HELGOL~NDER MEERESUNTERSUCHUNGEN Helgol~nder Meeresunters. 40, 309-319 (1986)

Ultrastructural observations on feeding appendages and gills of Alvinella pompejana (Annelida, Polychaeta)

V. S t o r c h 1 & F. G a i l l 2

I Zoologisches Institut I (Morphologie/Okologie); Im Neuenheimer Feld 230, D-6900 Heidelberg, Federal Repubh'c of Germany

2 Centre de Bio]ogie Cellulaire; 67, rue Maurice Giinsbourg, F-94200 Ivry sur Seine, France

ABSTRACT: The feeding appendages of Alvinel]a pompe]ana obtained from a deep-sea hydrother- real vent environment are described. They are characterized by a ciliated groove, the cells of which have a very" distinctive ultrastructure, by groups of bipolar receptor cells and by several kinds of gland cells. Among these, one ceil type is in an upside down position suggesting a function completely different from other epidermal secretory cells. The gills differ considerably from the feeding appendages on the basis of their ultrastructure. Their epidermis is very irregular in height; basal infoldings give the blood access to a space coming very near to the external medium. The blood vascular system is open. On the other hand, the gills of Amphicteis gunneri are not effective sites of gas exchange, since their columnar epithelium is underlain with muscle cells. The cells composing the feeding appendages and gills of Alvinella pompe]ana are characterized by ultra- structurally very different mitochondria.

INTRODUCTION

Amphare t idae is a family of tube-dwel l ing polychaetes re la ted to Terebe l l idae and

Amphic tenidae . They comprise over two hundred descr ibed species and are wel l

r epresen ted in deep waters whe re food is scarce. Some years ago, a n e w species, Alvinella pompejana, was descr ibed by Desbruy~res & Laubier (1980) from the immedi - ate vicinity of the warm hydrothermal springs east of the Galapagos Islands. As in other

representa t ives of the family, the anterior body region carries numerous f eed ing appen-

dages which p resumably can be wi thdrawn comple te ly into the mouth cavity into the

roof of which they are inserted. Additionally, the anterior segment s bear four pairs of branchiae composed of a s tem and many fi laments and a r ranged in lateral groups.

In the meant ime, six species and subspecies of the recent ly e rec ted subfamily

Alvinell inae have b e e n described. Desbruy~res & Laubier (in prep.) supposed that these are well separated from all other t e rebe l lomorph polychae tes due to the absence of a

clear differentiation b e t w e e n thorax and abdomen, a character just ifying the proposal of

a new family, Alvinell idae. All of them are strictly associated with deep hydro thermal vents. Among them, A. pompe]ana, is the most thermophi lous species of inver tebra tes

currently known from this biotope. It can tolerate t empera tu res from 20 to 40 °C (Laubier

& Desbruy~res, 1985; Desbruy~res et al., 1985). Most Amphare t idae are cons idered surface depos i t - feeders (for l i terature see

