A M . ZOOI-OUST, 9:857-868 (1969).
A Comparative Study of Bivalves Which Bore Mainly
by Mechanical Means
ALAN D. A.NSELL
Marine Station, Millport, Isle of Cumbrae, Scotland
and
N. BALAKRISHNAN NAIR
Marine Biological Laboratory and Aquarium, Trivandrum 7, South India
SVNOI'SIS. This account of the boring mechanisms of those bivalve groups which bore
mainly by mechanical means attempts to show partly by reference to published
accounts of boring and partly from our own recent observations of certain characteristics of the boring process in the Pholadidae and Petricolidae, that in contrast to the
movements of burrowing forms from which originally all the boring movements derive,
the process of boring makes few demands on the hydrodynamic system of the
bivalve. The characteristics of the boring process are closely related to the movements
in modern forms having epifaunal or infaunal habits, supporting the suggestions of
Yonge (1963) concerning the origin of this habit in the Bivalvia. In all groups in
which boring is mechanical, the shell forms the boring tool. However, in those groups
in which boring has its origin in the epifaunal habit, the major force applied to the
shell in abrading the burrow is provided by contractions of the pedal or byssal
retractor muscles. In the Adesmacea alone, where boring has been derived from a deep
burrowing habit, the adductor muscles provide the major force in abrasion, and
the basic digging cycle has become specialized by the addition of the rocking action of
the valves which succeeds retraction. In the former group the ligament is retained and
provides the strong outward force with which the shell is held against the wall of the
burrow. In the latter group, the ligament is reduced, allowing the valves to rock, but
here the reciprocal action of the adductors allows the valves to diverge anteriorly as
the large posterior retractor muscle contracts. In the more specialized species, water
pressure plays a minor role, the maximum pressures recorded being associated with
actions subordinate to those involved primarily in abrasion, such as rotation in the
burrow or expulsion of debris from the burrow as pseudofeces. The least specialized
borers, such as Petricola, resemble burrowing forms in the importance of the
hydrodynamic role of the body fluids. In all groups there is a tendency for hypertrophy to take place in the muscles which produce the main boring effect, and for their
action to be applied with maximum mechanical advantage against a fulcrum provided
in most cases by the foot.
The literature on the molluscs abounds
in descriptions of the boring mechanisms
of individual bivalve species. For all the
major groups there have been perhaps as
many theories of the mechanism of boring
as there have been investigators, which is
not surprising because most rock borers are
difficult to observe undisturbed in situ,
boring activity normally takes place only
infrequently, and most species fail to reform a burrow in hard substrates when
forcibly removed.
A review of the considerable literature
shows that almost without exception the
descriptions of boring activity and conclusions concerning the mechanisms involved
are based on visual observations unsupported by recording, and indeed that many
theories of boring are merely deductions
from observations of morphological structure. Nonetheless, from these observations
a fairly clear picture of variations on the
boring habit in the Bivalvia appears, and
in most cases the major outlines of the
boring process are no longer disputed. The
type of information available, however,
remains largely qualitative, and many
statements of details are imprecise.
857
858
A. D. ANSELL AND N. BALAKRISHNAN NAIR
Until recently a somewhat similar situation existed with relation to the much
more abundant and varied burrowing bivalves, but application of cinephotography
and of modern electronic recording techniques, by means of which activity can be
monitored with little restraint to the animal even when it is buried, and by means
of which such important parameters as the
pressure in the mantle and body cavities
can be measured, has enabled the events of
the burrowing process to be studied in
great detail, and has shown how the bivalve structure operates as a hydraulic machine in penetrating soft substrate—often
very rapidly.
In re-investigating the boring activity of
some bivalves, in clay, in calcareous and
other rocks, and in wood, we have attempted to apply to the study of boring
bivalves similar methods to those used in
these earlier studies of burrowing (for a
review, see Trueman and Ansell, 1969)
with particular reference to the hydrodynamic role of the fluids contained in the
haemocoele and the mantle cavity. In
doing so we hope to consider more critically the many references to the role of water
pressure in boring by members of the Bivalvia. This comparative study of boring
mechanisms is not, however, complete; in
particular it has not yet been possible to
examine examples of all those bivalve
groups which include boring forms, and
for this reason some of the conclusions
presented may be premature. This paper
represents a preliminary attempt to present a unified background against which
further studies of the boring mechanisms
can be made.
habit has been adopted independently in
no less than seven superfamilies of the Bivalvia (Fig. 1). In only one of these seven
superfamilies, the Mytilacea, is boring undoubtedly assisted by chemical means; in
all the others boring is now usually considered to occur by mechanical means alone.
