‘Flapping valves’ in brachiopods
RICHARD COWEN
E m
Cowm, R. 197501 15: ‘Flapping valves’ in brachiopods. Lethnia, Vol. 8, pp. 23-29. Oslo.
ISSN 0024-1 164.
M. J. S. Rudwick and others postulate ‘rhythmic-flow’ feeding for the Permian richthofeniacean bi-achiopods, whereas R. E. Grant claims that they fed by normal ciliary action.
Suspension-feeding has two components, current generation and food capture; normal
brachiopod lophophores d o both, but this is neither universal nor compulsory among animals. Opening and closing the richthofeniid shell generated a ‘tidal-flow’ current precisely
analogous to respiratory currents in mammals; this is neither inefficient nor ‘self-defeating‘,
as Grant claims. Grant’s analysis fails because he chose the wrong mechanical analogy
(a pump). Morphological features of richthofeniids are better explained on a tidal-flow
hypothesis than on a ciliary-flow model, and all the data adduced by Grant in rejecting the
former is compatible with it o r favorable to it. It explains morphological features that are
bizarre mysteries o n the ciliaiy-current model, and is therefore superior even though it
implies that these Permian brachiopods were radically innovative.
Richard Cowm. Departnietit of Geology, Uiiiversity of Califortiia. Davis, Culifornia 95616,
U.S.A., 26th October, 1973.
Rudwick (1961) suggested an unusual feeding
mechanism for species of Permian richthofeniaceans. The thin opercular dorsal valve was
inferred to have moved rapidly, creating strong
eddies that would have swirled in and out of
the conical ventral valve. Rudwick suggested
that this eddying could have provided the basis
for a functional alternative to the normal
ciliary feeding mechanism of other brachiopods, and he demonstrated that many of the
‘anomalous’ morphological features of richthofeniaceans could be interpreted as reasonable
concomitants of the inferred feeding mechanism.
Rudwick & Cowen (1968) extended the concept to other richthofeniaceans, and suggested
that lyttoniaceans operated a different but
analogous feeding mechanism. Rudwick (1971)
analyzed the morphology of the earliest lyttoniacean, Poikilosakos, and showed explicitly
that a conventional reconstruction of its feeding mechanism was far less satisfactory than
the unusual alternative, which had by now
come to be called ‘rhythmic-flow’.
I argued (Cowen 1970) that some features of
both richthofeniaceans and lyttoniaceans are
compatible with the presence of symbiotic
zooxanthellae in exposed mantle tissue. I en-
visaged both these groups as harmoniously coadapted for an unusual mode of life in shallow
clear warm water: their unusual feeding mechanism was only one facet of an adaptive strategy
that is reasonable in terms of the paleogeographic and paleoclimatic habitat of these
forms, and has appropriate analogues among
living organisms.
Reaction to these various suggestions has
been mixed. Cocks (1970), for example, extended the proposal to the Plectambonitacea,
claiming that they too operated a rhythmicflow feeding mechanism. Grant (1972), on the
other hand, denied that the feeding mechanism
of richthofeniaceans and lyttoniaceans was in
any way unusual. In fact, he used the alleged
deficiencies in the functional reconstruction of
these brachiopods to cast doubt on the viability, if not the validity, of the ‘paradigmatic
method’ of functional analysis of fossils.
It is appropriate to reconsider the ‘flappingvalve’ idea in the light of these different reactions, and in the light of the twelve years of
accumulated data since the idea first appeared.
On the one hand, its proponents have expanded
it into a synthesis which appears to explain
much data that otherwise lacks a unified explanation; on the other hand, its opponents
24
LETHAIA 8 (1975)
Richard Cowen
II
claim that even the original idea is ‘dubious’,
‘erroneous’, ‘has a very low level of probability’, and is in fact a ‘self-defeating system’
(Grant 1972).