© Biologische Anstalt Helgoland, Hamburg

310 V. Storch & F. Gail l

F a u c h a l d & Jumars , 1979). They stretch out of thei r t ube sp read ing their tentac les over the subst ra tum, and k e e p their b r anch i ae up in the water . It is not cer tain whe ther the same is t rue of the a b o v e - m e n t i o n e d spec ies of hyd ro the rma l vents. Electron microscopic analys is of A. pompejana has demons t r a t ed the p re sence of coccoid and fi lamentous bac te r ia on var ious a reas of thei r i n t e g u m e n t (Desbruy~res et al., 1983). The microorgan- isms are espec ia l ly numerous in the dorsa l par t of the body and on the posterior pa rapod ia . Gai l l et al. (1984a) were ab le to find them in four types of in t egumenta l associat ions. The funct ional s igni f icance of the epib io t ic bacter ia , however , is still an en igma. A l a y s e - D a n e t et aL (1985) sugges t tha t some metabo l i t e e x c h a n g e b e t w e e n the mic roorgan i sms and their an imal host occurs. W h e r e a s the surface specia l iza t ions of the pos ter ior reg ion and the tube have b e e n a n a l y s e d by t ransmiss ion and scann ing e lec t ron microscopy and mic roprobe analys is by severa l au thors (Alayse-Dane t et al., 1985; Desbruy~res et al., 1983; Gail l et al., 1984b; Laubier et al., 1983; Vovelle & Gafll, 1986), inves t iga t ions on the feed ing a p p e n d a g e s and gills are lacking, not only for this species, but for the whole family. F e e d i n g ten tac les of the re la ted Lanice conchilega (Terebel- l idae) have b e e n ana lysed u l t ras t ruc tura l ly by Schul te & Riehl (1976); gills of various species , inc lud ing Te rebe l l i dae and Amph ic t en idae , have been inves t iga ted by Storch & Alber t i (1978) and by M e n e n d e z et al. (1984). Receptor cells on the body a p p e n d a g e s

s. b

Fig. 1. Alvinella pompejana. Schematic representation of feeding appendage (a, cross section) and gill filament (b). B: blood space in gill, M: muscle cell, R: receptor cell, Sa-~: secretory cells, SG:

ciliated groove

F e e d i n g a p p e n d a g e s and gills of Alvinella 311

were ana lysed , e.g. by Boi l ly-Marer (1972), Dorset t & H y d e (1969), Lawry (1967), Miche l (1970), Storch (1972). F ind ings on A m p h a r e t i d a e are lacking. Mucous cells have b e e n inves t iga ted by Bielakoff et al. (1975), Dorset t & H y d e (1969), H a u s m a n n (1982), Hi lb ig (1986), Kryvi (1972), Mar t in (1978), Storch & Welsch (1972), aga in exc lud ing the a forement ioned family.

Since the ex te rna l a p p e a r a n c e of gills var ies wide ly wi thin the family A m p h a r e t i d a e (and wi thin Alv ine l l inae /Alv ine l l idae) , a second spec ies hav ing smooth b ranch iae , Amphicteis gunneri, was sec t ioned for compar i son in this s tudy.

MATERIAL AND METHODS

Alvinella pompejana was col lec ted at a dep th of 2600 m at 12 ° 48' N and 103 ° 56' W by the research submers ib le " C y a n a " . After re t r ieval to the surface, smal l p i eces of the animals were f ixed with 0.4 cacody la t e -bu f f e r ed g l u t a r a l d e h y d e (3 % final concent ra - tion) at pH 7.2 and then pos t - f ixed with osmium te t roxide ( 1 % final concentra t ion) . The mater ia l was e m b e d d e d in Durcopan.

Amphicteis gunneri was col lec ted in the Kat tega t by the r e sea rch vesse l , ,Poseidon". Pieces were i m m e r s e d in ice-cold g l u t a r a l d e h y d e (3.5 % in p h o s p h a t e buffer, p H 7.5). After post-f ixat ion with 1% osmium te t roxide , the t issue was d e h y d r a t e d in e thano l and e m b e d d e d in Araldi te .

Thin sect ions were s t a ined for 5 min with uranyl ace ta te ( sa tura ted solut ion in 70 % methanol) and for a fur ther 5 min in l e ad ci t rate (Reynolds, 1963). The sect ions were examined in a Zeiss EM 9-S2 and Zeiss EM 10 C microscope.