Only those forms which employ chemical
means are restricted to calcareous rocks; in
the other groups, calcareous rocks represent only one of a range of substrates
which may be used.
Yonge considers that the rock-boring
habit has been arrived at by the seven
superfamilies by one or the other of two
routes. In some members of the superfamily Myacea and all members of the Adesmacea the boring habit has been derived from
a primitive infaunal habit, that is, from
animals which burrowed into soft substrata
by using the foot. Their morphological
characteristics became specialized and preadapted step-by-step to allow penetration
of stiffer and stiffer substrata until a true
boring habit was evolved. In the other
groups; Veneracea, Saxicavacea, Gastrochaenacea, Cardiacea (Tridacnidae), and
Mytilacea, the rock-boring habit is regarded
as having been derived from an earlier active epifaunal habit, that is, from types
which were byssally attached throughout
life to hard substrata although retaining
the ability to move over the surface by
means of the foot. It is thus in contrast and
comparison with these two types of bivalve
that we may consider the rock-boring forms.
In particular we should compare the characteristic mode of locomotion, since it is this
habit which has become modified alongside morphological specialization to allow
penetration of harder substrates.
TYPES OF BORING BIVALVE
Yonge (1963) reviewed the occurrence
of the rock-boring habit among marine invertebrates including the bivalves. We
have taken his paper, which described
briefly the boring mechanisms employed by
the various groups of bivalves and the
evolution of this habit, as the starting
point for our discussion. The rock-boring
THE FLUID DYNAMICS OF BURROWING, AND
MODIFICATIONS OF EPIFAUNAL TYPES
The basic features of burrowing into soft
substrata are essentially the same in all
those bivalves which have been studied in
detail. The behavioral pattern involved is
obviously of great antiquity, and we may
assume that the infaunal ancestors of mod-
BIVALVE MECHANICAL BORERS
859
FIG. 1. Examples of rock-boring bivalve molluscs
from the seven superfamilies in which this habit
appears, to show the form of the burrow, the
muscles responsible for abrasion, and the direction
of the major abrasive movements of the shell. A,
Zirphaea crispata (Adesmacea) viewed vertically,
laterally and in cross section. The boring is circular in section because of rotation during boring;
the major abrasive action is by an opening thrust
of the anterior shell margins caused by contraction
of the posterior adductor muscle (after Nair and
Ansell, 1968); B, Platyodon cancellatus (Myacea) ,
viewed laterally, vertically, and in cross section; the
major abrasive action is by rocking of the shell
valves caused by contractions of the adductor
muscles. There is no rotation and the cavity takes
the form of the shell, Horny parts on the siphon
enlarge the diameter of the burrow as growth
proceeds (after Yonge, 1951). C, Botula falcata
(Mytilacea) viewed laterally and in section. The
major abrasive action is by contraction of the
byssal retractor muscles drawing the shell back and
forth in the burrow. There is no rotation, and
the cross section of the burrow takes the form of
the shell (after Yonge 1955). D. Petricola pholadiformis (Veneracea) viewed laterally and in section.
Boring takes place by means of a modified
burrowing cycle, the main abrasive action occurring
when the posterior pedal retractor muscle contracts, drawing the anterior margin of the shell
upward. There is no rotation and the burrow is
slightly oval in section, (after Duval, 1963) . E,
Tridacna crocea (Cardiacea: Tridacnidae) viewed
laterally and in section. Abrasion is by alternate
contractions of the byssal retractor muscles,
drawing the shell downwards onto the byssus attachment (after Yonge, 1936) . F, Rocellaria cuneiformis (Gastrochaenacea) viewed laterally and in
sections. The major abrasive action is by contraction of the anterior pedal retractor muscle, drawing
the anterior margin of the shell downward in
the burrow (after Otter, 1937; and Purchon,
1954). G, Hiatella arctica (Saxicavacea) vif.-wed
laterally and in section. The major abrasive action
is by contraction of the posterior pedal retractor
muscle drawing the anterior shell margins upwards
in the burrow (after Hunter, 1949) .
