lateral supports passingunder them, the medial ones levering on the antero-ventral support.

Three identical body plates measuring 62 X 16 ßm, 70X 123 ¿im-and 64.4 X 17 ßm respectively. Each one ofthem laterally protruding with one conical spike foreach side, .measuring 19.4 ßm, 20 ßm and 21 ßmrespectively. The spikes, as well as the lateral arms ofthe cephalic plate, are ventrally bent at a right angle.Two intermetamerical smooth or finely punctated,oval, dorsal plates delimited by a prominent coarselydotted ridge, are located between the body plates. Cau-dal plate with two large dorso lateral outgrowths fromwhich cirri E (31 ßm) arise. The latter consisting of ascapus (4 ßm), an accordion-pleated portion (7 ßm)and a flagellar part (20. ßm). Two ampullar seminalreceptacles extending ventrally with their ducts to eachside of the gonopore are present in the lateral out-growth of the caudal plates. Three ventral plates, corre-sponding to the three dorsal body plates, are present. Asmall cavity followed : by a thin cuticular flap, in eachof the three ventral plates ; : j • '

Gonopore (3.4 ßm) delimited byi six cells surround-ed by a second circle of a dozen cells and flanked bythe openings of the two seminal receptacle •' ducts.Anus-gonopore distance 83 ßm. Anus (8.4 ßm) co-vered by two longitudinal cuticular folds. Four typicalclaws, the medial of which with a long filament, foreach leg.

Post-embryonal development

First-stage larvae are smaller than adults and haveonly two claws, which correspond to the central onesof adults; neither anus nor gonopore is present. Thecephalic plate, which differs in the different stages, isnot only smaller in the first-stage larva, but has also

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INDIAN OCEAN TARDIGRADA 349

TABLE I - Parastygarctus renaudae; measurements (in ßm) of larvae and adults

LcWcbWI aaSmCiCeCICICIIICICEP4AGA-GsLbWSIS2S3

HOLOTYPE

126794445

423162129171431

683

5013192021

range

67-9545-5328-34

11-177-129-16

12-188-106-8

27-452-4

4-107-118-10

firstmean

82493038

15101214

97

363

2710898

stage

a

7.92.623

2.91.62 22 20.90.7650.6

1.91.40.7

LARVAE

n°

111010

101111101011108

11888

range

90-14658-8425-48

2-412-239-16

12-229-30

11-178-13

22-484-74-9

34-458-11

10-259-25

11-25

second stagemean

108633545

320121620141031

57

389

151515

a

14.92&5.6

0.62.9232.54 21.41.46.41.11.4

5.82.14 34.442

n°

181615

11191719191919191715

32999

range

112-16864-9336-50

3-89-3511-2416-3117-4114-2511-1814-634-87-142-36-17

48-6711-1617-3117-3417-34

ADULT

mean

133794150

425152128191435

6949

5013222222

FEMALES

a

12.76.14.9

1.1532.6334 51.9\&7.611.80.81.68.61.73 2333 3

n°

595858

385560595859595559564949179

494849

25pm

Fig. 1 - Parastygarctus renaudae female. A. dorsal view; B. ventral view: f. flap; c. cavity; C. cephalic plate of first stage larva; D.pharingeal apparatus.

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350 S. GRIMALDI DE ZIO, M. D'ADDABBO GALLO, M. R. MORONE DE LUCIA, L. DADDABBO

J-

Of.,-is:i>. t2>» v

x\<

Fig. 2 - Parastjgarctus renaudae. A. first stage larva; B. ventral organdíes: f. flap; c. cavity. (14 mm = 10 ßm).

two very short and straight lateral arms that bear pri-mary clava and lateral cirrus. These represent about381 of the total plate width. The terminal portion,which in the adults is ventrally bent with a terminalspike, is missing. Only in one specimen was there asmall terminal spike (0.6 fim). Both primary and se-condary clavae consist of a peduncle and an enlargedend, and are more evident and smaller than in adults.The lateral processes of the body plates are short andventrally bent. Intermetamerical plates are not always

evident. In all the specimens, the fourth pair of legpapilla is present, whereas in only one specimen was aventral cavity in the third ventral plate detected.