RESULTS

F e e d i n g a p p e n d a g e s

The feed ing a p p e n d a g e s of Alvinella pompejana are re t ract i le and f i lamentous. Their subep ide rma l core conta ins a compl ica ted muscu la tu re whose major cons t i tuents are longi tud ina l musc le cells in the cen t re and t ransverse musc le cells that l ink a c i l ia ted a rea with the oppos i te s ide (Fig. la) . Addi t ional ly , the re a re ob l ique musc le ceils and muscle cells spann ing the inner and outer e d g e s of the groove. The f r amework of the muscle cells m a y be fi l led with amebocytes , ra ther h o m o g e n e o u s b lood cells (Fig. 5d) and by s ingle h a t - s h a p e d cells which cannot be in t e rp re t ed with cer ta in ty from our l imited mater ia l . Their condensed nucleus which is assoc ia ted with mi tochondr ia sug- gests that they could r ep re sen t ex t r eme ly modi f ied spe rm ceils. Since these po lychae t e s successfully occupy the ex t r eme habi ta t s of the hyd ro the rma t vents , d i rec t t ransfer of (modified) spe rm cells s eems plaus ib le . Immed ia t e ly be low the ep idermis , co l l agen fibrils can be found. The ci] iated a rea occupies nea r ly one half of a cross-sect ion. Normal ly it is concave forming a longi tud ina l groove. The whole of the ten tac le ep idermis is p rov ided with secre tory cells be long ing to severa l types. The cuticle of these a p p e n d a g e s is re la t ive ly thin (1-2 ~m), p e n e t r a t e d by numerous microvil l i and covered by typical ep icu t icu la r pro jec t ions (Fig. 2a, b). Often, the fibrils follow a s inusoidal pa th (Fig. 2a). In the c i l ia ted groove the shape of the cells r a n g e s from flat (in the centre) to pr ismat ic (in the marg ina l position). Thei r cilia are cons tan t ly of the

312 V. S torch & F. Gai l l

Fig. 2. Alvine]la pompejana (a-c) and Amphicteis gunneri (d), cuticle. E: epicuticular projections, a Tangential section of feeding tentacle (19 000: 1); b cross section of feeding tentacle (19 000: 1); c tangential section of stem of gill (19 000: 1); d cross section of gill of Arnphicteis gunneri (19 000:11

c o n v e n t i o n a l 9 + 2 formula . The i r root le t s a re i n se r t ed at an a n g l e of abou t 45 ° to the

su r f ace (Fig. 3a -c ) and a re a r r a n g e d m o r e or less pa r a l l e l to o n e ano the r . The a d j a c e n t

c y t o p l a s m is d o m i n a t e d by a d e n s e p o p u l a t i o n of m i t o c h o n d r i a wi th a v e r y d is t inc t ive u l t r a s t ruc tu re (Fig. 3d). The i r c r i s tae a r e o f ten l o n g i t u d i n a l l y a r r a n g e d , s o m e t i m e s in

z i g z a g or ien ta t ion . A n o t h e r a c c u m u l a t i o n of m i t o c h o n d r i a of t he s a m e type can be found

in the basa l po r t ion of t h e s e cells, w h e r e a s the r o u n d n u c l e u s is l oca t ed centra l ly , often

s u r r o u n d e d by s o m e d i c t y o s o m e s a n d b u n d l e s of f i l aments . O u t s i d e the c i l i a ted groove , s u p p o r t i v e cells, s ec re to ry a n d r e c e p t o r cel ls d o m i n a t e .

F e e d i n g a p p e n d a g e s a n d gills of Alvinella 313

Fig. 3. Alvinella pompejana. Ciliated groove (a-d) and gill (e). M: subepidermal muscle cell, R: rootlets of cilia, Sc and Sd: secretory cells, a Low power micrograph of ciliated groove (2400: 1); b Cuticle, basal bodies and ciliary rootlets (R) (9500: 1); c Ciliary rootlets and secretory cell (S~) (9500: 1); d mitochondria of ciliated cells in groove (19 000: 1); e mitochondria of gill epi thel ium (19 000: 1)

314 V. Storch & F. Gafll

The suppor t ive cells are pr ismatic , but have an i r regular outline, which is due to their ne ighbou r ing cells (see below). Their nucleus is e longa ted , and in a central posit ion. Apical ly , these cells have m a n y da rk mi tochondr ia , which differ cons iderab ly from the a fo remen t ioned mi tochondr ia of the c i l ia ted cells (Fig. 5c). Dic tyosomes com- posed of about 10 cis ternae, s ingle c is te rnae of the rough endop lasmic ret iculum, long i tud ina l ly a r r a n g e d bund le s of f i laments , and vesic les of different sizes commonly occur in the cytoplasm.