The broader methodological questions raised
by Grant have been fluently discussed by Paul
(1975) and need little further attention in this
paper. There is an ironic twist in the functional
reconstruction of fossil organisms. Where there
are no living representatives of a group, there
is often little conceptual difficulty in formulating an acceptable interpretation of the mode
of life of the organisms, based on morphological analysis and on analogy with any available
living group. For example, the graptolites are
accepted as predominantly floating suspensionfeeders, based on their structure and geometry,
and this idea survived their reassignment from
coelenterates to hemichordates. Paradoxically,
the existence of living representatives of a
group tends to limit the variety of analogues
that are considered appropriate in helping interpretation of fossil forms. The reconstructions
of dinosaur paleobiology by Ostrom, Bakker
and others have met severe criticism, mainly
because large living savanna mammals rather
than living reptiles were used as appropriate
analogues. In fact, the use of homology in
functional reconstruction is only as good as the
similarity of biological function of the structures being compared; thus while homological
7k
Fig. I . Chinese metallurgical
blowing-engine, illustrated in
the Nung Shu (Treatise on
Agriculture), Chapter 19,
p. Sb, 6a (published 1313).
Conversion of rotary power
of the water-wheel to reciprocating action by the
connecting-rod drives a onebladed plate which forces air
into a furnace. After
Needham 1965, Fig. 602.
comparisons are usually superior to others,
they are not universally so.
In the case of the Permian richthofeniacean
and lyttoniacean brachiopods, Rudwick’s interpretation relies on analogies outside the brachiopods rather than homologies within the
phylum. In fact, homological comparisons indicate that richthofeniaceans and lyttoniaceans
were structurally and anatomically aberrant,
suggesting the possibility that functional factors
might also require interpretation by resorting
to unusual methods.
Some first principles
Suspension-feeding. - Brachiopods seem always
to have been suspension-feeders. There are two
components of this feeding mechanism; fluid
containing food particles must be brought to
the organism, and the particles must be extracted from the fluid. In living brachiopods,
these two components of the system are both
accomplished by the lophophore, as the cilia
on the filaments beat to generate water currents, and act to trap and transport particles
passing through the lophophore. Bryozoans
operate ‘impingement feeding’, where cilia on
the lophophore filaments generate a water current, but food capture is effected at the mouth.
Baleen whales generate a water current by
LETHAIA 8 (1975)
swimming forward, but food particles are
trapped by the baleen plates in the mouth.
At least some, and probably most, of the
morphological features of the normal brachiopod lophophore are specified by the need to
generate and control ciliary water currents.
Thus if a brachiopod were to operate a ‘flapping-valve’ feeding mechanism, in which water
flow were generated by valve movement, we
should not automatically expect to find a normally arranged lophophore in the mantle cavity. Close analysis might in fact show that a
normal lophophore would be necessary, but
only if it was required by conditions of the
‘food-collecting’ component of the suspensionfeeding system.
Pumps. - Grant’s arguments depend heavily on
his statement that ‘by Rudwick’s methodology
the efficiency of the mechanism (of a flapping
dorsal valve) must be evaluated in terms of the
function of a pump’. Grant uses a dazzling
array of different pumps to show that the
richthofeniacean dorsal valve could not have
acted as a pump. He did not find any example
of a single-bladed oscillating pump, although
the Chinese had invented one before the 14th
century (see Fig. 1 and Needham, 1965:371).
A pump is a mechanism which raises or decreases fluid pressure in order to transmit fluid
from one place to another. The ciliary feeding
mechanism of most brachiopods certainly
works on a pumping principle, because water
flows in a unidirectional way through the
lophophore. But it is not clear that the word
and concept, ‘pump’, can be applied to the
tidal-flow mechanism postulated by Rudwick
for richthofeniacean brachiopods. In this case,
fluid is not transmitted in a unidirectional way
through the system, but flows in and out of
a blind-ended cavity with no net directional
transport. A tidal flow like this may require a
‘pump’ to drive each half of the cycle, but
assessment of the total mechanism in terms of
a pump can be very misleading.
Tidal flow. - The postulated operation of the
richthofeniacean dorsal valve is shown in Fig.