Second stage larvae are very similar to adults: thecephalic plate is in fact practically the same and thelateral arms represent 452 of total head width. At aboutone-half of their length, the arms bend ventrally in anelbow shape. A small spike is present at their end. Thelateral processes of the body plates are longer than inthe first-stage larvae. Intermetamerical dorsal smooth

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plates are present and ventral cavities with correspon-dent flaps are also present. Four claws on each leg andanus are present. The gonopore is missing.

The outline of the post-embryonal development ofP. renaudae is as in the majority of Arthrotardigrada: afirst stage with two claws, with neither anus nor gono-pore: the two claws corresponding to the central onesof the second stage larva and adult; a second stagewith four claws and anus, but without gonopore (Ber-tolani et al., 1984). The body length increases duringdevelopment and the three lateral spine lengths growfrom the first stage to the adult stage. They are 7.7 [im,8.6 /im and 8.5 ßm respectively in the first stage,whereas in the second stage they are 15.2 fim, 15.1 ßmand 15.4 //m, respectively and in adults, 21.7 /¿m, 22/¿m and 22.3 /an, During development, the cephalicsense organs also increase in length.

The most interesting aspect of the development isthe evolution and transformation of the cephalic plate.It consists of a central body and two arms which, inthe first stage larva are short and straight, withouteither an elbow or a terminal spike. In this stage, thearms represent 382 of the total plate width. In thesecond stage, arm length is longer, one elbow isevident and a small spike is present in the terminalportion. In this stage, the arm length represents 45Z oftotal plate width. In the adult the arms are much longerthan in the previous stages: they are bent almost at aright angle, with a marked elbow, and represent 50? oftotal head diameter. This lengthening of arms, which ismuch more relevant than the increase of the centralpart of the plate, is correlated with the need for theadult to improve the functionality of its sense organsso as to have a better mobility in the marine medium.

Remarks

Although P. renaudae shows evident affinities with P.sterreri Renaud-Mornant, 1970, it has peculiar featuresthat distinguish it from the specimens of the speciesfound in the Mediterranean (Renaud-Mornant, 1970)and in the Galapagos, Bermuda (Me Kirdy et al.,1976), Madagascar (Renaud-Mornant, 1979) andAntilles (Renaud-Mornant, 1984). The most evidentpeculiarity is the shape of the cephalic plate with itstwo ventrally bent elbow-shaped lateral arms. A lessevident elbow is also present in P. biungulatus MoroneDe Lucia et al., 1984, and a slight prominence can alsobe observed in P. higginsi Renaud-Debyser, 1965.

The spike ending of the arms, is ventral and stout inP. renaudae, whereas in P. sterreri P. higginsi and P.biungulatus, it is long, sharp and dorsal. The cephalicplate of the first-stage larva is deeply indented in theAntilles specimens (Renaud-Mornant, 1984), whereasin P. renaudae the cephalic lobes become more evidentin the adults.

Primary and secondary clavae consist of two parts: aproximal cylindrical one and a distal enlarged one; in

the larval stages the distinction is much more evident.This distinction is not evident in adults of either P.sterreri or P. higginsi, where the clavae are club-shaped.Renaud-Mornant (1984) observed this clavaeevolution during the post-embryonic development alsoin P. sterreri; in adults of P. biungulatus the primary andsecondary clavae shape is that of the first-stage larvaeof P. sterreri and P. renaudae. If this clava shape weretypical of larval stages in all the species of the genusParastygarctus, P. biungulatus would show two larvalcharacteristics, namely two claws and the clavae shape.The pharyngeal bulb is in the exact position of thedrawing of Stygarctus bradypus Schulz, 1951, wherethree placoids with strong apophysis, (two lateral and amedial one) are evident. The apophysis are analogousto the stylet support of all other Arthrotardigrada thathave two supports external to the bulb.