Secre tory cells can be classif ied as follows: (a) In this common cell type the rough endop la smic re t icu lum is a r r a n g e d as

c i s te rnae and occupies most a reas of the cy top lasm (Fig. 4a-c) . Dic tyosomes are a r r anged in the vicinity of the cent ra l cell nucleus. The secre tory produc ts are e lec t ron dense and globular . The mi tochondr ia a re la rge and dark; aga in these o rgane l l e s differ from that p rev ious ly descr ibed . If the bu lk of the secre tory produc ts we re not loca ted basal ly, and if these cells had an open ing into the cut icular face of the in tegument , then the u l t ras t ructure of this cell type would co r re spond to a w i d e s p r e a d cell type within mar ine inve r t eb ra t e s {Storch & Welsch, 1972).

In fact, t hese cells were never found to r each the apica l surface of the epi thel ium. (b) The cy top lasm of this cell type is d o m i n a t e d by the secre tory produc t and Golgi

fields which are cha rac te r i zed by e lec t ron- lucen t and a l te rna t ing e l ec t ron -dense areas (Fig. 4d, e). The gene ra l outl ine of these cells is very i r regular . The round nucleus is loca ted in the lower third.

(c) Ano the r cell t ype conta ins g lobu la r secre tory drople t s which are p a c k e d close together . E lec t ron-dense dots are d i s t r ibu ted all over the secret ion, which is of med ium e lec t ron-dens i ty (Fig. 3c). The nuc leus is loca ted basal ly , the secre tory produc t is the p r e d o m i n a n t fea ture of the cell.

(d) This cell type is s lender ; its cell body can be loca ted in the sub-ep i the l ia l t issue e x t e n d i n g a process to the surface. The nuc leus occupies a basa l or la te ra l posi t ion and is su r rounded by a r im of cytoplasm. The distal par t of the cell is domina t ed by electron- dense secre tory droplets .

Groups of abou t six i n t e r spe r sed s l ender b ipo la r cells with apica l cilia (about 10 per cell) can be found. The cilia t raverse the cuticle (Fig. 5a, b) and are of the ord inary 9 + 2 pat tern . Below their basa l bod ies m a n y mi tochondr ia occur (Fig. 5b), which are less dense than those of the suppor t ive cells. In the i m m e d i a t e vicini ty of the recep tor cell aggrega t ions , a s ingle secre tory cell wi th a very l ight secre t ion occurs (Fig. 5b). Nerve cell p rocesses can be found in a bas i ep i the l i a l posit ion.

G i l l s

The gills differ cons ide rab ly from the f eed ing a p p e n d a g e s . This appl ies to their shape and to their ul t ras t ructure . They are p inna te , bea r ing very m a n y thin outgrowths. Their cuticle is th ick (5 ~tm) in their cent ra l s tem (Fig. 2c), but ex t r eme ly thin (0.5 ~tm) in the p innu les (Fig. lb) . The cuticle of the s tem is s imilar to the one desc r ibed from the dorsa l s ide of the body (Gaill & Boul igand, 1985). Fibri ls a re a l igned a long r igh t -handed or l e f t - h a n d e d hel ices a round the organ. Ultrastructural ly, they r e semble the gills of Terebellides as de sc r ibed by Storch & Alber t i (1978), which means that their epidermis is ve ry i r regular , info lded in c i rcumscr ibed a reas g iv ing the b lood access to a space coming

F e e d i n g a p p e n d a g e s a n d gi l ls of A l v i n e l l a 315

Fig. 4. Alvinella pompejana. Secretory cells. C: cuticle, M: mitochondrium, So: secretory cell a. a-c Secretory cell type a; d, e secretory cell type b. a Low power micrograph of secretory cells and supportive cells (2400: 1); b nucleus, surrounding endoplasmic reticulum, and mitochondria (M) (9500: 1); c endoplasmic reticulum, dictyosorne, and secretory droplets (19 000: 1); d nucleus and

surrounding cytoplasm {9500: 1); e dictyosome and mitochondria (19 000: 1)