2. As the dorsal valve moved, the volume of
the mantle cavity would have undergone considerable change. The more rapidly the dorsal
valve moved, the more dramatic would have
been this volume change. Since the valve is a
flat plate, the net result would have been a
‘Flapping valves’ 25
Fig. 2. Diagram to show the ‘tidal-flow’ feeding
mechanism postulated for richthofeniacean brachiopods. Water movements (shown by arrows) based on
experiments with brachiopod models by Rudwick
(1961). The brachiopod illustrated is ‘Richthofenid
sicitla Gemmellaro from the Permian of the Sosio
valley, Sicily (figured by Rudwick & Cowen 1968, Fig.
9A, PI. 36:l).
tidal flow of water in and out of the mantle
cavity. In order to exploit this mechanism for
a suspension-feeding mode of life, several conditions are necessary:
(1) The inflowing water should contain food
particles.
(2) There should be a food-collecting device in
the mantle cavity.
(3) Outflow water should sweep the mantle
cavity free of filtered water.
The important point here is that this postulated
fluid-flow mechanism is not uncommon or inefficient as Grant seems to imply (1972:234).
Relatively rapid volume change within a closedended chamber, with resultant ‘tidal’ fluid flow
in and out, is characteristic of many organisms,
including Richard E. Grant. It is the mechanism for reptilian and mammalian respiration,
in which the internal volume of a blind-ended
chamber (the chest cavity) is fluctuated by
mechanical processes (rib movements, crocodile liver oscillation, and so on) so that fluid
(air) is driven in and out and exploited for the
particles (oxygen molecules) that it carries in
suspension (see Gans 1970).
‘Tidal’ flow of fluid is not the only possible
respiratory mechanism: thus in birds, for example, there is an approximation towards a
‘through-flow’ respiratory circulation, with only
the mouth and throat being used both for inflow and outflow (see Schmidt-Nielsen 1970).
26 Richard Coiven
As a fundamental principle, inflow and outflow
must be separated either spatially or temporally
to avoid mixing, and this principle must apply
to vertebrate respiration as well as brachiopod
suspension-feeding.
In principle, then, there is no inherent inefficiency in a mechanically generated tidalflow mechanism for suspension-feeding as contrasted with a steady-state through-flow, just as
in vertebrate respiration there is no inherent
inefficiency in mammalian tidal-flow breathing
as contrasted with avian through-flow breathing.
Concentration on a ‘pump’ as the appropriate
mechanical analogue was probably the basic
flaw in Grant’s reasoning. Since a ‘tidal-flow’
mechanism cannot be reconciled with this
kind of machinery, Grant was inevitably led to
reject tidal-flow as a hypothesis for the feeding mechanism of richthofeniaceans and lyttoniaceans. Even if Grant’s analysis was in
error, however, it does not mean that the tidalflow mechanism is in fact the right interpretation. But it does represent a viable basis for
further discussion.
The richthofeniacean feeding
method
We must contrast the relative merits of tidalflow and of ciliary-pump flow to establish their
relative probabilities for the richthofeniacean
feeding method. As Rudwick (1971) and Grant
(1972) both observe, we should be biased initially in favor of the latter.
The most telling point against the conventional interpretation of richthofeniaceans as
normal brachiopods is philosophical. If we believe that structures have functions, then structures which we recognize as unusual denote
some special adaptation that is different from,
or equivalent but different from, or additional
to, adaptations of more normal members of the
group under study. Richthofeniaceans were
demonstrably derived from more normal strophomenides, and their diagnostic and unusual
features were the result of divergent natural
selection away from whatever was the normal
adaptive strategy of normal strophomenides.
The unusual features of richthofeniaceans that
led to their delineation as a superfamily were
adaptive and demand explanation. Unusual
morphology is not automatically correlated
LETHAIA 8 (1975)
with an unusual feeding mechanism. But the
structural peculiarities of richthofeniaceans extend to parts of the shell associated with the
feeding mechanism, such as the size, disposition and secondary shell modification of the
apertural gape.