The lateral processes, which are 50 ßm long in P.sterreri and sinuous, are shorter (21-22 fim) andventrally bent in P. renaudae. In P. sterreri there are nointersegmental plates, whereas both in P. renaudae andin P. biungulatus they are always evident.

In P. renaudae three structures, the function of whichis unknown, were observed: in each ventral plate thereis a simple medial cavity followed by a flap, which insome cases is inserted in it. When this flap is inserted,small folds are evident by the side. It is not clear ifthese structures could be used to change the length ofthe ventral plates, or if they could be connected withinternal glands which, however, were never observed.

These structures are present in adult females and atall larval stages. They might be present also in males,however we did not examine any male specimens. It ispossible that they are present in all Stygarctidae in adifferent shape; in fact Stygarctus lambertii shows evidentventral pores, and similar structures are found in P.sterreri, P. biungulatus and Mesostygarctus intermedius Ren-aud-Mornant, 1979. We re-examined old slides of thelatter three species, however the specimens in poly-vinyl-lactophenol are no longer clear, although poresare recognizable and we are sure that they are presentin all the family.

Ecology

Intertidal interstitial species, in coralline sand (105¿urn) with Foraminifera 15 m depth. 61 maturefemales, 19 second stage larvae, 11 first-stage larvaewere found. Males not found.

The following key of the genus Parastygarcuts isproposed.

1 Adult Parastygarctus with two claws . . P. biungulatus— Adult Parastygarctus with four claws . . 22 Body plates with two lateral

expansions P. higginsi- Body plates with only one lateral

espansion 3

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3 Cephalic plate with straight lateralprocesses and secondary club-shapedclavae P. sterreri

- Cephalic plate with lateral processesventrally bent and I and II clavaepedunculated P. renauda

Genus Stygarctus Schulz, 1951

Diagnosis: Stygarctidae with funnel-shaped lateralprocesses; legs with four claws, the central pair ofwhich with long filaments. Secondary clavae elongated,primary clavae either elongated or globular.Type species: Stygarctus bradjpus Schulz, 1951.

Stygarctus lambertii n . sp.(Table 2, Figs. 3-4).

Diagnosis: Stygarctus with a globular primary clava,three microspines on the two first funnel-shaped later-al processes; two accessory dorsal processes fromsecond body plate; three ventral plates; unpaired ven-tral pores on first and second ventral plates.

Type locality: Island of Mauritius, «Belle Mer» beach,20"ll' S, 57° 16' E. Intertidal zone, fine and well sortedsand (105 ßm), with Foraminifera.

Holotype: adult female. In authors' collection, slideSty-Ma, 2/85.

Derivatio nominis: Stygarctus lambertii is dedicated toProf. Franco Lamberti of the «Laboratorio di Nemato-logia) (C.N.R.) Bari, Italy.


Body length 102 ßm, from anterior rim betweeninternal cirri, to posterior end between caudalprocesses; body plates dimension, between funnel-shaped lateral outgrowth, 39 X 15 ßm, 42 X 13 ¿urnand 40 X 16 ßm, respectively. All plates having avariable number of longitudinal and irregular ridgesparallel to the body axis. Ventrally and dorsally punc-tated cuticle.

Cephalic plate deeply indented. Anterior lobes withthe internal cirri (112 jtim), globular, pedunculatedclavae (5.6 ¿um) and lateral cirri (13.4 /zm) on thelateral lobes, latero-ventrally flaring and forming fun-nel-shaped processes. Ventral lobes, bent at right angle,extending to each side of the mouth opening, fromwhich external cirri (10.6 ßm) and sausage-likepedunculated secondary clavae (112 /im) arise. Medialcirrus (13.4 /im) dorsally inserted in a conical process.