V. S torch & F. Gai l l 316

Fig. 5. Alvinella pompejana. Various cell types of feeding appendage, a cross section of receptor cells (R) and surrounding supportive cells (SC) (9500: 1); b longitudinal section of receptor cells (R) and adjacent secretory cell (S) (9500: I); c mitochondria of supportive cell (19 000: 1); d blood cell

(9500: 1)

v e r y n e a r to the e x t e r n a l m e d i u m . T h e s e in fo ld ings a r e r e g u l a r l y a r r a n g e d , and the

b lood s p a c e is no t l i ned by an e p i t h e l i u m of m e s o d e r m a l or igin. Aga in , this is a case of

an a n n e t i d wi th an o p e n b lood v a s c u l a r sys tem. T h e ep i the l i a l cel ls h o u s e a dense

p o p u l a t i o n of m i t o c h o n d r i a , w h i c h a g a i n di f fer in the i r u l t r a s t ruc tu re (Fig. 3e). Secre tory

Feeding appendages and gills of Alvinella 317

cells of the goblet cell type and groups of bipolar ciliary receptor cells occur on the gills. The basal part of the gills contain muscle cells in their core.

The gills of Amphicteis gunneri are long and smooth appendages with thick cuticle (5-7 ~tm). At its surface, it carries epicuticular projections, which are similar to the ones described from Alvinella pompejana (Fig. 2d). The epi the l ium is co lumnar a nd under - lain with a thick layer of muscle cells.

DISCUSSION

The present invest igat ion has shown that the so-called gills of Alvinella pompejana and Amphicteis gunneri are so different in their ul trastructure that their funct ion can by no means be identical. The gills of Amphicteis gunneri have a very thick cuticle and prismatic epidermis cells which are under la in with musculature . Thus, they do not fulfil the demands of respiratory epithel ia which are composed of flat cells that allow ~as exchange across the body surface merely by diffusion. On the other h a n d in the gills of Alvinelta pompejana, the dis tance be tween the i n t egumen ta l surface and the sub- epidermal blood spaces can be as small a 1 ~tm. This value corresponds to ext reme cases reported for other polychaetes (Storch & Alberti, 1978). This is of the same magn i tude as diffusion distances in the m a m m a l i a n lung, or in fish gills.

Polychaete gills can be classified as follows: (a) gills with true blood vessels bordered by epi thel iomuscular cells. (b) gills with partly opened vessels. The vessels are no longer tubular channels , but

open out in the direction of the epidermis. (c) gills with blood spaces directly below the surface epithel ium, which are not l ined

by coelothelial cells. (d) gills with blood spaces bu lg ing deeply into the surface epi thel ium. Here, the

greatest reduct ion of the dis tance b e t w e e n blood and water has b e e n achieved. This last- ment ioned type was found in Alvinella pompejana.

Furthermore, it has to be men t ioned that epibiotlc bacter ia are absent from the gills and feeding tentacles of Alvinella pompejana. It seems that the presence of sea water does not allow their colonization. The worms general ly stay inside their tubes, only their buccal part be ing in contact with the ambien t water.

The feeding tentacles are characterized by several k inds of ep idermal secretory cells. As in other mar ine invertebrates, these cells exhibit varied ultrastructures. Their function, however, remains to be elucidated. In AnaitJdes mucosa, H a u s m a n n (1982) found many kinds of mucous cells, bu t could not explain their function. On sectional preparations, one cannot even see whether they, in fact, correspond to different cell types, or whether they merely represent different phases of matura t ion of one cell type.

