C
The vascular anatomy of the Annelid worms has, in
general, been little studied. This is especially true of
marine worms of the class Polychaeta. The errent polychaetes
(Errantia) seem to have received most of the attention; there
are, for example, very adequate studies of the families
Nephtyidae and Nereidae. The sedentary forms (Sedentaria)
and those forms which cannot be easily placed into either
grouping have generally escaped serious study. A prime
example of this lack is the more or less sedentary family
Cirratulidae. A detailed study of the vascular anatomy of
Chartozone was done by Meyer in 1887; more general works
exist on Audorina filagera and Cirratulus Setosa (Claparede,
1873), Cirratulus cirratus (Picton, 1898 and Courtney, 1958),
Dodecaceria concharum, and Audorina tentaculata (Courtney,
1958).
Cirriformia spirabrancha (Moore, 1904) is a member of
this family in which the vascular anatomy has not been
examined. In order to add to the limited knowledge of
polychaete vascular anatomy, and also for the challenge and
enjoyment of working with a completely unexamined species,
g. spirabrancha was chosen for this study. The vascular
organization, blood flow pattern, and blood vessel structure
have been examined in detail.
MATERIALS AND METHODS
Specimens of C. spirabrancha were collected from shallow
mud flats near the Municipal Pier, Monterey, California.
The course of all the major vessels and most of the
smaller branches was traced by dissection under a binocular
dissecting microscope. Doubtful connections between vessels
and the course of smaller ones were confirmed by the
examination of serial sections.
For dissection, the worms were lightly anesthetized in
a solution of magnesium chloride and seawater. The region
of dissection was then painted with 1% novocaine, permitting
extensive surgery without excessive muscular stimulation.
The anesthetized worms, when dissected, were allowed to revive
in fresh seawater. The vessels thus exposed continued to
exhibit what was assumed to be normal contractile behavior
for periods of one hour or more. To determine flow patterns,
india ink was injected into the vessels at various points. In
most cases, the india ink quickly settled on the vessel wall
near the point injected. However, a few specks would
occasionally remain in solution, allowing observation of flow.
For microscopic examination, the worms were fixed in
Bouin's fluid and the sections stained with the Foote-Goldner
modification of Masson's trichrome (Jones, 1950).
RESULTS
The vascular system in C. spirabrancha, as in most
polychaetes, can be viewed as a combination of two general
systems: a typical replicating segmental system, and a
longitudinal system which is superimposed upon the segmental
system.
The segmental system generally consists of a series of
contractile vessels which move blood through a roughly
circular pathway within each segment. The major vessels
of this system (see Figure 1,A) are the ventro-lateral
vessels (VL), the dorso-lateral vessels (DL), the medio¬
lateral vessels (ML), the medio-ventral vessel (MV), and
the branchia supply vessels (BS).
The longitudinal system consists of five major vessels
(see Figure 1,A): the dorsal vessel (DV), the supra-esophageal
vessel (SV), the ventral vessel (VV), and paired lateral
vessels (LV). These vessels communicate indirectly with
each other through the segmental system except in the
modified anterior segments and the pygidium, where the
dorsal and ventral vessels communicate directly in the
terminal anal segmental ring.
Proceeding along the longitudinal axis of C. spirabrancha,
variations appear in the vascular anatomy of both the
longitudinal and segmental systems. These differences appear
principally between the anterior, central, and posterior
sections of the worm. For purposes of discussion, these
sections are labelled I, II, and III.
Section I refers to the prostomium and anterior segments
1-7. This section is characterized by the extensive modification
of both the longitudinal and segmental vascular systems and
by the presence of dorsally placed branchia on segment 6.
Section II refers to the fully developed central
portion of the worm, segments 10 through 200 (approximately).
Despite minor variations in individual segments, the
organization of the vascular anatomy here follows a consistent
pattern. At the posterior end of this region, the
longitudinal system is reduced by the joining of the dorsal
and supra-esophageal vessels. Lateral branchia occur in
almost every segment in this section.
The posterior 100 (*) segments and the pygidium are
referred to as Section III. Here, four longitudinal vessels
are superimposed upon a segmental system which is similar to
that of Section II. The major difference is a progressive
simplification of the segmental system, proceeding posteriorly.
A. Vascular Anatomy
The dorsal vessel, suspended in a thin connective tissue
mesentary below the dorsal muscle band, is continuous through¬
out Sections II and III. In Section II, a loose, spongy,
intravasal organ commonly called the heart body is present.
In a study of the heart body in polychaetes, Picton (1898)
ascribed a mechanical function to the dorsal vessel in
Cirratulids. It is not unreasonable to apply this conclusion
to C. spirabrancha, since at systole, the lumen is completely
obliterated by the contraction of the walls against the
heart body. Kennedy and Dales (1958) examined the heart body
in a related species, Audorina tentaculata, by long paper
chromatography of extracts and other methods. They concluded
that in addition to the possible mechanical function, the
heart body is also a haematopoetic organ.