Intermetamerical smooth plates with a prominentrim, present. The latter with a marked medial narrow-ing, making it appear as if divided into two plates.Three microspines (2 ßm) on the first and secondfunnel-shaped lateral processes. Two long dorsal spines(17 //m) with a forked end (7.3 ßm) arising from thecaudal rim of the second body plate. Two small, simple

dorso-lateral processes from the caudal ridge of thefirst (2 jUm) and second (3 ßm) dorsal body plates.

Three ventral plates, corresponding to the dorsalbody plates. Each plate with a median thickening witha sinuous anterior ridge and two lateral lobes formingthe three pairs of funnel-shaped lateral processes.

A ventral pore (1.7 ßm) in the caudal part of thefirst ventral plate; a second pore, smaller than the first(1.12 /im) in the middle of the second plate. Bothpores continuing inside the body with a short tube.

Caudal plate with a pair of conical lateral outgrowthswith an accessory point delimited by a circular furrowand a pair of latero-caudal membranaceous expansionssurrounded by a thin lamella. Between these two lateralprocesses, a cirrus E (24.6 ßm) with a strong articulat-ed portion is present. Posterior part of the caudal plateelongating with two caudal spikes (15.7 ßm) with amembranaceous medial ridge.

Anus opening (6.7 ßm), between the abovementioned caudal spikes, covered by two cuticularfolds. Telescoping limbs, the fourth of which morestiffer than the others. A papilla (2.4 ßm) similar tothe primary clava on the fourth pair of legs.

Rosette-like gonopore surrounded by six smallplates. Small, pear-like seminal receptacles with curledducts, opening laterally to the gonopore.

Description of males

Males smaller (90-100 ßm average) than females(100-110 ßm average). Sexual dimorphism limited tothe gonopore, which is simple and circular, and co-vered with a cuticular crescent-shaped fold, 1-2 ßmfrom anus.

Postembryonic development

One first-stage larva, 55 ßm long, was found. It issmaller and simpler than the adult. All sense organs areshorter than in the adult, but proportional to the bodysize. Intermetamerical plates are absent. The two dorsalspines of the second body plates end in a single point.Caudal processes, anus, genital apparatus and thereforegonopore, are absent. Only two claws, with long fila-ments are present on each leg; they correspond to thecentral pair of the adult. Ventral pores do not exist.

Three second-stage larvae were found. Their mor-phology and size are practically the same as the adults.Dorsal spines are longer than in the first-stage larvaand have two terminal short points at an acute angle.Intermetamerical plates and caudal processes are pre-sent. The latter are shorter than in adults. They havefour claws and an anus, but lack gonopore.

Stygarctus lambertii development seems to be similarto that of S. bradypus as described by Renaud-Mornantand Anselme-Moizan (1969) but it is simpler becauseonly two larval stages were observed: the first corre-sponding to the second stage of S. bradypus, with dorsalshort, not forked spikes, two claws, no caudal pro-

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TABLE II - Stygarctus lambertii: measurements (in p.m) of larvae and adults

LcWmCiCeCICICIIIC1dSdsFCEP4AGA-GcPIvPIIvP

I stage

552510999487

221

LARVAE

6218777648

11

2012

8

II stage

6431

899

1147

14

1827

3

9637

9

135

13

2325

13

HOLOTYPE

10237131111136

11177

242734

1611

range

69-10628-42

9-159-136-11

10-174-6

10-1411-203-7

19-251-36-82-33-8

11-171-21-2

femalesmean

933412109

125

12164

222735

14

G

113422131.92.10.91231.420.5

15.8021.62.4

n'

161410157

15141515111413141413161616

ADULTS

range

76-11227-3710-137-1599-144-68-17

14-203-6

17-252-36-82-31-2

11-181-21

malesmean

933412119

125

12165

212731

14

a

12.82.81.0422

1.6OS2.61.91.12250351.070.50.723

n°

1111101010111111119

111188

10111111

cesses and neither anus nor gonopore; the secondcorresponding to the third stage of S. bradypus, withdorsal forked processes, caudal appendages, anus andfour claws on each leg. The next stage is the adultstage. The lack of larvae corresponding to the firststage of S. bradypus may be due either to the small sizeof the sample or to the difficulty of finding specimenssmaller than 55 fim, which is the length of the smallestlarva found and which we classified as first-stage (Ber-tolani et ai., 1984).