In our opinion, the ER-rich cell type differs principally from the others and all other secretory cells described so far for mar ine inver tebrates from the point of view of their upside down position. That it is in such a position raises doubt as to how the secretory products are extruded. Since they always seem to be located adjacent ly to a basiepi the- lial nerve plexus, their funct ion may be associated with nervous activity.

Another unusua l feature is the ultrastructural diversity of mitochondria in different cell types. Our results indicate that there is good reason to bel ieve that this diversity is an expression of their equal ly diverse tasks.

318 V. S to r ch & F. Gaill

H o w e v e r , c o n c e r n i n g t h e s e c r e t o r y ce l l s a n d t h e m i t o c h o n d r i a , our i n v e s t i g a t i o n

w h i c h w a s b a s e d on l i m i t e d m a t e r i a l h a s p r o d u c e d m o r e q u e s t i o n s t h a n a n t i c i p a t e d , a n d

c a n on ly b e c o n f i r m e d b y f u r t h e r c o m p a r a t i v e a n d e x p e r i m e n t a l s tud ies .

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Bielakoff, J., Damas, D. & Vovelle, J, 1975. Histologie et histochimie des formations glandulaires imphqu6s dans l 'elaboration du tube chez Lanice conchflega (Ann61ide Polych6te). - Archs Zool. exp. g6n. 116, 499-520.

Boilly-Marer, Y., 1972. Etude ultrastructurale des cirres parapodiaux de Nereidiens atoques (AnnSlides Polych~tes). - Z. Zellforsch. mikrosk. Anat. 131, 309-327.

Desbruy~res, D. & Laubier, L., 1980. Alvinella pompejana gen. sp. nov., Ampharet idae aberrant des sources hydrothermales de la ride Est-Pacifique. - Oceanologica Acta 3, 267-274.

Desbruy6res, D., Gaill, F., Laubier, L., Prieur, D. & Rau, G. H., 1983. Unusual nutrition of the "Pompeii worm" Alvinella pompe jana (polychaetous annelid) from a hydrothermal vent envi- ronment: SEM, TEM, 13C and 15N evidence. - Mar. Biol. 75, 201-205.

Desbruy~res, D., Gaill, F., Laubier, L. & Fouquet, Y., 1985. Polychaetous annelids from hydrother- real vent ecosystems: an ecological overview. - Bull. biol. Soc. Wash. 6, 103-116.

Dorsett, D. A. & Hyde, R., 1969. The fine structure of the compound sense organs on the cirri of Nereis diversicolor. - Z. Zellforsch. mikrosk. Anat. 97, 512-527.

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Gaill, F. & Bouligand, Y., 1985. Long pitch hehces in invertebrate collagens. In: Biology of invertebrate and lower vertebrate collagens. Ed. by A. Bairati & R. Garrone. Plenum Publ. Corp., London, 267-274.

Gaill, F., Halpern, S., Quintana, C. & DesbruyOres, D., 1984a. Presence intracellulaire d'arsenic et de zinc associSs au soufre chez une Polych~te des sources hydrothermales (Alvinella pompe- j a n a ) . - C. r. Acad. Sci., Paris 298, (S6r. 3), 331-336.

Gaill, F., Desbruy6res, D., Prieur, D. & Gourret, J. P., 1984 b. Mise en ~vidence de communaut6s bact~riennes ~pibiontes du "Ver de Pomp6i" (Alvinella pompe]ana). - C. r. Acad. Sci., Paris 298, (S~r. 3), 553-558.

Hausmann, K., 1982. Elektronenmikroskopische Untersuchungen an Anait ides mucosa (Annelida, Polychaeta). Cuticula und Cil~en, Schleimzellen und Schleimextrusion. - Helgol~nder Meeresunters. 35, 79-96.

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F e e d i n g a p p e n d a g e s a n d g i l l s of At~4nella 3 1 9

Reynolds , E, S., 1963. T h e u s e of l e a d ci t rate at h i g h p H as an e l ec t ron o p a q u e s ta in in e l ec t ron microscopy. - J. Cel l Biol. 17, 208-212 .

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