HELGOL~NDER MEERESUNTERSUCHUNGEN
Helgol~nder Meeresunters. 40, 309-319 (1986)
Ultrastructural observations on feeding a p p e n d a g e s
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 N e u e n h e i m e r 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 hydrotherreal 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 ultrastructurally very different mitochondria.
INTRODUCTION
A m p h a r e t i d a e is a family of t u b e - d w e l l i n g p o l y c h a e t e s r e l a t e d to T e r e b e l l i d a e a n d
A m p h i c t e n i d a e . T h e y comprise over two h u n d r e d d e s c r i b e d s p e c i e s a n d are w e l l
r e p r e s e n t e d in d e e p w a t e r s w h e r e food is scarce. S o m e y e a r s ago, a n e w species,
Alvinella pompejana, w a s d e s c r i b e d by D e s b r u y ~ r e s & L a u b i e r (1980) from the i m m e d i ate vicinity of the w a r m h y d r o t h e r m a l springs east of the G a l a p a g o s Islands. As in other
r e p r e s e n t a t i v e s of the family, the anterior b o d y r e g i o n carries n u m e r o u s f e e d i n g a p p e n d a g e s w h i c h p r e s u m a b l y c a n be w i t h d r a w n c o m p l e t e l y into t h e m o u t h cavity into the
roof of w h i c h they are inserted. Additionally, the anterior s e g m e n t s b e a r four pairs of
b r a n c h i a e c o m p o s e d of a stem a n d m a n y filaments a n d a r r a n g e d in lateral groups.
In the m e a n t i m e , six s p e c i e s a n d s u b s p e c i e s of the r e c e n t l y e r e c t e d subfamily
Alvinellinae h a v e b e e n described. D e s b r u y ~ r e s & Laubier (in prep.) s u p p o s e d that t h e s e
are well s e p a r a t e d from all other t e r e b e l l o m o r p h p o l y c h a e t e s d u e to t h e a b s e n c e of a
clear differentiation b e t w e e n t h o r a x a n d a b d o m e n , a c h a r a c t e r justifying t h e proposal of
a n e w family, Alvinellidae. All of t h e m are strictly associated with d e e p h y d r o t h e r m a l
vents. A m o n g them, A. pompe]ana, is the most t h e r m o p h i l o u s species of i n v e r t e b r a t e s
currently k n o w n from this biotope. It c a n tolerate t e m p e r a t u r e s from 20 to 40 °C (Laubier
& Desbruy~res, 1985; D e s b r u y ~ r e s et al., 1985).
Most A m p h a r e t i d a e are c o n s i d e r e d surface d e p o s i t - f e e d e r s (for literature see
© Biologische Anstalt Helgoland, Hamburg
310
V. Storch & F. Gaill
F a u c h a l d & J u m a r s , 1979). T h e y stretch out of their t u b e s p r e a d i n g their tentacles over
the substratum, a n d k e e p their b r a n c h i a e u p in the water. It is not certain w h e t h e r the
s a m e is true of the a b o v e - m e n t i o n e d s p e c i e s of h y d r o t h e r m a l vents. Electron microscopic
analysis of A. pompejana has d e m o n s t r a t e d the p r e s e n c e of coccoid a n d filamentous
b a c t e r i a on various a r e a s of their i n t e g u m e n t (Desbruy~res et al., 1983). The microorganisms are e s p e c i a l l y n u m e r o u s in the dorsal p a r t of the b o d y a n d on the posterior
p a r a p o d i a . Gaill et al. (1984a) w e r e a b l e to find t h e m in four t y p e s of i n t e g u m e n t a l
associations. T h e functional s i g n i f i c a n c e of the e p i b i o t i c bacteria, however, is still an
e n i g m a . A l a y s e - D a n e t et aL (1985) s u g g e s t t h a t s o m e m e t a b o l i t e e x c h a n g e b e t w e e n the
m i c r o o r g a n i s m s a n d their a n i m a l host occurs. W h e r e a s t h e surface specializations of the
posterior r e g i o n a n d t h e t u b e h a v e b e e n a n a l y s e d b y t r a n s m i s s i o n a n d s c a n n i n g electron
m i c r o s c o p y a n d m i c r o p r o b e analysis b y s e v e r a l a u t h o r s ( A l a y s e - D a n e t et al., 1985;
D e s b r u y ~ r e s et al., 1983; Gaill et al., 1984b; L a u b i e r et al., 1983; Vovelle & Gafll, 1986),