Rudwick (1961:457) argued that since the
dorsal valve is deeply recessed within the ventral cone, inhalant and exhalant water currents
generated by normal ciliary action would have
to traverse the outer mantle cavity simultaneously in opposite directions and would have
intermingled, seriously jeopardizing the efficiency of the system. In some richthofeniaceans,
particularly young ones, this problem might
not have been too important, since the dorsal
valve was not recessed far within the ventral
cone. But in a significant number of specimens
and species, the dorsal valve is deeply recessed
within the ventral, and re-mixing of inhalant
and exhalant water would have been inevitable.
This point is extremely important in view of
the modifications which are associated with
current separation in almost all other groups of
brachiopods, in most other groups of suspension-feeders, and in very many respiratory
systems involving active fluid transport. Yct the
problem is not discussed by Grant (1972).
Richthofeniaceans have an extremely rcstricted lateral gape, compared wifh a very wide
anterior gape. The lateral gape is virtually zero
during the first 20”-40” of opening, because of
the presence of the ‘arcuate zone’ of secondary
shell material. Even when the dorsal valve is
wide open, the lateral gape is very narrow
(Rudwick 1961, PI. 73:7-9). Grant makes the
same point (1972:238). This is a strong and
significant contrast with normal brachiopods,
in which the lateral gape, though automatically
narrower than the anterior gape, is usually
longer in arc, and has no secondary secretion
constricting it. The net result is that the exhalant area is smaller than the inhalant, and
water is expelled from the shell at comparatively high velocity. This occurs in other suspension-feeders, notably sponges, and is a device to inhibit re-circulation of water (see Bidder 1923). The absence of such an arrangement
in richthofeniaceans, and in fact the presence
of a contrary modification, is a minor but significant piece of evidence against the conventional interpretation of their feeding mechanism.
An explanation has been offered for all the
LETHAIA 8 (1975)
unusual features of richthofeniaceans, one
which envisages an unusual feeding mechanism
among other adaptive aspects. Acceptance of a
conventional interpretation of the feeding
mechanism in these circumstances is not parsimonious, because it leaves without explanation a myriad of puzzling morphological features. If a normal ciliary feeding mechanism is
seriously to be proposed for richthofeniaceans,
it must now be accompanied by a model which
will explain the many aberrant features of richthofeniacean morphology in terms of other life
functions. I suspect that Grant's (1972) appeal
to Occam's razor in this context is a very
dangerous gamble.
Having established that there are serious
deficiencies in the ciliary-pump interpretation
of the richthofeniacean feeding mechanism, we
must now consider objections to the tidal-flow
mechanism. Grant has presented these in some
detail. He argues (1972:236) that the cardinal
process of richthofeniaceans is small, with
minimal area for muscle insertion, and that the
valve is not strengthened o r thickened in the
cardinal area, as it is in most normal productaceans. He infers that the dorsal valve could
not have moved rapidly. Rudwick (1961:458459) had already dealt with these points. The
cardinal process is small relative to that of
most productaceans. But in relative size, it is
clear that the diductor attachments were no
smaller than those of contemporary productaceans and chonetaceans. Compare, for example, Sestropoma (Cooper & Grant 1969, P1.
2:21) or Cyclantharia (PI. 5:15) with the chonetaceans Undulella (PI. 2 5 , 6), Chonetinetes
(Pl. 3:6) and Micraphelia (PI. 5:12) and the
productacean Anemonaria (PI. 5:28). See also
Rudwick, 1961, PI. 72.
Grant's misconception probably arose because most productaceans have dorsal valves
which are much larger and thicker than those
of even the largest richthofeniaceans. When
one considers that the richthofeniacean valve
is extremely thin and light, it will be appreciated that comparable musculature with that
opening the heavier valves of productaceans
would have at least been capable of opening
the richthofeniacean quickly. Heavy thickening
is presumably necessary for longer productacean cardinal processes, but is not found to any
great extent in the small short cardinal processes
of small productaceans, chonetaceans, or richthofeniaceans.