ern boring forms burrowed in an essentially similar way. During burrowing, a series
of movements involving most of the organ
systems of the body is repeated at intervals
so that the animal penetrates the substra-
tum in a series of steps. During each step,
or digging cycle, the shell is first anchored
by the outward force exerted by the elastic
hinge-ligament while the foot is extended
and probed into the sand. The extended
860
A. D. ANSELL AND N. BALAKRISHNAN NAIR
foot is then dilated, forming a terminal
anchorage, and the shell is drawn downwards by contraction of the pedal retractor
muscles. Dilation of the foot is achieved
by a large increase in pressure in the
haemocoele and mantle cavity caused by
contraction of the adductor muscles of the
shell while the mantle cavity is sealed. The
increase in pressure forces blood into the
foot, and in many bivalves causes a jet of
water to be ejected from the mantle cavity
into the sand, so that downward movement
of the shell is aided by the production of a
fluid-filled cavity immediately adjacent to
the ventral edges of the shell valves.
The haemocoele and the mantle cavity
act in a hydrodynamic role in this process,
as a double fluid skeleton by means of
which the forces generated by the adductor
muscles may be transmitted to the foot to
act in achieving terminal anchorage by exploiting the dilatant properties of the
sand. Maximum pressures in both the
haemocoele and mantle cavity are recorded
as the foot is dilated, and may reach values of up to 100 cm water in specialized
burrowing forms such as Ensis (Trueman,
1967). In contrast, during probing, relatively small fluctuations in pressure (max
10 cm) are observed in the haemocoele as
the intrinsic musculature contracts to cause
repeated thrusts with the tip of the foot.
Figure 2 illustrates these characteristics.
The role of the ligament in burrowing
forms is to open the valves as the adductor
muscles relax and to press the shell valves
outwards, forming the shell anchorage and
consolidating the walls of the burrow. The
ligament thus acts in burrowing as a
mechanism which effectively stores part of
the energy of the adductors for use later in
re-opening the valves. In some burrowing
forms, however, the ligament is not strongenough to open the valves fully against
the compacted sand and, in these, the forces exerted by the ligament are supplemented by pressures developed in the
sealed mantle cavity by a withdrawal of
the siphons or foot which occurs during
the resting period between retractions.
This secondary cycle of siphonal with-
Mm
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foot
siphon
gape
shell
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vi
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An
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vi
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FIG. 2. Above: Diagrams showing the principal
stages in the burrowing of a generalized bivalve,
A, stages i, ii, or vi of the digging cycle (below) with
the valves pressing against the sand by means of the
opening thrust of the ligament to provide a penetration anchor (PA) while the foot is extended in
probing (P) . B, stage iii where contraction of the
adductor muscles (am) ejects water from the
mantle cavity (m) so loosening the sand (c)
around the valves. High pressure simultaneously
produced in the haemocoele (h) gives rise to pedal
dilation to form a terminal anchor (TA) . C,
stage iv, contraction of the retractor muscles (rra)
pulls the shell down into the loosened sand, tm,
transverse pedal muscles, pm, protractor muscle
(after Trueman, 1968) . Below: Diagram summarizing the principal activities of a bivalve during the
digging cycle. Probing of the foot (Foot, solid
rectangle) and pedal dilation (hollow rectangle) ,
duration of closure of the siphons (Siphon) , adduction of the shell valves (Gape) , shell movement, and hydrostatic pressure in the pedal haemocoele are shown in relation to stages i-vi of the
digging cycle. (Pressure, cm water) (after Trueman,
1966).
drawal and extension coupled with pedal
retraction is illustrated in Figure 3. In burrowing forms, the secondary cycle usually
begins when the shell is about half to twothirds buried, and is not apparent during
the earlier digging cycles, suggesting that it
appears as a direct response to increasing
resistance from the sand to the opening of
the shell. A comparable hydrodynamic
relationship occurs in some deep-burrowing
BIVALVE MECHANICAL BORERS
ck»ing
I 30 « c I
FIG. 3. Simultaneous recordings of external pressures (upper traces), valve movements (center),
and event-marker (lower trace, made by visual
observations) of digging cycles (numbered) during
a single digging period of Glycymeris glycymeris. In A, the event-marker shows closing (C) and
opening (O) of the exhalent siphons and, in B,
adduction (AD), the period when the valves are
opening (G), and the contraction of anterior
(RA) and posterior (RP) retractor muscles. F
indicates the secondary cycle referred to in the text
when pedal retraction (and in the case o£
siphonate bivalves, simultaneous siphonate retraction) causes the maximal opening of the valves
(after Ansell and Trueman, 1967).