i n v e s t i g a t i o n s on the f e e d i n g a p p e n d a g e s a n d gills are lacking, not only for this species,
b u t for the w h o l e family. F e e d i n g t e n t a c l e s of the r e l a t e d Lanice conchilega (Terebellidae) h a v e b e e n a n a l y s e d u l t r a s t r u c t u r a l l y b y Schulte & Riehl (1976); gills of various
species, i n c l u d i n g T e r e b e l l i d a e a n d A m p h i c t e n i d a e , h a v e b e e n i n v e s t i g a t e d b y Storch &
A l b e r t i (1978) a n d b y M e n e n d e z et al. (1984). R e c e p t o r cells on the b o d y 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 a n d gills of Alvinella
311
w e r e a n a l y s e d , e.g. b y B o i l l y - M a r e r (1972), Dorsett & H y d e (1969), L a w r y (1967), M i c h e l
(1970), Storch (1972). F i n d i n g s on A m p h a r e t i d a e a r e lacking. M u c o u s cells h a v e b e e n
i n v e s t i g a t e d b y Bielakoff et al. (1975), Dorsett & H y d e (1969), H a u s m a n n (1982), H i l b i g
(1986), Kryvi (1972), M a r t i n (1978), Storch & W e l s c h (1972), a g a i n e x c l u d i n g the
a f o r e m e n t i o n e d family.
Since the e x t e r n a l a p p e a r a n c e of gills varies w i d e l y within the family A m p h a r e t i d a e
(and within A l v i n e l l i n a e / A l v i n e l l i d a e ) , a s e c o n d s p e c i e s h a v i n g s m o o t h b r a n c h i a e ,
Amphicteis gunneri, w a s s e c t i o n e d for c o m p a r i s o n in this study.
MATERIAL AND METHODS
Alvinella pompejana w a s c o l l e c t e d at a d e p t h of 2600 m at 12 ° 48' N a n d 103 ° 56' W
b y the r e s e a r c h s u b m e r s i b l e " C y a n a " . After retrieval to t h e surface, small p i e c e s of t h e
animals w e r e fixed with 0.4 c a c o d y l a t e - b u f f e r e d g l u t a r a l d e h y d e (3 % final c o n c e n t r a tion) at p H 7.2 a n d t h e n p o s t - f i x e d with o s m i u m tetroxide ( 1 % final concentration). T h e
m a t e r i a l w a s e m b e d d e d in Durcopan.
Amphicteis gunneri w a s collected in the K a t t e g a t b y the r e s e a r c h v e s s e l ,,Poseidon".
Pieces w e r e 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-fixation with 1 % o s m i u m tetroxide, t h e tissue w a s d e h y d r a t e d in e t h a n o l a n d
e m b e d d e d in Araldite.
Thin sections w e r e s t a i n e d for 5 m i n with u r a n y l a c e t a t e ( s a t u r a t e d solution in 70 %
methanol) a n d for a further 5 min in l e a d citrate (Reynolds, 1963). The sections w e r e
e x a m i n e d in a Zeiss EM 9-S2 a n d Zeiss EM 10 C microscope.
RESULTS
Feeding appendages
The f e e d i n g a p p e n d a g e s of Alvinella pompejana are retractile a n d filamentous.
Their s u b e p i d e r m a l core contains a c o m p l i c a t e d m u s c u l a t u r e w h o s e m a j o r c o n s t i t u e n t s
are l o n g i t u d i n a l m u s c l e cells in t h e c e n t r e a n d t r a n s v e r s e m u s c l e cells that l i n k a c i l i a t e d
a r e a with the o p p o s i t e side (Fig. la). Additionally, t h e r e a r e o b l i q u e m u s c l e ceils a n d
muscle cells s p a n n i n g the i n n e r a n d o u t e r e d g e s of t h e groove. T h e f r a m e w o r k of t h e
muscle cells m a y b e filled with a m e b o c y t e s , r a t h e r h o m o g e n e o u s b l o o d cells (Fig. 5d)
a n d b y single h a t - s h a p e d cells w h i c h cannot b e i n t e r p r e t e d with c e r t a i n t y from our
limited material. Their c o n d e n s e d n u c l e u s w h i c h is a s s o c i a t e d with m i t o c h o n d r i a suggests that t h e y c o u l d r e p r e s e n t e x t r e m e l y m o d i f i e d s p e r m ceils. Since t h e s e p o l y c h a e t e s
successfully o c c u p y t h e e x t r e m e h a b i t a t s of t h e h y d r o t h e r m a t vents, direct t r a n s f e r of
(modified) s p e r m cells s e e m s plausible. I m m e d i a t e l y b e l o w the e p i d e r m i s , c o l l a g e n
fibrils can b e found. T h e ci]iated a r e a occupies n e a r l y one half of a cross-section.