'Flapping valves'
27
Grant (1972:236-239) has argued that the
angle of gape of the richthofeniacean was (a)
less than 90" in most cases, and (b) less than
was mechanically possible. Certainly in many
richthofeniaceans the maximum gape was less
than 90" (see for example, Rudwick & Cowen
1968, Fig. lOB), but this does no damage to
the concept of a tidal-flow mechanism, provided that the dorsal valve did in fact open as
widely as was mechanically possible. Here Rudwick's original arguments (1961:455-457) need
no modification. He cites spines with resorbed
tips, and flattened areas on the posterior wall
of the ventral valve, both features which have
no explanation except that their morphology
and distribution coordinate precisely with the
reconstructed path of a widely gaping dorsal
valve. Grant's data on the angle of gape in
preserved shells (1972, Fig. 9) show only that
there is a great deal of variabality in the death
position of the dorsal valve, which is often
open further in death than Grant claims it was
in life.
The arcuate zone takes on significance here.
Grant (1972:237-238) argues that it marks the
angle of habitual gape. The arcuate zone is a
posterior and lateral seal, designed, as Grant
points out, so that the 'sides and posterior
edges of the dorsal valve remain effectively
sealed during the process of opening'. This
adaptation receives a plausible explanation on
the ciliary-pump hypothesis, but it would equally be very advantageous in a tidal-flow feeding
mechanism. Sealing the posterior and lateral
sides of the dorsal valve during the first 20"40" of opening would effectively have channeled the inrushing eddies of water through the
large anterior gape. It is surely significant that
Grant's analysis of the diductor action of richthofeniaceans (1972:236-237) shows maximum
effectiveness while the dorsal valve traverses
the arcuate zone. In this part of their opening
action, the diductors were operating to pull the
dorsal valve against maximum water pressure,
and were generating a large inward water flow
through the anterior aperture, with the rest of
the gape still effectively sealed by the arcuate
zone. Only as the dorsal valve swung widely
open would any water at all have entered the
inner mantle cavity posteriorly and laterally,
and even then the relative amount would have
been very small. (The relative disparity of size
between anterior and lateral gape is if anything
evidence against the ciliary-flow model, as
LETHAIA 8 (1975)
28 Richard Cowen
argued above.) During closing of the shell, the
later stages of flushing of the inner mantle
cavity would have been directed entirelv
through the anterior gape, ensuring high and
directed water velocities.
Grant (1972) argues that richthofeniaceans
had a ptycholophous lophophore, by analogy
with genera such as Falafer. He also argues
that since the lophophore was attached to the
dorsal valve, flapping movements of that valve
were not likely. There are two fallacies here.
First, extrapolation of the ptycholophous lophophore found in three tiny strophalosiaceans to
productidines as a whole is rather precarious.
It is ingenious, but misleading, to make col)
lages showing a brachidium ( ~ 8 superimposed on a shell ( x 3 ) (Grant 1972, PI. 5:1820): Gould (1970) has stressed that brachidial
morphology must become more complex as
size increases. Secondly, it is quite wrong to
say that the lophophore of any brachiopod
is attached to the dorsal valve. The lophophore
is attached to the body wall, which may or may
not have a close relationship with the dorsal
valve near the lophophore attachment. Richthofeniaceans in particular must have had an
extensive area of body wall, and the lophophore could in principle have been attached
very low down in the mantle cavity. It is futile
to be dogmatic on this point, because there is
no evidence at all about the nature of the
richthofeniacean lophophore. But Grant’s arguments are quite irrelevant in terms of this
problem.