Remarks

Stygarctus lambertii shows strong affinities with S.gourbaultae Renaud-Mornant, 1981. The most impor-tant differences between these species are: the shape ofprimary clava, the presence of a short peduncle in thesecondary clava, pores in the ventral plates; the latterwith a median thickening whose anterior ridge can beeither sinuous or straight. The microspines on the la-teral funnels are three instead of four and five as inS. gourbaultae; the latter has the caudal ridge of the dorsalplates more indented than does S. lambertii. The dorsalspines of the Mauritius species have small terminalbranching similar to S. bradypus. Differences are evi-dent also in the caudal plate whose lateral processes aremore stout in S. lambertii than in all other species ofStygarctus.

The meaning of the ventral pores is unknown, but,since we have observed similar structures in such othergenera as Parastygarctus and Mesostygarctus, they couldbe a very common feature in this family.

Ecology

S. lambertii is an interstitial intertidal species of coral-line, fine and well sorted sand (105 /zm). Sixteen fe-males, eleven males, three second-stage larvae (pre-adults) and a first-stage larva were found.

The following key of the genus Stygarctus is pro-posed:

1 Dorsal spines present 2- Dorsal spines absent 5

2 Comb-like processes on the funnel-shaped lateral expansions 3

- No comb-like processes 43 Comb-like processes with five

microspines on the first funnel andfour on the second funnel S. gourbaultae

- Comb-like processes with three mi-cro-spines on the first two lateral fun-nels S. lambertii

4 No comb-like processes, but micro-spines along the ridge of the bodyplate S. spinijer

- Neither comb-like processes, nor mi-cro-spines on the body plates S. bradypus

5 Sense organs on the legs S. abornatus- No sense organs on the legs S. granulatus

Although S. spinifer Hiruta, 1985 has been includedin the above key, it has cephalic plate whose morpho-logy is more of the Parastygarctus type than of the Sty-garctus type whereas its dorsal spines and caudal plate

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Fig. 3 - Stygarctus lambertii female. A. dorsal view; B. ventral view.

are typical of Stygarctus. Thus, S. spinifer appears to beequidistant between the genus Parastygarctus and all thespecies of the genus Stygarctus. Furthermore, it has nu-merous spines on all the plates as does NeostygarctusGrimaldi de Zio et al., 1982. The foregoing featuresindicate that the systematic position of this species de-serves more detailed studies, which might result eitherin the institution of a new genus or in the unificationof Parastygarctus and Stygarctus as sub-genera in onegenus.

Family ECHINISCOIDIDAE Kristensen & Hallas.1980.

Diagnosis: unplated marine Echiniscoidea Marcus,1927 without toes. Papilla cephalica dome-shaped orindistinct. Other cephalic appendages and legappendages small (reduced). Lateral cirri and cirri Esimilar. Papular fourth leg appendage as the clava.

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TABLE III - Anisonyches mauritianus adult females.

Fig. 4 - Stygarctus lambertii female, vp. ventral pores. (14 mm = 1 0¿im).

Genus Anisonyches Pollock, 1975.(emended).

Diagnosis: Echiniscoididae with four claws on each ofthe first pairs of legs and three claws on the fourth pairof legs. Medial cirrus sometimes present.

Type species Anisonyches diakidius Pollock, 1975.