Normally it is c o n c a v e f o r m i n g a l o n g i t u d i n a l groove. T h e w h o l e of the t e n t a c l e
e p i d e r m i s is p r o v i d e d with s e c r e t o r y cells b e l o n g i n g to s e v e r a l types. The cuticle of
these a p p e n d a g e s is r e l a t i v e l y thin (1-2 ~m), p e n e t r a t e d b y n u m e r o u s microvilli a n d
c o v e r e d by typical e p i c u t i c u l a r p r o j e c t i o n s (Fig. 2a, b). Often, t h e fibrils follow a
sinusoidal p a t h (Fig. 2a). In the c i l i a t e d g r o o v e the s h a p e of t h e cells r a n g e s from flat (in
the centre) to prismatic (in the m a r g i n a l position). T h e i r cilia are c o n s t a n t l y of the
312
V. S t o r c h & F. Gaill
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 f o r m u l a . T h e i r r o o t l e t s a r e i n s e r t e d at a n a n g l e of a b o u t 45 ° to t h e
s u r f a c e (Fig. 3 a - c ) a n d a r e a r r a n g e d m o r e or less p a r a l l e l to o n e a n o t h e r . T h e 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 b y 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 w i t h a v e r y d i s t i n c t i v e
u l t r a s t r u c t u r e (Fig. 3d). T h e i r cristae a r e o f t e n 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 o r i e n t a t i o n . 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 h e s a m e t y p e c a n b e f o u n d
in t h e b a s a l p o r t i o n of t h e s e cells, w h e r e a s t h e r o u n d n u c l e u s is l o c a t e d centrally, 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 a m e n t s . O u t s i d e t h e c i l i a t e d g r o o v e ,
s u p p o r t i v e cells, s e c r e t o r y a n d r e c e p t o r cells d o m i n a t e .
Feeding appendages
a n d gills of Alvinella
313
Fig. 3. Alvinella pompejana. Ciliated groove (a-d) and gill (e). M: s u b e p i d e r m a l muscle cell, R:
rootlets of cilia, Sc and Sd: secretory cells, a Low power micrograph of ciliated groove (2400: 1); b
Cuticle, basal bodies a n d ciliary rootlets (R) (9500: 1); c Ciliary rootlets a n d secretory cell (S~) (9500:
1); d mitochondria of ciliated cells in groove (19 000: 1); e mitochondria of gill epithelium (19 000: 1)
314
V. Storch & F. Gafll
T h e s u p p o r t i v e cells are prismatic, b u t h a v e an i r r e g u l a r outline, w h i c h is due to
their n e i g h b o u r i n g cells (see below). Their n u c l e u s is e l o n g a t e d , a n d in a central
position. Apically, t h e s e cells h a v e m a n y d a r k m i t o c h o n d r i a , w h i c h differ c o n s i d e r a b l y
from the a f o r e m e n t i o n e d m i t o c h o n d r i a of t h e ciliated cells (Fig. 5c). Dictyosomes comp o s e d of a b o u t 10 cisternae, single c i s t e r n a e of the r o u g h e n d o p l a s m i c reticulum,
l o n g i t u d i n a l l y a r r a n g e d b u n d l e s of filaments, a n d vesicles of different sizes c o m m o n l y
occur in t h e cytoplasm.
