Canadian Translation of Fisheries and Aquatic Sciences

No. 5069

On the biology of the marine heterotardigrade Tetrakentron synaptae

R.M. Kristensen

Original title: Zur Biologie des marinen Heterotardigraden Tetrakentron synaptae

In: Helgol. Meeresunters. 34(2): 165-177, 1980

Original language: German

Available from: Canada Institute for Scientific and Technical Information National Research Council Ottawa, Ontario, Canada R1A 0S2

1984

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On the Biology of the Marine Heterotardigrade Tetrakentron synaptae.

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Helaolânder Meeresuntersuchungen, Vol.34, No.2 (1980); pp.165-177.

On the Biology«of the Marine Heterotardiqrade

Tetrakentron synaptae.

By R.M. Kristensen.

Institut for Sammenlianende Anatomi; UniversitetsParken 15, DK-2100 Kobenhavn (Kopenhagen) 0, Denmark.

ABSTRACT: On the biology of the 'marine heterotardigrade Tetrakentron synaptae. The lite cycle of Tetrakentron synaptae Ctienot, 1892, a tardigrade closely associated with the sea cucumber Leptosynapta galliennei Herapath, was investigated in the littoral zone at Roscoff (France). Eqgs and juveniles were found only in June and July, adults only from Nlay to October. 'There are vagile males and stationary dwarf nialt.s. The dorsoventraIly Ilaltimed body, an enlarged slimy epicuticle in females and dwarf males, the full set of claws also in juveniles, and the anus, which is in a dorsocaudal position, are indicative for un epizoic, sessile life. There is strong evidence that T synaptae punctures the cells of L. galliennei and sucks out their content, which is indicative of parasitism.

Introduction:

The marine heterotardigrade Tetrakentron synaptae

was first described by CUÉNOT in 1892; since then numerous

authors have investigated it, such as RICHTERS (1909), MARCUS (1927), THULIN (1942), BAREL & KRAMERS (1970), and recently

van der LAND (1975); the latter undertook a redescription of this

SEC 5-25 (Rev. 82/11) Canae 2 based on the material collected by KRAMERS. The only known habitat of T. synaptae is the Coast of Brittany where it lives intimately associated with the holothurian Lepto- synapta galliennei; CUENOT (1912) suspected that T. synaptae is a parasite which feeds on the cells of its host. I began in spring 1974 with the help of electron micro- scopic methods to investigate T. synaptae for indications of and adaptations to a parasitic life-style; however, I soon found that not only was the phenology of this tardi- grade species insufficiently known despite numerous light microscopic studies, but there was practically no evidence suggestive of a parasitic life-style (see also MARCUS, 1927); thus, even in the more recent secondary literature, T. synaptae was simply described as an obligatory symphoriont

(see MATTHES, 1978).

The present study provides new data on the biology of this unusual marine tardigrade species, and a description of previously insufficiently known morphological details which identify T. synaptae as a true parasite.

Material and Methods:

The holothurian Leptosynapta cralliennei HERAPATH was collected in mid-April 1974, in mid-May 1974 and at the end of June, beginning of July 1975 in d'Aber de Roscoff east of the rock of Madeira. 3

Light microscopy:

Fixation of the holothurians in Bouin. After addina more glacial acetic acid, T. synaptae can be shaken off the host. The investigations were carried out by means of an interference phase contrast microscope. Additionally, 1 pm- thick sections of the material that had been embedded for the electron microscopy (see below) were stained with

Toluidine Blue-Borax and investigated.

Scanning electron microscopy:

Fixation of the holothurians in Bouin. Small pieces of holothurians with attached tardigrades were dehydrated bypassing 'through a araded alcohol series and Benzol, and dried according to the "critical-point-method" (NORREVANG & WING-

STRAND, 1970). The objects were fastened on aluminum stages using self-adhesive foil or nail polish, contrasted with carbon and gold and investigated in the scanning electron microscope Stereoscan 600 of the Firm Cambridge.