Grant argues that the energy expenditure of
the tidal-flow feeding mechanism of richthofeniaceans would have been so great as to make
them very inefficient machines. This follows an
argument by Rudwick & Cowen (1968), who
suggested that richthofeniaceans must have
lived in areas of rich food resources, so as to
sustain an energetic feeding mechanism. Rudwick & Cowen were in error here: there is
nothing inherent in the richthofeniacean tidalflow model that demands continuous operation
of the rapidly moving dorsal valve, or life
among rich food resources. In fact, then, the
richthofeniacean feeding mechanism could
easily have been discontinuous in operation,
with intermittent energetic and quiescent activity levels. The average expenditure of energy
need not have been higher than a contemporary
ciliary-flow brachiopod feeding mechanism.
Even if richthofeniaceans expended more
energy than other normal brachiopods, this
does not mean that they were at an evolutionary disadvantage, as long as their extra expenditure of energy resulted in the acquisition
of extra nutrients. Many organisms operate by
processing relatively large quantities of metabolic energy, rather than living at ‘efficient’
subsistence levels. This is a question of life
strategy rather than relative efficiency. Hamilton (1973) has made the same point with reference to warm-blooded organisms, and it is discussed in standard ecology texts (Colinvaux
3973:233, 577).
Richthofeniaceans lived in enviroments which
can be considered analogous in many respects
to modern reef environments. Modern reefs are
areas of high productivity, but most of this
productivity takes place on the reef mass in
calcareous algae and symbiotic zooxanthellae.
The productivity is channelled into secretion
of carbonate skeletal material and into the nutrition of coelenterates, and in general the levels
of both phytoplankton and zooplankton are
stable and low. I have argued (Cowen 1970)
that richthofeniaceans show evidence of having
had symbiotic zooxanthellae, which could have
increased the available resources for these
brachiopods, and I have drawn an analogy with
the living giant clam Tridacna, in which unusual morphology, feeding mechanism and
restricted habitat are co-adaptive with life in a
reef environment where suspended food materials are scarce.
In summary, the tidal-flow hypothesis is not
jeopardized at all by Grant’s criticisms, and
remains in my opinion much more viable than
the ciliary-flow model. There is no argument
about published data, only about their interpretation.
The lyttoniacean feeding
mechanism
The lyttoniacean morphology is as unusual as
the richthofeniacean, though in a different way.
Rudwick & Cowen (1968) proposed a tidalflow mechanism for this group also, envisaging
a more gentle movement of the dorsal valve,
but employing the same mechanism and logic
of interpretation. Rudwick’s objections to a
conventional ciliary-flow mechanism (1971)
are not compromised by any of Grant’s com-
LETHAIA 8 (1975)
ments, which are restricted to a critique of the
‘flapping valve pumping mechanism’.
The main point of Grant’s critique is in the
energy expenditure of a tidal-flow mechanism.
Here again, Rudwick & Cowen (1968) were
mistaken in supposing that the tidal-flow mechanism necessarily involved high energy expenditure by continuous operation. As an analogy, whales do not have to breathe continuously in order to operate an efficient respiratory
mechanism. It is conceivable, though there is
no way of testing, that the average expenditure
of energy of lyttoniaceans would have been
higher than conventional brachiopods of the
same size. I have argued that lyttoniaceans as
well as richthofeniaceans may have had symbiotic zooxanthellae in their exposed mantle
tissues (Cowen 1970).
Grant’s discussion of this point (1972:242243) contains serious errors, notably in the comparison of piston engines with turbines, the
acceptance of McCammon’s ideas on dissolved
nutrients (compare McCammon 1969; Cowen
1971; Levinton & Suchanek 1972), and simplistic ideas on the relative nutrient levels of
reefs. In lyttoniaceans as in richthofeniaceans,
there is no quarrel over data, but only over
their interpretation.
As in all scientific disputes, more data are
desperately needed. Hopefully the forthcoming
publication of the monograph on the Permian
Texas brachiopods by G. A. Cooper and R. E.
Grant will provide a data base that will allow
this particular dispute to be put to rest in a
definitive way.
Ackriowledgemerirs. - The manuscript was improved by
comments made by Dr. C. R. C. Paul. Friendly arguments with Dr. R. E. Grant were most stimulating.
Lanci Valentine drafted the figures.
‘Flapping valves’
29
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