forms where siphonal retraction causes the
valves to gape, and where, conversely, adduction of the shell valves is a necessary
part of the mechanics of siphonal extension
(Chapman and Newell, 1956). In both
cases, the siphonal muscles act as antagonists to the adductors and we will see that
in this they foreshadow the situation occurring in some boring forms.
In epifaunal species the requirements of
attachment by a byssus to a hard substratum have led to modifications of the foot,
and some of the pedal retractors become
byssal retractor muscles. However, in those
epifaunal bivalves which retain some activity, e.g., Area, the foot retains its role in
locomotion over the surface, and this is
still accomplished by the same complex of
muscular movements although now without the requirements for anchorage except
of the extended tip of the foot. During
861
locomotion, the tip of the foot adheres to
the rock surface with the aid of mucous
secretion, and while there may be some
dilation the pressures involved are small,
and the reduction in shell gape involved is
minimal. The ligament of epifaunal
forms is, in general, no less powerful than
that of burrowing forms, perhaps reflecting
the necessity for an efficient mechanism to
open the valves against the forces set up
by surrounding organisms sometimes in the
confines of a small crevice, but in normal
surface locomotion the ligament is sufficiently strong to open the valves, and there
is no secondary cycle of siphonal and footwithdrawal involved. In contrast to the situation in burrowing bivalves, where digging cycles are repeated until the animal is
buried normally, and where, consequently, a characteristic digging period appears,
in epifaunal species long periods of wandering may occur during which the characteristic locomotory cycle is repeated at
regular intervals (Fig. 4). The maximum
muscle tensions developed in the retractor
muscles of epifaunal species have been
measured since the byssal retractor muscle
forms an excellent experimental material.
Values for maximum tension exerted are
of the order of 2-2.5 kg/cm2 (Hoyle,
1964) and it may be assumed that the
values found reflect the muscle tension
available to both burrowing and boring
forms. In the former, however, the maximum tension exerted during burrowing is
limited by the strength of terminal anchorage which can be produced, and measurements of muscle tensions obtained during
burrowing are generally somewhat lower
than those obtained for isolated muscle
preparations (Trueman, 1967, 1968).
Of the seven superfamilies of the Bivalvia which have representatives which bore,
we shall consider only two in detail, the
Veneracea and the Adesmacea. In the
former group, the borers are included in
the family Petricolidae which includes also
species which nestle in crevices as well as
some which burrow into sand, or mud,
while members of the latter group are all
specialized borers and include the mainly
862
A. D. ANSELL AND N. BALAKRISHNAN NAIR
6
7
8
9
FIG. 4. An extract from a kymograph recording of
the epifaunal bivalve, Area tetragona, during detachment from the byssus and through a period of
locomotion over a solid surface lasting approx-
imately 9.5 hr. The number of movement cycles
per hour remained more or less constant throughout.
rock-boring Pholadidae and woodborers
such as Martesia, Xylophaga, and the
Teredinidae.
members of the Adesmacea such as Barnea Candida also occur. Petricola pholadiformis shows little morphological specialization for boring, apart from the elongated
shell and a development of shell ridges,
especially toward the anterior end. This
lack of morphological specialization is
reflected also in the details of the boring
behavior.
When removed from its burrow, a young
Petricola pholadiformis will reform a burrow in the softer substrates. The movements involved are essentially the same as
the movements of the modified digging cycle used in other bivalves in surface locomotion. Indeed Petricola will burrow
into loose sandy mud and can move over
hard surfaces using the same movements
(Duval, 1963). The burrow extends at an
angle from the surface, and, in boring, the
foot is extended to rest against the ventral
area, acting as a fulcrum against which the
valves are rocked by the contraction of
first the anterior and then the posterior
pedal retractor muscles. During this movement the foot is dilated to form a broad
area of application to the walls of the bur-
BURROWING AND BORING IN
Pclricola
The morphology of different species of
Petricola and the rock-boring habit of this
group have been described by Otter
(1937) for Petricola lapicida, Yonge
(1958) for Petricola carditoides and Purchon (1955) and Duval (1963) for Petricola pholadiformis. Some species show
characteristics intermediate between the
boring forms and the bysally attached and
non-boring members of the Veneracea
such as Venerupis. In the boring forms, a
variety of substrates may be penetrated;
for example, we have recently found a Petricola boring into compacted sand blocks
produced on stone breakwaters along the
Kerala coast of India by the action of a
species of the polychaete genus Sabellaria.