The dorsal vessel is not continuous through Section I.
It tapers somewhat in segments 9, 8, and 7, and in segment 6,
the lateral vessels (LV) branch off from it. The dorsal vessel
itself then bifurcates to form the dorsal branchia vessels (DBV).
In its course through Section II, the dorsal vessel is
about 5 mm. in diameter, narrowing to 2 mm. when passing through
a septa. It is directly connected to the supra-esophageal
vessel (SV) in each segment by a thin-walled vessel just
posterior to the septa.
At the posterior end of Section II, the dorsal vessel
joins vessel SV and, throughout Section III, communicates
directly in each segment with the capillary net about the
gut and with vessel DL (see Figure 1,B).
Vessel SV, lying just ventral to the dorsal vessel and
directly above the gut is continuous throughout Section II.
In each segment, one, two, or three small vessels branch from
it and supply a capillary network about the gut. On the
posterior side of each septa, the medio-lateral vessels
(ML) branch off from vessel SV and proceed laterally,
joining vessel DL. In Section I (see Figure 2), vessel
SV continues beyond the terminus of the dorsal vessel. In
segment 4, two small vessels branch from it and enter the
dorsal muscle mass. In segment 1, vessel SV branches, again,
the dorsal branch bifurcating to form the dorsal prostomial
vessels (DPV); the ventral branch forming the supra- pharyngeal
vessel (SPV). Vessels DPV supply the extensive capillary
network in the body wall of the prostomium. Vessel SPV
opens into the capillary net surrounding the pharynx.
The circum-oral vessels (CO) drain these capillary
networks and in segment 1, join to form the ventral vessel
(VV). In segments 1-5, the ventral vessel receives blood
from the lateral branchia through the latero-ventral
vessels (LV). These branchia are supplied from a small
vessel (ST) which runs along the exterior wall of the pharynx
and drains the capillary network surrounding it. In segment
2, a branch proceeds dorsally from the ventral vessel, then
bifurcates to form two smaller vessels which run to the
individual nephridia.
After the lateral vessels (LV) branch from the dorsal
vessel in segment 6, they proceed ventrally to the lateral
midline and then continue posteriorly throughout Sections
II and III. These vessels usually terminate in blind endings
approximately five segments anterior to the pygidium. In each
segment, a branch from the lateral vessel (LV) either
enters a branchia, if one is present, or ends abruptly at
the body wall.
As mentioned above, the segmental vascular organization
throughout Section II repeats itself in each segment (see
Figure 1,A). The medio-lateral vessels (ML) run from vessel
SV to vessels DL which lie just inside the dorsal muscle
band. Vessels DL connect dorsally to vessels PV, a pair
of small vessels which run the length of the worm. Vessels
PV supply both the dorsal muscle band and the dorsal body
wall through a series of small branches. Vessels DL run
ventrally from their connections with vessels ML, joining
vessels LV and the efferent branchial vessels in small
bulbs near the lateral body walls. Vessels LV run from these
bulbs to the ventral vessel (VV) with small branches supplying
both the ventral and lateral muscle bands. In each segment,
the gut capillary plexus is supplied from vessel SV and drains
into the sub-esophageal vessel (SIV) which runs directly to
the ventral vessel.
In Section III, the segmental vascular pattern is
repeated as above, but there appears to be a general gradation
of development from the fully developed segments of Section
II posteriorly to the pygidium. Figure 1,B is a diagram of
a section through a typical posterior segment. Here the
segmental vessels connect directly to the dorsal vessel
and vessel ML connects directly to vessel PV. In the most
0
posterior segments of this section, both vessels PV and DL
are lacking; vessels ML connect directly to vessels LV.
Ventrally, vessel SIV is not present; it is replaced by a
direct connection between the gut plexus and the ventral
vessel.
B.
Flow Patterns and Vascular Activity
The general pattern of flow through the vascular system
of C. spirabrancha is a partial interdigitation of two
sub-patterns. The intra-segmental pattern of flow is generally
circular. Blood moves ventrally from vessel SV through the
gut plexus to the ventral vessel, then flows dorsally through
vessel LV and vessel DL. Flow is then latero-medial through
vessel ML back to vessel SV. Superimposed upon this pattern
is the rather sluggish dorsal-anterior to ventral-posterior
longitudinal flow pattern.
The actual volume displacement, and in some vessels the
direction of flow, is dependent upon the activity of the
animal. The motivating force for blood flow is supplied
by local contractions of muscular vessels walls. The activity,
spreading along a vessel as a contractile wave, causes
displacement of a volume of blood from one portion of the
system to another. These contractile waves are irregular
and frequently conflict with one another. Injury or
irritation to a vessel at any point will set up contractile
waves in both directions. This may cause flow to cease
or to be reversed.