Anisonyches mauritianus n. sp.(Table 3, Fig. 5)

Diagnosis: Anisonyches with medial cirrus, mouthterminal and sense organs on the first three pairs oflegs (PI, P2, P3). Clavae and fourth pair of legs papil-la (P4) indistinguishable.

Type locality: Island of Mauritius, «Belle Mer» beach,20°ll' S, 57°16' E. Intertidal zone, fine and well sortedsand (105 fJ.m) with Foraminifera.

Holotype: female, slide An-Ma 1/85, in authors,collection.

Derivatio nominis: mauritianus = from the Island ofMauritius.


Worm-like body with conical cephalic region. Totalbody length 150 ßm, maximum body width at 502 of

LbWmCiCeCICPIP2P3CEA-G

150311.5444333610

141311.544633

120

2436

3348

120

3335

9718153363336

20/Jm

Fig. 5 - Anisonyches mauritianus female. Dorsal view and claws.

body length, 31 ßm. Mouth opening terminal, flankedby dorsal internal cirri (4 ßm) and ventral externalcirri (4 ßm); lateral cirri (5 ¿im) 23 /im back from themouth. Medial cirrus (1.5 ßm) equidistant betweeninternal cirri and lateral cirri. No primary clavae. Smallbrown kidney-shaped eye spots evident at the lateralcirri level. Cirri E (6 ßm) with evident inner fila-

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ment. All cephalic appendages and cirri E consistingof a basal cilindrical portion (502) and a conical ter-minal spike (502). In cirri E the distinction is markedby a rifrangent zone.

Buccal tube 30 /zm long, stylets with small rectangu-lar furca (20 ßm) with stylet sheaths 20 (im long; nostylet supports. Pharyngeal bulb 10 ßm wide, withthree placoids (6 /im).

Stubby legs with sexile claws. Claws very large witha very strong uncus which is similar to the uncus of theclaws of Parastygarctus, and with two stout basal spurs.All claws connected with legs with a dorsal contractilemembrane which allows the claws to recline complete-ly on the tarsus. The innermost claws shorter than theoutermost. The first three pairs of legs with a shortsense organ (PI, P2, P3) 3 jUm long. No sensoryorgan (P4) on the fourth pair of leg.

Rosette-like female gonopore (5 ßm). Two seminalreceptacles consisting of a small terminal ampoul andof a long curled tube opening ventrally and laterally tothe gonopore. Anus-gonopore distance 10 ¿urn.

Five adult females were found.

Remarks

Anisonyches mauritianus is very similar to A. diakidius,but differs from it in the shape of the head, which isconical with the mouth opening terminal, in havingno primary clavae and P4, and in having medial cirrusand sensory organs PI , P2 and P3.

The presence of the medial cirrus, as well as itsabsence, is not a very important character because itcan be present also in A. diakidius: in fact we haveobserved it in all the specimens of a Mediterraneanpopulation and it is so small (1-2 ß\m) that it couldhave been overlooked in the past. All the cephalic cirriare short and appear very similar to the cirri of Coro-narctidae Renaud-Mornant, 1975.

Much more important is the absence of clavae. Noevidence of clavae can mean either that they do notexist or, more probably, that they are so small or flatas to be indistinguishable. In A. diakidius, clavae arealways clearly evident. It is not by chance that the P4is also absent or, if present, not visible. In fact, the twosense organs have frequently the same shape and func-tion (Kristensen, 1981).

Anisonyches is a very interesting genus and its syste-matic position needs to be discussed. In fact, it seemsclosely related either to Stygarctidae, because of theuncus morphology, or to Coronarctidae, because theshape of cephalic sense organs. It seems to be closer toArthrotardigrada than to Echiniscoidea. The differentnumber of claws in the different legs is a characteristicalso of Stygarctidae. The presence or absence of medialcirrus is not important because also in Echiniscoides itcan appear as an ancestral character (Kristensen &Hallas, 1980).