The example we have examined, Petricola
pholadiformis (Fig. ID), is found in Britain boring into stiff mud, hard clay, peat,
chalk, and limestone, often in places where
BIVALVE MECHANICAL BORERS
struction from other cycles in which these events
were marked visually, Q, the pressure in the
mantle cavity; Q., the tension measured by an
isometric myograph attached to the shell. Opening
and closing of the siphons are marked visually
above the trace (5 sec).
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shell
row where adhesion is aided by the secretion of mucus. The shell is held against the
walls of the burrow during pedal retraction by the outward force exerted by the
ligament. The movements involved are
those of a typical bivalve digging cycle,
and in reforming a burrow, such cycles are
repeated at regular intervals for extended
periods. In Figure 5 the activity of Petricola is compared with that of the related
burrowing form, Venerupis pullastra. Two
records of Petricola are shown, one from a
specimen burrowing into sand, the other
from a specimen boring into a consolidated substrate, in this case London Clay.
The close similarity of burrowing and boring movements is apparent from these recordings. In harder substrates such as chalk,
the same type of activity occurs, although
the periods of boring are shorter. This pattern of short periods of boring activity between long periods when the siphons are
fully extended and a feeding current is
maintained, is probably more typical of the
normal situation where the burrow needs
to be enlarged only sufficiently to accommodate the growing animal.
THE BORING MECHANISM OF THE ADESMACEA
FIG. 5. Extracts from recordings of A, Venerupis
pullastra, burrowing in sand; B, Petricola pholadiformis, burrowing in sand; and C, Petricola
pholadiformis, burrowing in London clay. In each
case one cycle of boring or digging activity is shown
together with the events referred to in the text
as the secondary cycle of siphonal withdrawal
and extension. In A are shown simultaneous recordings of the pressure in the mantle cavity (Aj);
the pressure recorded in the sand adjacent to the
burrowing animal (A2), and the tension measured
by an isometric myograph attached to the shell
(A3). Siphonal closure (c) and opening (o)
and the withdrawal (w) and extension (e) of the
siphons are marked visually above the time trace
(5 sec). In B is shown the pressure in the mantle
cavity. Siphonal closure and opening, withdrawal
and extension of the siphons, and adduction and
opening of the shell valves are shown by recon-
The second group of the boring bivalves
which we will discuss are the Pholadidae,
the rock-boring family of the Adesmacea.
Members of this group occupy a range of
substrates varying from clay and consolidated peat, through chalk, limestone, and
sandstone. Calcareous rocks lie at around
the maximum limit of hardness for attack,
as is the case for Petricola and all the
purely mechanical bivalve borers.
The morphological characteristics of the
pholads are well documented (cf. Purchon, 1955a; Turner, 1954). The important characteristics relative to the rockboring habit include the emargination of
864
A. D. ANSELL AND N. BALAKRISHNAN NATR
the shell anteriorly to provide a wide pedal gape, the development of cutting spines
on the anterior faces of the shell, the
presence of accessory shell plates, the reduction or loss of the ligament, and the
reflection of the shell anterior to the hinge
so that the anterior adductor muscle
which is reduced in size and fragmented is
inserted dorsal to the hinge line. The result of this rearrangement, together with
the loss of the ligament, is that the shell
valves can now rock on a dorso-ventral
axis as well as open about the hinge line.
The foot is cylindrical, and the pedal muscles are more or less reduced to a single
pair which are inserted on the apophysis
(=myophore).
We may take as an example of the
Pholadidae the species Zirphaea crispata
(Fig. 1A). In Zirphaea, boring is accomplished by a cycle of movements which we
may call the boring cycle, in which we can
recognize the elements of the digging cycle
described earlier but in which we can also
recognize movements specifically adapted
for boring.