Transmission electron microscopy:

Fixation of the holothurians in a Trialdehyde solu- tion mixed with seawater (modified after KALT & TANDLER,

1971), pH 7.9, at room temperature (1 h); rinsing in buffer

(100 ml 0.1 M Sucrose + 5 ml 2 M Sodium Cacodylate, pH 7.9; postfixation in 2% Osmium Acid in the same buffer (1 h).

Dehydration in the ascending alcohol series - in 70% alcohol the tardigrades were carefully detached from the host with a fine needle - and embedding over Propylene Oxyde in Epon.

The sections were contrasted with Lead Citrate and investi- aated in the Elmiskop 9.2 of the Firm Zeiss. 4

Results:

On the Biology of Leptosynapta galliennei.

Leptosynapta galliennei is found predominantly on the banks of tidal channel systems which become visible only at ebb. In Roscoff, the perhaps most abundantly colonized biotope occurs east of the rock of Madeira where two large tidal channel systems meet. The sediment Con- sists of coarse sand which is still saturated with water at maximal ebb. Up to 25 L. galliennei occur here on one square meter of sand area. Evidence of their presence are ring-shaped depressions in the sediment where the holo- thurians have searched for food.

As far as I am aware, only little is known about the life cycle of L. galliennei. In mid-April I found only juvenile individuals; in mid-May these were fully grown but not yet sexually mature. which contained eggs and sperms were not found until June/July; BAREL & KRAMERS

(1970) collected fully grown, sexually mature L. aalliennei still in October. This species probably lives several years without producing pelagic developmental stages (MORTENSEN,

1931) - as is the case incidentally also in L. inhaerens.

L. galliennei forms a tube from cemented sediment which becomes heavily oxydized in time. The tubes contain a rich meiofauna including the tardigrade Batillipes roscoffiensis

(KRISTENSEN, 1978a), but never T. synaptae.

In some places L. aalliennei and L. inhaerens occur together. The former is distinguished by its size and red color from L. inhaerens which is smaller, pale red to white. Moreover, L. inhaerens is very sticky and possesses only nine commensals or parasites, respectively, as compared to

11 in the case of L. galliennei (BAREL & KRAMERS, 1977).

On the Biology of Tetrakentron Synaptae. p.167

The rate of infestation.

T. synaptae and L. galliennei invariably occur in association with each other, but the holothurians are not always and also not always uniformly infested by tardigrades.

In April, I was able to collect only few juvenile holothurians, none of which were infested. In mid-May, I received 20 L. galliennei (fixated in Bouin) from Roscoff; of these only two were infested with T. synaptae. On one holothurian two tardigrades were attached to the tentacles, as CUENOT (1892) had already described; however, the other was infested by 273 tardigrades which were scattered, fre- quently in groups of several individuals, over the entire body of the holothurian. All animals were sexually mature. van der LAND (1975) also found only adults on the holo- thurians collected in October. Not until the end of June/ beginnina of July did I find egas, juvenile stages of all aaes as well as sexually mature males and females. At this time, nearly 80% of the collected holothurians were infested.

This observation is at variance with the findings by MARCUS

(1927) who at that same time of year observed sexually mature males and females, but no juveniles. 6

Sex ratio and sexual dimorphism.

The sex ratio is ca. 1:1. The males are slightly smaller than the females (figs.1, 3) and possess a larger cephalic papilla (fig.2D). The male gonopore is oval and situated caudal (fia.2D); the female gonopore is difficult to locate in most cases since the is surrounded by a

loose cuticle. But in sexually mature females it is also situated so far caudally that the anus, which is lying in front of it, can be seen from dorsal (figs.1, 4). The aonopore is surrounded here by rosette-shaped cuticular folds. Beneath each element of the rosette lies one epidermis cell. In juvenile females these cells occur already at a very early stage; but they are still situated more medioventrally as is also the case in other heterotardigrades (fig.2B).

None of the investigated, sexually mature males,

100 in total, possessed cuticular rosettes around the gono- pore as described and depicted by MARCUS (MARCUS, 1929, fig.19).