To date, we have had too few elements to be able to

change the systematic position of Anisonyches, but tak-ing into account also the morphology of the seminalreceptacles, this genus seems to be strongly related toArthrotardigrada.

CONCLUSIONS

The three new species of Heterotardigrada (Arthro-tardigrada and Echiniscoidea) of the Island of Mauri-tius seem to be phylogenetically interesting. The phar-yngeal apparatus of P. renaudae shows a peculiar mor-phology, and there is also a relationship between styletsand placoids which, previously described only in S.bradypus (Schulz, 1955), appears to be common withinthe Stygarctydae, but peculiar to this family.

Another interesting element, common to the twospecies described here, is the presence of the unpairedventral pores that in P. renaudae and S. lambertii havedifferent shapes, but probably the same function. Asvery similar ventral pores exist also in Mesostygarctus, itis possible that they could be present in all the generaof the family, and they could be analogous to the ven-tral pores observed by Kristensen (1984) in someHalechiniscidae.

Another important feature is the presence of ventralplates in both P. renaudae and S. lambertii. This plesio-morphic character, which is present also in Renaudarc-tidae (Kristensen & Higgins, 1984) and in someEchiniscoidea (Kristensen, 1987), highlights the phy-logenetic position of the Stygarctidae family at the baseof the two orders of Heterotardigrada.

Lastly A. mauritianus is a very interesting speciesbecause it prompts studies on the affinity of the genusAnysonikes with Arthrotardigrada, mainly Stygarctidaeand Coronarctidae, in order to establish a more correctsystematic position for the genus.

REFERENCES

Bertolani R., Grimaldi de Zio S., D'Addabbo Gallo M., Morone DeLucia M. R, 1984 - Postembryonic development in Heterotardi-grades. Monitore zool. ital. (N. S.), 18: 307-320,

Grimaldi de Zio S., D'Addabbo Gallo M., Morone De Lucia M. R.,1982 - Neostygarctus acanthophorus n. gen., n. sp. nuovo Tardigra-do marino del Mediterraneo. Cah. Biol. mar., 23: 319-323.

Grimaldi de Zio S., D'Addabbo Gallo M., Morone De Lucia M. R.,1987 - Adaptive radiation and phylogenesis in marine Tardigra-da and the establishment of Neostygarctidae, a new family ofthe Heterotardigrada. Boll. Zool., 54: 27-33.

Hiruta S. I., 1985 - A new species of marine interstitial Tardigradaof the genus Stygarctus Schulz from Hokkaido, Japan. Spec.Pubis. Mukaishima Mar. biol. Stat.: 127-129.

Kristensen R. M., 1981 - Sense organs of two marine Arthrotardi-grades (Heterotardigrada, Tardigrada). Acta Zool., 62: 27-41.

Kristensen R. M., 1984 - On the biology of Wingstrandarctus coral-linus nov. gen. et spec., with notes on the symbiotic Bacteria inthe subfamily Florarctinae (Arthrotardigrada). Vidensk. Meddrdansk naturh. Foren., 145: 201-218.

Kristensen R. M., 1987 - Generic revision of the Echiniscidae(Heterotardigrada) with a discussion of the origin of the family.In: R. Bertolani (ed.), Biology of Tardigrades. Selected Sympo-sia and Monographs U.Z.I., 1, Mucchi Modena, pp. 261-335.

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Kristensen R. M., Hallas T. E., 1980 - The tidal Genus Echiniscoidesand its variability, with erection of Echiniscoididae fam. n.(Tardigrada). Zool. Scr., 9: 113-127.

Kristensen R. M., Higgins R., 1984 - A new family of Arthrotardi-grada (Tardigrada: Heterotardigrada) from the Atlantic Coast ofFlorida, USA. Trans. Am. microsc. Soc., 103: 295-311.