In the boring cycle of Zirphaea the foot
is first protracted so that the shell is
pushed upwards in the burrow. The tips of
the siphons close and the pedal retractor
muscles then contract, drawing the shell
forcibly down to the base of the burrow,
and perhaps causing the pointed anterior
regions of the shell to abrade its end. As
the shell is drawn downwards the shell
gape is reduced. Pedal retraction is followed by rocking of the shell valves about
the dorso-ventral axis, the contraction of
the posterior adductor muscle supplying
the main force used in abrasion at this
stage of the cycle.
Two other types of movement occur between boring cycles. The first of these involves the retraction of the siphons with
their tips closed, a movement which serves
to increase the pressure in the mantle cavity and causes the posterior shell margins to
diverge as the posterior adductor muscle
relaxes. In this movement the siphonal retractor muscles antagonize the posterior
adductor, with the water in the mantle
cavity acting as the fluid in the hydraulic
system. This hydrodynamic relationship is
completely analogous to that noted earlier
as occurring in burrowing forms. With the
shell thus pressed against the wall of the
burrow, a rotation of the animal occurs
first in counter-clockwise and then in a
clockwise direction, these movements also
serving to abrade the burrow. Longer-term
rotations occur which ensure that all faces
of the burrow are equally worked. Finally, the shell valves may be adducted and a
wave of contraction may pass along the
siphons, these movements serving to eject
from the mantle cavity as pseudofeces the
material collected from the base of the
burrow.
Figure 6 illustrates the type of activity
we have recorded during boring by Zirphaea crispata. The uppermost record (A)
shows part of an extended period of boring recorded by attaching an isotonic myograph transducer to the shell of the bivalve
and recording downward movement. Each
boring cycle appears as a major downward deflection of the recording pen while
adduction of the shell also appears as
smaller excursions of the pen. The longterm rotation of the animal in the burrow
is recorded visually above the trace. The
shell first moved counterclockwise through
an angle of 260° in 55 min and then after
a pause of 10 min turned clockwise
through 630° for the next 95 min. Only
part of this movement is shown. The second recording (B), obtained using an
isometric myograph attached to the shell,
shows each boring cycle in greater detail
and illustrates also the association with
each boring cycle of a secondary siphonal
retraction and extension associated with
rotation of the shell. The changes in pressure associated with the boring cycle are
shown in the third recording (C) for
which the pressure was recorded through a
hypodermic needle inserted dorsally near
the pericardium. Visual observations show
the closing and opening of the siphons and
contraction of the accessory ventral adductor muscle and the posterior adductor
muscle. Pressure in the haemocoele rises as
BIVALVE MECHANICAL BORERS
865
al retraction and rotation the maximum
pressures reached were only 3 cm water.
The reduced hydraulic role is accounted
for by the development of hinge systems
allowing direct antagonism of the rearranged elements of the anterior adductor,
the posterior adductor, and the accessory
ventral adductor muscles. Associated with
the reduction of its importance in a hydraulic role, the haemocoele in pholads is
much reduced compared with burrowing
forms or with Petricola, the foot becoming
11111111111 111 i 11 1111 i'T'u i
T I I I I I 1 I I \
filled with a loose spongy connective tissue
which, however, enables it to retain its
form during boring and to press lateroventrally against the walls of the burrow to
form a secure anchorage, with the expanded mantle margins dorsally acting as a
counter pressure.