Among the tardigrades collected in June/July two different types of males were found: a small one (ca. 80 pm lona), which perhaps reaches sexual maturity immediately after hatching without molting; and a second larger one

(ca. 175 pm long) with a conspicuously large cephalic papilla

(fia.2, C,D). The dwarf males as well as the sexually mature females possessed a loose cuticle with which they partially adhered to the holothurian; they were therefore largely sessile. Contrastingly, the large males had a - 7 - closely fitting cuticle and changed their position more frequently. On one of the holothurians collected in May were found also males of intermediate lenath with already closely fitting cuticle.

In July 1975, I collected a specimen of L. galliennei which was infested by 296 tardiarades. Of these, 75 were juveniles and the remaining 105 males and 116 females were sexually mature. The smallet juvenile was 55 pm long, the p.168 largest 180 pm. Sexually mature males measured 75-83 pm

(dwarf form) and 127-198 pm ("normal form"). The smallest sexually mature female with seven intraovarian oocytes was

182 pm, the largest with only two oocytes was 235 pm long.

The intraovarian eggs differed considerably in size also

(45 x 27 pm to 65 x 50 pm).

Eggs and embryos.

On the heavily infested holothurian collected in

July were found five singly deposited egas between 70 x 65 pm and 45 x 32 pm in size. Ega size is perhaps sex-specific, the large eggs developing into females (and normal males ?), while the smallest eaas result in dwarf males.

In contradiction to van der LAND (1975), the major- ity of the ovarian and all deposited eggs had thin, sticky shells. Of 300 females examined in July, only three had a single egg each in the ovary the chorion of vedch as thickenad and

as well. This is perhaps the result of varia- sculptured

tions related to weather or season; such variations are - 8 - suspected also in some eutardigrades (PENNAK, 1953).

In sprina, POLLOCK (1970) found several eags of change- able form contained in the ovary of Batillipes pennaki, but in fall and winter there wenaonly few hard-shelled eggs.

All deposited egas already contained fully developed embryos, except for the missina stylets, whose gonadal buds were so larae that they miaht be mistaken for the body cavity (fig.2A).

50tem Fig.': y of Tetrakentron synaptae with four mature oocytes in the ovary (ov), ventral. The gonopore (go) is situated caudally. Note the U-shaped stylet sheaths

In one of the embryos four claws were recognizable p.170 on each leg. The freshly hatched animais must therefore be already equipped with the same number of claws as the adults. 50/.cm Fig.2: Developmental stages and ed of Tetrakentron synaptae. A: Embryo with gonadal buds (goa). B: Juvenile female, ventral. Note that the anus is still situated ventrally. C: Fertile dwarf male with hyaline cuticle, dorsal, with dorsally positioned anus. D: vagile male with closely fitting cuticle and large cephalic papilla

Abbreviations in the figures: es = puncture area of the stylets mc = cirrus medianus cA = cirrus A (cirrus lateralis) mu muscle cE = cirrus E ov = ovary cp = cephalic papilla pr procuticle da = gut p2 spine on 2nd pair of legs ep = epicuticle te = testis go = gonopore = z-bands Kr = claws Le = Leptosynapta goa = gonadal buds aalliennei - 10 -

This had previously not been knowr from any heterotardi-

grade species. Here the juvenile stages usually possess

fewer claws than the adults, mostly two. Also the number

of claw hooks is identical in juverdle and adult T. synaptae. The

smallest juvenile (length 55 pm) had a total of 80 claw

hooks (10 per lea), the same number as the largest female

(compare also van der LAND, 1975). I did not find a single

specimen with 96 claw hooks as reported by MARCUS (1928).

Fig.3: Fertile y of Tetràkentron synaptae onLeptosynapta aalliennei. - 11 -

À.. naz Fig.4: Posterior view of the same female as in fig.3, with the anus situated dorsoventrally. The depression in the sea cucumber is distinctly visible, the cuticle is partially destroyed.

The Cuticle.

The females and dwarf males of T. synaptae possess p.171 a loose, hyaline cuticle. This was regarded by MARCUS

(1927) as beina a fixation artifact or possibly the result p.172 of a patholoaical molt (fia.5). In the electron microscopic - 12 - image it becomes evident that this envelope is the result of enlaraed parts of the epicuticle sensu lato (on the terminology compare GREVEN, 1975) which in addition may be stronaly folded.