S e c r e t o r y cells can b e classified as follows:
(a) In this c o m m o n cell t y p e the r o u g h e n d o p l a s m i c r e t i c u l u m is a r r a n g e d as
c i s t e r n a e a n d o c c u p i e s most a r e a s of t h e c y t o p l a s m (Fig. 4a-c). D i c t y o s o m e s are a r r a n g e d
in the vicinity of the c e n t r a l cell nucleus. T h e s e c r e t o r y p r o d u c t s are electron d e n s e a n d
globular. T h e m i t o c h o n d r i a a r e l a r g e a n d dark; a g a i n t h e s e o r g a n e l l e s differ from that
p r e v i o u s l y d e s c r i b e d . If the b u l k of t h e s e c r e t o r y p r o d u c t s w e r e not l o c a t e d basally, a n d
if t h e s e cells h a d an o p e n i n g into the cuticular face of the i n t e g u m e n t , then the
ultrastructure of this cell t y p e w o u l d c o r r e s p o n d to a w i d e s p r e a d cell t y p e within m a r i n e
i n v e r t e b r a t e s {Storch & Welsch, 1972).
In fact, t h e s e cells w e r e n e v e r f o u n d to r e a c h the a p i c a l surface of the epithelium.
(b) T h e c y t o p l a s m of this cell t y p e is d o m i n a t e d b y the s e c r e t o r y p r o d u c t a n d Golgi
fields w h i c h a r e c h a r a c t e r i z e d b y e l e c t r o n - l u c e n t a n d a l t e r n a t i n g e l e c t r o n - d e n s e a r e a s
(Fig. 4d, e). T h e g e n e r a l outline of t h e s e cells is v e r y irregular. The r o u n d nucleus is
l o c a t e d in the l o w e r third.
(c) A n o t h e r cell t y p e contains g l o b u l a r s e c r e t o r y d r o p l e t s w h i c h a r e p a c k e d close
together. E l e c t r o n - d e n s e dots are d i s t r i b u t e d all over the secretion, w h i c h is of m e d i u m
e l e c t r o n - d e n s i t y (Fig. 3c). T h e n u c l e u s is l o c a t e d basally, the s e c r e t o r y p r o d u c t is the
p r e d o m i n a n t f e a t u r e of t h e cell.
(d) This cell t y p e is slender; its cell b o d y c a n b e l o c a t e d in the s u b - e p i t h e l i a l tissue
e x t e n d i n g a p r o c e s s to the surface. T h e n u c l e u s o c c u p i e s a b a s a l or l a t e r a l position and is
s u r r o u n d e d b y a rim of cytoplasm. T h e distal p a r t of t h e cell is d o m i n a t e d b y electrond e n s e s e c r e t o r y droplets.
G r o u p s of a b o u t six i n t e r s p e r s e d s l e n d e r b i p o l a r cells with a p i c a l cilia (about 10 p e r
cell) can b e found. T h e cilia t r a v e r s e t h e cuticle (Fig. 5a, b) a n d are of the o r d i n a r y 9 + 2
pattern. Below their b a s a l b o d i e s m a n y m i t o c h o n d r i a occur (Fig. 5b), w h i c h are less
d e n s e than those of the s u p p o r t i v e cells. In the i m m e d i a t e vicinity of the r e c e p t o r cell
a g g r e g a t i o n s , a single s e c r e t o r y cell with a v e r y light secretion occurs (Fig. 5b). N e r v e
cell p r o c e s s e s can b e found in a b a s i e p i t h e l i a l position.
Gills
T h e gills differ c o n s i d e r a b l y from the f e e d i n g a p p e n d a g e s . This a p p l i e s to their
s h a p e a n d to their ultrastructure. T h e y a r e p i n n a t e , b e a r i n g v e r y m a n y thin outgrowths.
Their cuticle is thick (5 ~tm) in their c e n t r a l stem (Fig. 2c), b u t e x t r e m e l y thin (0.5 ~tm) in
the p i n n u l e s (Fig. lb). T h e cuticle of the s t e m is similar to the one d e s c r i b e d from the
dorsal side of t h e b o d y (Gaill & Bouligand, 1985). Fibrils a r e a l i g n e d a l o n g r i g h t - h a n d e d
or l e f t - h a n d e d helices a r o u n d the organ. Ultrastructurally, t h e y r e s e m b l e the gills of
Terebellides as d e s c r i b e d b y Storch & Alberti (1978), w h i c h m e a n s that their epidermis is
v e r y irregular, i n f o l d e d in c i r c u m s c r i b e d a r e a s g i v i n g t h e b l o o d access to a s p a c e coming
Feeding appendages
a n d gills 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)
316
V. S t o r c h & F. Gaill
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 t h e e x t e r n a l m e d i u m . T h e s e i n f o l d i n g s a r e r e g u l a r l y a r r a n g e d , a n d the
b l o o d s p a c e is n o t l i n e d by a n e p i t h e l i u m of m e s o d e r m a l origin. A g a i n , this is a c a s e of
an a n n e t i d w i t h a n o p e n b l o o d v a s c u l a r s y s t e m . T h e e p i t h e l i a l cells h o u s e 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 , w h i c h a g a i n differ in t h e i r u l t r a s t r u c t u r e (Fig. 3e). S e c r e t o r y
F e e d i n g a p p e n d a g e s a n d gills of Alvinella
317
cells of the goblet cell type a n d groups of bipolar ciliary receptor cells occur on the gills.