Our studies of boring in Zirphaea have
been
carried out mainly on specimens re-i—i—i—;—i—i—i—i—i—i—i—T—r
boring into relatively soft substrata. Under
FIG. 6. Extracts from recordings of the activity of
/.irphaea crispata during boring activity. A, isotonic these conditions, while a new burrow is
myographic recording from a partly buried
being completed, long periods of boring
'/.irphaea shows boring cycles repeated at approxiactivity occur with boring cycles repeated at
imately 1-min intervals. Shell rotated 65° counterintervals of as little as 30 sec. Boring acclockwise between 11:30 and 11:55, and then 45°
tivity is reduced when the new burrow is
clockwise (rotation) . B, isometric myogram recordcompleted, and boring cycles then occur in
ed from partly buried '/.irphaea. Boring cycles (b)
repeated at approximately 30-sec intervals. Siphonal
groups at infrequent intervals, this patretraction and extension (r) , accompanied by
tern of activity probably more accurately
first counter-clockwise and then clockwise rotation
reflecting
normal boring activity as the
of the shell, follow each boring cycle. C, recording
burrow is gradually enlarged to accomof the pressure (upper record) in the haemocoele
of '/.irphaea during one boring cycle. Pressure was modate increments in growth. In harder
recorded through a hypodermic needle inserted
substrates, the study of boring activity is
dorsally near the pericardium. Visual observations more difficult since animals are unable to
show the closure and opening of the siphons, and
re-bore in such materials if greatly discontraction of the necessary ventral adductor muscle (va) , and the posterior adductor muscle (pa) . turbed. To overcome this difficulty we have
Pressure in the haemocoele rises as the foot is used laminated blocks exposed during the
extended, and remains raised at the end of the period of larval settlement from which
boring cycle, (after Nair and Ansell, 1968) .
the surface laminations can later be removed to reveal, with luck, part of the
the foot is extended, and remains raised shell of the borer in the base of the burat the end of the boring cycle. The max- row. This technique, which allows eximum pressure pulse reaches a value of posure of part of the borer with a miniapproximately 2.5 cm water.
mum of disturbance, has been used successThe hydrodynamic role of the fluids of fully with wood blocks in studies of the
the mantle cavity and haemocoele is less wood borers, Xylophaga dorsalis and Marimportant in Zirphaea than in burrowing tesia striata, but so far no rock borers have
forms. In Zirphaea, maximum pressures up grown to a sufficiently large size in similar
to 8 cm water were recorded during ex- laminated blocks of chalk to allow us to
trusion of pseudofeces, while during the test this technique there.
boring cycle and the movements of siphon-
866
A. D. ANSELL AND N. BALAKRISHNAN NAIR
knowledge does it occur in any rock-boring
pholad.
BORING IN OTHER BIVALVE GROUPS
1
1
1
1
1
1
1
1
1
1
1—I
FIG. 7. Extracts from isometric myographic recordings of parts of extended periods of boring of
A, Zirphaea crispata in clay; B, Martesia striata in
wood; and C, Xylophaga dorsalis in wood. Each
boring cycle consists of first extension of the foot
causing a dorsal deflection (e) of the recording pen
as the shell is lifted in the burrow, followed by
pedal retraction causing rapid upward deflection (r), and the consecutive contractions of the
adductor muscles (a) which are single in Zirphaea
and Martesia and replicated in Xylophaga.
Before going on to consider briefly other
rock-boring groups, we would like to refer
to observations on one wood-boring form,
since they indicate a further stage in the
elaboration of the boring movements described for the Pholadidae. In the boring
cycle of Xylophaga dorsalis, contraction of
the pedal retractor muscles drawing the
shell down into the burrow is followed by
a series of alternate contractions of the
adductors (Fig. 7), as many as 24 pairs of
contractions having been recorded on
several occasions. From accounts in the literature, it seems likely that this multiplication of the rocking movements associated
with abrasion of the burrow walls also occurs in members of the Teredinidae, but it
does not take place in the wood-boring
pholad, Martesia; neither to our present
We have considered in detail the boring
mechanism of the relatively unspecialized
form, Petricola pholadiformis, and of the
highly adapted Pholadidae, and seen that
in both cases the movements involved in
reforming and enlarging the burrow in
hard substrates including those of a calcareous nature are closely allied to, and
presumably developments of, the normal
pattern of locomotory activity seen in burrowing or epifaunal species. We should
now consider briefly the remaining groups
of borers and for each consider how far
boring might be a development along similar lines of the normal bivalve locomotory
movements or how far other types of behavior are involved.
A somewhat similar situation to that we
have described for Petricola occurs in
members of the Saxicavacea, such as Hiatella, (Fig. 1G), which bore into muddy
limestones, mudstones, sandstone, calcite,
and chalk. Hunter (1949) concluded that
the burrowing mechanism of Hiatella
evolved from the protective reactions of
non-boring animals where the partially
withdrawn siphons press against the walls
of the burrow to provide a fixed point
about which the shell could rotate in boring. While it is no doubt the case that by
thus withdrawing the siphons and sealing
the burrow, pressures could be exerted
against the walls of the burrow in the way
suggested by Hunter, the main forces involved in boring in Hiatella, as in Petricola, are produced by contractions of the
pedal retractor muscles and especially of
the large and powerful posterior pedal retractor. The movements involved are those
of the digging cycle, repeated at regular
intervals as in Petricola, and, as in that
species, involving also the secondary cycle
of siphonal retractions and extensions associated with each cycle. Excavation of the
burrow is not dependent on anchorage by
the retracted siphon since the foot can act
BIVALVE MECHANICAL BORERS
as a fulcrum and anchor for movements
brought about by the pedal musculature.