Fig.5: Tetrakentron synaptae y detached from the host.

A areater resolution of the outer epicuticle is hardly possible. The epicuticle is covered by a mucous layer which is not always distinctly recoanizable. - 13 -

Adjacent to it are the hexagonal tubules ("striated layer", "honeycomb layer", KRISTENSEN, 1976) which are very typical in heteroarades. Then follows an electron- dense space, filled partially with a flocculent, osmiophilic material, into which processes of the procuticle protrude.

The latter is demarcated toward the electron-permeable area p.173 by a triple- layer which is only narely identifiable ( fig .7b) . The entire area between the triple-layer and the epidermis is defired as procuticle, since no further layers can be iden- tified in it. Thus, we do not find here any of the "rods" traversing the free electron-dense area as is characteristic for many heterotardigrades. The contact between epicuticle and procuticle is therefore extremely limited.

The Musculature. p.175

MARCUS (1928) already pointed out that the muscul- ture of T. synaptae is more strongly developed as compared to other tardigrades, However, he does not mention any cross striation. But under the light microscope already this can be distinctly recognized in the dorsal longitudi- nal muscles,there are up to 15 sarcomeres present (fig.7c), and also in the leg musculature.

The Buccal Apparatus.

Unfortunately, I could exame the buccal apparatus only in animais whose stylets had been dissolved by the - 14 -

Fia.6: e of Tetrakentron synaptae with larae cephalic papilla (cp). Note the bent head and the mouth opening which is tightly appressed to the host.

fixation mixture. As in the members of the genus Echiniscoides

(compare KRISTENSEN&RALLAS, 1980), a delicate,cuticular, transverse stylet support occurs on each side of the buccal tube. The stylet has a broadened base with a thick (cuti- cular?) sheath which does not dissolve after Bouin-fixation.

The sheath is U-shaped and it must not be mistaken for the furca which disappears after Bouin-fixation (fig.1). I am - 15 - aware of only one other example with such U-shaped stylet sheaths, namely the semiterrestrial heterotardigrade genus

Hypechiniscus (KRISTENSEN, unpublished). The buccal tube aradually widens from front to back, but is always narrower than the lumen of the muscularpharyngeal bulb.

The Anchorage of Tetrakentron synaptae on Leptosynapta galliennei.

Even after fixation, T. synaptae is difficult to detach from its substrate. Favored by its dorsoventrally flattened body, it lies closely appressed to the holothu- rian. In the scannina electron microscopic image, the holothurian body seems to have a shallow depression here

(fia.4). Since all claw hooks of T. synaptae are exception- ally long (ca. 3-4 pm) and are also inward curved, the claws penetrate deeply into the tissue of the sea cucumber.

The section preparations showed that T. synaptae also thrusts its extremely long stylets deeply into the host tissue which sustains extensive damage in the process (fig.7a; compare also fia.6).

It can be assumed that T. synaptae pierces the cells of L. galliennei and sucks out their content. This is supported by the fact that the gut of the animals is filled with a whitish-red mass which in no way resembles the crut content of other, predominantly herbivorous tardi- grades. - 16 -

Fig.7: (a): Tetrakentron synaptae on Leptosynapta galliennei (Le). The stylets and claws are deeply anchored in the host tissue. (b): Epicuticle (hyaline envelope) of T. synaptae. (c): Dorsal musculature of T. synaptae with distinct cross striation (interference phase contrast after NOMARSKI). - 17 -

Discussion:

Although Tetrakentron synaptae has been regarded as

a parasite since CUENOT (1892), there was some skepticism

(MARCUS, 1927). The only argument in favor of this assump-

tion was the persistent association of the tardigrade with

L. galliennei. The flattened body shape, the reduced head

appendages (KRISTENSEN, in preparation) and the large num-

ber of claw hooks, which serve to anchor the animal firmly

to its host, have been interpreted as adaptations to an

epizoic or, respectively, a phoretic life-style (MARCUS,

1927; van der LAND, 1975). Althouah it had been repeat-

edly assumed that the parasite pierces the host cells and

feeds on the content, this was never conclusively established.