The dorsal longitudinal vessel is the main contractile
vessel. The peristaltic waves which pass along it originate in
the segments just anterior to the terminal anal segmental
ring and sweep cephalad. In Section II, both the supra¬
esophageal vessel (SV) and the dorsal vessel are involved,
contracting simultaneously. As the contractile wave reaches
the junction of vessels LV and DBV with the dorsal vessel,
blood flows into both the dorsal branchia and the lateral
vessels. In vessel SV, the wave of contraction ceases near
segment 9 and only slight contractions are observed anterior
to this.
In an unanesthetized worm which has been secured to a
dissecting pan in such a way that only limited movements are
possible, blood flow in the non-contractile ventral vessel
is scarcely perceptible. Flow here is probably dependent
almost exclusively on body movements. In the lateral
vessels (LV), contractile waves have not been observed, and
blood flow here is probably also dependent upon body movements.
The flow into and out of the lateral branchia appears to
result from the extension and contraction of these organs.
When the branchia are severed close to the body wall, blood
flow from the body through the open vessels is minimal;
however, when the distal end of the organ is removed, blood
flows quite readily.
2
C. Histology of the Blood Vessels
With the exceptions of the ventral and lateral vessels,
the blood vessels of C. spirabrancha are all contractile.
Hanson (1949) stated that the blood vessel walls of Polychaetae
and Oligochaetae are composed of three layers: (1) an
endothelium occasionally appearing as a continuous layer,
(2) a layer of collagenous connective tissue, and (3) an
outer peritoneal layer, either differentiated into a muscle
coat, or, more often, with contractile fibers in the tails
of stellate cells. Most of the blood vessels in this species
follow this basic plan. Stellate cells occur on the walls
of all segmental vessels and on the walls of the vessels
within the branchia.
A heavy muscular coat surrounds both the lateral vessels
and the dorsal vessel. A thin band of connective tissue and
a thin endothelium occur in the dorsal vessel; a thick layer
of connective tissue occurs in the lateral vessels. The walls
of the supra-esophageal vessel are composed of only two
distinct layers: a connective tissue layer and a peritoneal
layer of occasional stellate cells with contractile fibers
radiating from them.
DISCUSSION
Although the blood vascular system of C. spirabrancha
follows the general pattern of closed circulatory systems found
in the class Polychaetae, it provides several anatomical
surprises. The lateral vessels, found only in certain other
8
Cirratulids, are especially interesting. Superimposed upon
the general dorsal-anterior, ventral-posterior longitudinal
flow pattern with its segmental interconnections, these
vessels make up a "sub-system" concerned specifically with
providing the lateral branchia with a constant blood supply.
The efferent vessels in these branchia lead directly into
vessel LV. Here the blood is able to mix with blood moving
dorsally in the segmental system. This provides a reasonably
efficient system for the supply of oxygenated blood to the
various tissues. This "sub-system" does not appear homologous
to any of the branchial supply systems found in the other
polychaetes reviewed.
Another interesting feature of the vascular anatomy of
C. spirabrancha is the anterior extension of the supra¬
esophageal vessel which supplies the capillary network of
the pharynx and prostomium. In a closely related species,
A. tentaculata, Courtney (1958) described a direct connection
of the supra-esophageal vessel with the dorsal vessel in
segment 7. The dorsal vessel, rather than terminating as
in C. spirabrancha, proceeds anteriorly to supply these
capillary networks. Due to the cursory nature of Courtney's
paper, this connection may have been misinterpreted in
A. tentaculata; however, anatomical differences of this sort
do exist in closely related species of other families of
polychaetes.
Although there are some 70 (f) branchia present in
14
an individual worm, only five to ten of these are exposed
above the substrate surface at any one time. No particular
ratio of exposure could be established between the two
different types. This presents an interesting problem,
since these two types of branchia appear to differ only in
vascular anatomy. No special experiments were performed to
determine if any functional differences existed. When the
worm is exposed to an anaerobic environment, however, it
has been observed that the lateral branchia become turgid
with blood, while the dorsal branchia maintain their normal
ebb and flow. This would seem to indicate that the lateral
branchia are more efficient respiratory organs, since a much
greater amount of blood is thus exposed for gas exchange.
Considered from a functional standpoint, the total
circulation in C. spirabrancha does not present itself
as a very efficient process. The lack of valvular structures
in the connectives of the lateral vessels (LV) and the dorsal
branchial vessels (DBV) with the dorsal vessel is particularly
interesting.