In Hiatella, however, the ligament, while
still powerful, allows some rocking movements to take place about a dorso-ventral
axis and such movements undoubtedly assist in the excavation of the burrow. Hiatella also differs from Petricola in producing a burrow of round cross section, indicating that rotation occurs during boring.
In both Hiatella and Petricola the material abraded is mostly passed to the mouth
of the burrow, mixed in mucus, laterally
around the sides of the shell, and this passage of material is aided by the ejection of
water from the mantle cavity into the base
of the burrow which occurs during each
boring cycle. Some material is also taken
into the mantle cavity from where it is
expelled through the inhalant siphon as
pseudofeces.
Among the Mytilidae, although most
species which bore, such as Lithophaga, do
so by chemical means, there are some species in which the boring is produced by
mechanical abrasion. An example is the
North American Botula falcata (Fig. 1C)
whose habits were described by Yonge
(1955). In this species, firm attachment to
the burrow is made by means of byssal
threads which are arranged in a large anterior and small posterior group. The rock is
abraded by the dorsal surface of the shell
valves which are deeply eroded and the
force responsible arises from the contraction of the byssal and pedal retractor muscles. The shell is held against the wall of
the burrow during this action by the opening thrust of the long and powerful ligament. There is no rotation within the burrow.
Finally we must consider boring in
other groups in which this habit has followed an initial epifaunal habit: the Gastrochaenacea and the Tridacnidae (Cardiacea) and we may do so briefly since we
have not yet had the opportunity to examine examples of these groups, most species
of which bore into the calcareous coral
rocks of tropical seas.
Rocellaria (Fig. IF) shows a superficial
867
resemblance to members of the Pholadidae, but the form of the burrow and the
detailed morphology of the animal (Otter,
1937; Purchon, 1954) show that the boring mechanism must be quite different.
The ligament is long and powerful, so that
rocking on a dorso-ventral axis is not possible. The foot is divided into anterior and
posterior regions, the former containing a
functional byssus gland opening into a
wide byssal groove around which the sides
of the foot are expanded to form a sucker.
Both anterior and posterior pedal (or byssal) retractor muscles are present, the anterior being much larger and attached to
small internal shell ridges. The anterior
adductor muscle is much reduced. Otter
(1937) considered that boring is accomplished by a powerful rocking action about
the suctorial foot in an antero-posterior
plane, while Purchon (1954) suggests,
from consideration of the muscular anatomy, that boring is brought about by the
interaction of the posterior adductor and
the anterior byssus retractor muscles. The
oval shape of the burrow, which resembles
that of Petricola pholadiformis in being
larger than the shell especially dorsally
and ventrally, suggests that the major boring movements arise as in that species from
the contractions of the retractor muscles,
contraction of the anterior pair providing
the main abrasive effect of drawing the
anterior margins of the shell down towards
the attached foot. Although this action is
thus similar to that of Petricola or Hiatella
the direction of the main abrasive force is
opposite, since it is the anterior retractor
muscles which are responsible rather than
the posterior as in these genera. These remarks, however, can be no more than
speculation until recordings of the action
of these bivalves become available.
The final species to which we shall refer
is Tridacna crocea (Fig. IE) which bores
into coral boulders and whose habits were
described by Yonge (1936). Owing to vertical longitudinal rotation of the mantle
shell in relation to the visceropedal mass,
the hinge comes to lie alongside the byssal
gape on the topographically underside of
868
A. D. ANSELL AND N. BALAKRISHNAN NAIR
the body. The posterior byssal retractor
muscles are greatly developed and their
alternate contractions cause the shell to
rock in the longitudinal axis on the fulcrum of the byssus.
The synopsis of this paper discusses and
summarizes the major points brought out
above.
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