Mc Kirdy D. J., Schmidt P., Mc Ginty-Baily M., 1976 - InterstitielleFauna von Galapagos. XVI. Tardigrada. Mikrofauna d. Meer-esbodens, Mainz, 58: 1-43.

Marcus E., 1927 - Zur Anatomie und Ökologie mariner Tardigra-den. Zool. Jahrb. (Abt. Syst.), 53: 487-558.

Morone De Lucia M. R., Grimaldi de Zio S., D'Addabbo Gallo M.,1984 - Description of Parastygartus biungulatus n. sp. and hypoth-esis of phylogeny in the Stygarctidae family (Heterotardigrada:Arthrotardigrada). Oebalia (N.S.), 10: 85-94.

Pollock L. W., 1975 - Observations on marine Heterotardigradaincluding a new genus from the western atlantic ocean. Cah.Biol. mar., 16: 121-132.

Renaud-Debyser J., 1965 - Parastygarctus higginsi n.g., n.s. Tardi-grade marin intestitiel de Madagascar. C. R. Acad. Sci., Paris.260: 955-957.

Renaud-Mornant J., 1970 - Parastygarctus sterreri n.sp. Tardigrademarin nouveau de l'Adriatique. Cah. Biol. mar., 11: 355-360.

Renaud-Mornant J., 1975 - Deep-sea Tardigrada from the «Me-teor» Indian Ocean Expedition. «Meteor» Forsch.-Ergebnisse,ser. D., 21: 54-61.

Renaud-Mornant J., 1976 - Le genre Florarctus Delamare Deboutte-ville et Renaud-Mornant 1965, en Mediterraneè; description dedeux especes nouvelles (Arthrotardigrada). Bull. Mus. natl. Hist.nat., Paris, 369: 325-333.

Renaud-Mornant J., 1979 - Tardigrades marins de Madagascar. II.Stygarctidae et Orellidae. III. Considerations ecologiques gener-ales. Bull. Mus. natl. Hist, nat., Paris, 1: 339-351.

Renaud-Mornant J., 1981 - Stygarctus gourbaultae n.sp. un nouveauTardigrade marin (Arthrotardigrada) de la Guadeloupe. Bull.Mus. natl. Hist. nat., Paris, 3: 175-180.

Renaud-Mornant J., 1984 - Nouveaux Arthrotardigrades des An-tilles. Bull. Mus. natl. Hist. nat., Paris, 6: 975-988.

Renaud-Mornant J., Anselme-Moizan M. N., 1969 - Stades lar-vaires du Tardigrade marin Stygarctus bradypus Schulz et posi-tion systematique des Stygarctidae. Bull. Mus. natl. Hist. nat.,Paris, 41: 883-893.

Schub E., 1951 - Über Stygarctus bradypus n.g., n.s., einen Tardigra-den aus dem Küstengrundwasser und seine phylogenetische Be-deutung. Kieler Meeresforsch., 8: 86-97.

Schulz E., 1955 - Studien an marinen Tardigraden. Kieler Meeres-forsch., 11: 73-79.

Abbreviations:

LcWcbWbWlaaSiCmCeCICICIII ClSIS2S3dSdsFCEPlP2P3P4cPI vPII vPAGA-GVsLbW

total lengthcephalic plate widthwidth of the central portion of the cephalic platebody widthI length of the two arms of the cephalic platearm spikeinternal cirrimedial cirrusexternal cirrilateral cirriprimary clavaesecondary clavaelateral process of the first toracic platelateral process of the second toracic platelateral process of the third toracic platedorsal spikesforked end of the dorsal spikescirri Efirst leg papillasecond leg papillathird leg papillafourth leg papillacaudal processesfirst ventral poresecond ventral poreanus lengthgonopore widthdistance anus-gonoporeventral cavity widthstylet lengthbulb width

All the measurements are in «m.

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Documents

Marine Arthrotardigrada and Echiniscoidea (Tardigrada, Heterotardigrada) from the Indian Ocean