Blood flow into both the lateral vessels and the dorsal
branchia must be very nearly random. Blood returning to the
dorsal vessel from the dorsal branchia may flow into the
lateral vessels, back into the dorsal vessel, or even
return to the dorsal branchia. Flow into the lateral vessels
is also uncontrolled. Since the lateral vessels are probably
important in respiration, this is not particularly favorable.
18
Blood is supplied to the prostomium and pharynx from
the supra-esophageal vessel. This is a remarkedly inefficient
means of providing freshly oxygenated blood to these tissues,
since no direct connectives exist between any of the branchia
and this vessel. It is likely that this problem is solved
by a rapid movement of blood into this area. Evidence for
this conclusion is limited, but it has been observed that
when the prostomium is removed from intact worms, profuse
bleeding occurs.
An attempt was made to compare the vascular anatomy of
C. spirabrancha to that of other members of the family
Cirratulidae. The literature on the family is quite limited
and the works which do exist are generally cursory and
incomplete. Therefore, although the vascular anatomy
exhibits certain similarities to that described for both
A. tentaculata and C. cirratus, the dissimilarities between
these three species and the others studied are such that no
general scheme for the family can be described.
3.
4.
SUMMARY
1. The anatomical organization of the vascular system of
g. spirabrancha has been studied in detail. Blood flow
patterns and the fine structure of the blood vessels
were worked out.
The most striking observation was the discovery of a very
specialized branchial supply system. This system consists
of a pair of non-contractile lateral vessels which branch
from the dorsal vessel in segment 6 and run posteriorly
throughout the entire worm. In each segment, branches of
this vessel run into the lateral branchia.
No mechanical heart or hearts were found. The circulation
of blood appears to occur as a result of a combination of
three factors: contractile waves moving cephalad in the
dorsal and supra-esophageal vessels, local contractions
moving along individual vessels, and movements involving
the entire worm.
The main flow patterns are shown to consist of an
interdigitation of two circulatory systems, one a primitive
segmental type, and the second a posterior-anterior flow
involving the whole worm. Neither system is independent
of the other and no valvular structures were found. The
result is that actual flow is often sluggish and quite
inefficient in most of the worm.
5. An intravasal structure called the "heart body" was found
16
6.
in the dorsal vessel. Similarities in the structure of
this organ in C. spirabrancha and in related species in
which the pigments from this organ have been studied lead
to the conclusion that this may be a haematopoetic organ.
The histology of the contractile blood vessels has shown
them to be similar in structure to the contractile vessels
in other polychaetes.
ACKNOWLEDGEMENTS
This work is supported in part by the Undergraduate
Research Participation Program of the National Science
Foundation, Grant GY-4369.
Special thanks are extended to the staff of the Hopkins
Marine Station of Stanford University for the assistance
and quidance afforded me during my research.
LITERATURE CITED
Claparéde, E., 1873. Recherches sur la Structure des
Annélides Sédentaires. 199 p. Geneve: Georg.
Courtney, W.A.M., 1958. Certain Aspects of the Biology
of the Cirratulid Polychaetes. PhD Thesis, University
of London.
Hanson, Jean, 1949. The Histology of the Blood System in
Oligochaeta and Polychaeta. Biol. Reviews, Cambridge
Philos. Soc., 24;2: 127-173.
Jones, Ruth M., ed., McClung's Handbook of Microscopic
Technique, 3rd edition, Hafner Pub. Co., N.Y., p. 249.
Kennedy, G.Y. and Dales, R.P., 1958. The Function of the
Heart-body in Polychaetes. J. Mar. Biol. Ass'n. U.K.,
37, 15-31.
Meyer, E., 1887. Studien über den Körperbau der Anneliden.
Mitt. Zool. Sta. Nepal, Bd. 7:592-741.
Picton, L.J., 1898. The Heart-body and Coelomic Fluid of
Certain Polychaeta. Quat. J. Mier. Sci., 41: 263-302.
C
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FIGURE LEGENDS
Figure 1. A. Gross section of a typical segment in Section
II. Semi-diagrammatic. DV, dorsal vessel; PV, small
longitudinal vessels; ML, medio-lateral vessel; SV, supra¬
esophageal vessel; DL, dorso-lateral vessel; BS, branchial
supply vessels; LV, lateral vessel; SIV, sub-intestinal vessel;
VV, ventral vessel; LB, lateral branchia; GP, gut capillary plexus.
B. Cross section of a typical segment in Section III. Vessels
marked as in A.
Figure 2. Semi-diagrammatical sketch of the anterior portion
of C. spirabrancha (Section I). Vessels marked as in Figure 1
except for: MV, medio-ventral vessel; DBV, dorsal branchia
supply vessels; SPV, supra-pharyngeal vessel; DPV, dorsal¬
prostomial vessel; CO, circum-oral vessel; ST, small vessel
supplying anterior lateral branchia; M, mouth; DB, dorsal
branchia; HB, heart body; NP, area in which the nephridia lie.