The basal part of the gills c o n t a i n muscle cells in their core.
The gills of Amphicteis gunneri are long a n d smooth a p p e n d a g e s with thick cuticle
(5-7 ~tm). At its surface, it carries epicuticular projections, w h i c h are similar to the ones
described from Alvinella pompejana (Fig. 2d). T h e e p i t h e l i u m is c o l u m n a r a n d u n d e r lain with a thick layer of muscle cells.
DISCUSSION
The p r e s e n t investigation has s h o w n that the so-called gills of Alvinella pompejana
a n d Amphicteis gunneri are so different in their ultrastructure that their f u n c t i o n can by
no m e a n s b e identical. The gills of Amphicteis gunneri have a very thick cuticle a n d
prismatic epidermis cells which are u n d e r l a i n with m u s c u l a t u r e . Thus, they do not fulfil
the d e m a n d s of respiratory epithelia which are composed of flat cells that allow ~as
e x c h a n g e across the body surface m e r e l y b y diffusion. O n the other h a n d i n the gills of
Alvinelta pompejana, the distance b e t w e e n the i n t e g u m e n t a l surface a n d the subepidermal blood spaces c a n b e as small a 1 ~tm. This v a l u e corresponds to e x t r e m e cases
reported for other polychaetes (Storch & Alberti, 1978). This is of the same m a g n i t u d e 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 b o r d e r e d b y e p i t h e l i o m u s c u l a r cells.
(b) gills with partly o p e n e d vessels. T h e vessels are no l o n g e r t u b u l a r c h a n n e l s , b u t
open out in the direction of the epidermis.
(c) gills with blood spaces directly b e l o w the surface epithelium, which are not l i n e d
by coelothelial cells.
(d) gills with blood spaces b u l g i n g deeply into the surface epithelium. Here, the
greatest reduction of the distance b e t w e e n blood a n d water has b e e n achieved. This lastm e n t i o n e d type was found in Alvinella pompejana.
Furthermore, it has to be m e n t i o n e d that epibiotlc bacteria are a b s e n t from the gills
a n d feeding tentacles of Alvinella pompejana. It seems that the p r e s e n c e of sea w a t e r
does not allow their colonization. The worms g e n e r a l l y stay inside their tubes, only their
buccal part b e i n g in contact with the a m b i e n t water.
The f e e d i n g tentacles are characterized by several k i n d s of e p i d e r m a l secretory
cells. As in other m a r i n e invertebrates, these cells exhibit varied ultrastructures. Their
function, however, r e m a i n s to b e elucidated. In AnaitJdes mucosa, H a u s m a n n (1982)
found m a n y k i n d s of m u c o u s cells, b u t could not explain their function. O n sectional
preparations, one c a n n o t e v e n see w h e t h e r they, in fact, correspond to different cell
types, or w h e t h e r they m e r e l y r e p r e s e n t different phases of m a t u r a t i o n of o n e cell type.
In our opinion, the ER-rich cell type differs principally from the others a n d all other
secretory cells described so far for m a r i n e i n v e r t e b r a t e s from the point of view of their
upside down position. That it is in such a position raises d o u b t as to how the secretory
products are extruded. Since they always s e e m to b e located a d j a c e n t l y to a b a s i e p i t h e lial nerve plexus, their function m a y b e associated with n e r v o u s activity.
Another u n u s u a l feature is the ultrastructural diversity of m i t o c h o n d r i a in different
cell types. Our results indicate that there is good r e a s o n to believe that this diversity is a n
expression of their equally diverse tasks.
318
V. S t o r c h & F. Gaill
H o w e v e r , c o n c e r n i n g the secretory cells a n d the mitochondria, our investigation
which was based on limited material has produced more questions than anticipated, and
can only be confirmed by further comparative and experimental studies.
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