A more or less close association of marine tardigrades with

other organisms is not uncommon; for instance, Halechinis-

cus quiteli (uncertain species!) lives in or on Ostrea

edulis (Bivalvia)(RICHTERS, 1909), Actinarctus doryphorus

on Echinocyamus pusillus (Echinoidea)(SCHULZ, 1935; GRELL, p.176

1937), Pleocola limnoriae on lignorum ()

(CANTACUZENE, 1951), Echiniscoides sigismundi on Mytilus

edulis (Bivalvia)(GREEN, 1950) or on Balanus balanoides

(Cirripedia)(CRISP & HOBART, 1954; POLLOCK, 1975; KRISTEN-

'SEN & HALLAS, 1980). However, all these species are found

also free-living within the sand interstitial system

(RENAUD-MORNANT & POLLOCK, 1971; POLLOCK, 1976),and their

body structure does not show any special features which can

be so clearly interpreted as adaptations to an epizoic - 18 - life-style as is the case in T. synaptae. In Western Green- land, an (vagile) Echiniscoides species was discove'red only recently which occurs in Balanus balanoides whose cells it pierces with its disproportionately long stylets and sucks out (KRISTENSEN & HALLAS, 1980).

The powerful "claw apparatus" in T. synaptae is not unique among tardigrades. For instance, the genus Styraconyx possesses up to 96 claw hooks with which it attaches itself to algae. It is conspicuous however, that the juveniles of

T. synaptae already possess the same large number of claw hooks as the adults. The attachment to the host is further facilitated by the external mucous layer and, where present, by the hyaline cuticular envelope. Comparable hyaline envelopes are known also from other tardigrade genera such as Florarctus and Actinarctus (RAMAZZOTTI, 1972). But in those, as is common also in other heterotardigrades, we find rods that are visible already light-microscopically and apparently traverse the area between the "honeycomb layer" and the procuticle (GREVEN, 1972, 1975; KRISTENSEN,

1976).

The firm anchorage of T. synaptae on the host animal makes a change of position if not impossible at least diffi- cult. Food intake, mating with males of which some are vacille however, defecation and oviposition all take place therefore in a more or less firmly defined place. The trans- location of anus and gonopore to a caudal position is quite uncommon in other heterotardiorades, and it can only be - 19 - understood as an adaptation to this sessile to semisessile life-style. The cross striation of the musculature is urusually well developed for tardigrades, but whether and in what way there is a connection between it and this life- style, is difficult to decide. Cross striation in tardigrade musculature is found in the muscles of the stylets (WALZ,1D75);

KRISTENSEN, 1978b) as well as in those of the legs of

Batillipes noerrevanai (KRISTENSEN, 1978b), where up to

four well defined sarcomeres occur one behind the other, and is thought to be related to the special demands during food intake or, respectively, to the mode of locomotion.

A sessile life-style may have promoted parasitism. The

insertion of the stylets into the host tissue is now

regarded as servina primarily to obtain food and secondarily as additional anchorage device. The findings presented here characterize T. syraptae as a laraely sessile tardi- grade species that is living parasitically on L. galliennei.

Acknowledgements.

I am indebted to Lecturer Dr.H. Greven, Münster,

for stimulating discussions, Miss J. Tesch and Mr. B.

Rasmussen for assistance with the illustrations, and the

Station Biologique (Roscoff) for my stay in 1974 and 1975. Biblioaraphy

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Foreign Bibliographic Items.

1) A new marine tardigrade, a commensal of Limnoria lignorum (RATHKE). 2) Contributions on the knowledae of Actinarctus doryphorus E. SCHULZ, as well as remarks on the tardigrade fauna of the Skitt-Gatt of Helgoland. 3) Comparative investigations of heterograde and eutardi- Grade inteauments. 4) On the anatomy and ecology of marine tardigrades. 5) On the comparative anatomy and histology of tardigrades. 6) Animal symbioses and similar forms of associations. 7) Marine tardigrades. 8) Actinarctus doryphorus nov.gen.nov.spec., a peculiar tardigrade from the North Sea. 9) A new marine tardigrade.