THE BIOLOGY OF LIMPETS:
PHYSICAL FACTORS, ENERGY FLOW, AND ECOLOGICAL INTERACTIONS
By G. M. BRANCH
Zoology Department, University of Cape Town, Rondebosch, 7700, South Africa
INTRODUCTION
Limpets have attracted the attention of biologists for many years, and the past twenty years have yielded
a wealth of new information on their biology, ranging from their influence on community structure to
the expression of genes during larval development. The breadth and extent of information have made it
necessary to confine this review, and I have done so in two ways: by concentrating on three aspects of
limpet biology and by placing taxonomic limits on the groups covered. Three main themes are dealt with
in this review, in all of which recent advances have been made which are of general relevance to other
groups, and which have furthered our basic understanding of physiological and biological principles.
First, I am concerned with the adaptations of limpets to physical factors and the role that physical
factors may play in determining the zonation and distribution of limpets. The second theme deals with
energy flow, including the acquisition of food, the loss of energy in faeces, respiration and excretion, and
the retention and use of energy in growth, reproduction and secretion. Included in this section is much
background material which, although not strictly concerned with energy flow, relates to each of the
components in the energy budget. Finally the ecology of limpets is covered in terms of their interaction
with other organisms: predators, commensals, parasites, competitors, and algae; and the role limpets
may have in changing the structure of communities.
Several aspects of research on limpets are omitted. The taxonomy of limpets is not covered: there is a
recent worldwide review of the Patellidae by Powell (1973), whose nomenclature I have followed.
Advances have also been made in our understanding of the higher groupings of limpets, particularly due
to analyses of shell structure (see MacClintock, 1967). The genus Acmaea has been split into several
genera, (the most important being Collisella, Nofoacmea, and Patelloida). I have followed recent work in
using these new genera, but as some species have not yet been assigned they appear under the name
Acmaea.
The morphology of Patella vulgata is explored by Davis & Fleure (1903) and that of Lottia by Fisher
(1904); limpet morphology in general is admirably reviewed by Fretter & Graham (1962) and that of
pulmonates (including Siplionaria) by Fretter & Peake (1975). This has made it unnecessary to deal with
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
morphology except for recent findings. I have also bypassed a lot of biochemical research which does
not relate to the above themes, but much of this can be found in Florkin & Scheer (1972). Finally, I do
not deal with the use of limpets in monitoring oil pollution and the effects of emulsifiers, ably covered
in a series of papers by G. Crapp (in Cowell. 1971).
The second constraint placed on this review is a taxonomic one. I have concentrated on the Patellacea
(Patellidae, Acmaeidae, and Lepetidae) but because the Siphonariidae are so equivalent in behaviour and
ecology, they too are covered. The remaining ‘limpet-like’ families, such as the Fissurellidae,
Calyptraeidae, Hipponicidae, and Trimusculidae, are largely omitted. I have had, however, no
compunction about discussing these groups where they clearly fill a gap in our knowledge of the ‘true’
limpets. In the same spirit I have not hesitated to bring in examples of freshwater pulmonate limpets.
PHYSICAL FACTORS
Desiccation
Many limpets occur intertidally and are subject to wetting and drying each tidal cycle. Several physical
factors may potentially be stressful under these conditions, including desiccation, temperature (both heat
and cold), and salinity. These factors may be linked and can augment one another so that it is often not
possible to disentangle their separate effects under field conditions. Desiccation is usually considered the
most important of the three and has been singled out for extensive work.
The consequences of desiccation
The height to which particular species extend up the shore is often linked with desiccation stress.
Limpets may extend higher on the shore where wave action is strong (Evans, 1947; Southward & Orton,
1954; Ebling, Sloane, Kitching & Davies, 1962), where the aspect of the rocks reduces exposure to the
sun, and in areas where low tide does not occur at midday (Orton, 1929; Das & Seshappa, 1948).
Short-term movements may also be related to desiccation stress. Many authors have recorded an upward
movemeat on the shore during storms which wet the shore for longer than normal (Abe, 1931; Frank,
1965a; Millard, 1968; Haven, 1971; Choat 1977), while conversely during hot dry conditions downward
movement may occur, even involving abandoning horne scars to retreat to shaded and damp crevices
(Branch, 1975c). O’Gower & Meyer (1971) found that Cellana tramoserica occurred uniformly over the
rock face in winter but accumulated at the ‘intersection’ between dry rock and pool during summer.
Underwood (l976a), using multiple regression and analysis of covariance, failed, however, to detect any
seasonal change in preference in this species.
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
More striking are long-term movements up or down the shore. Abe (1931) recorded Acmaea dorsuosa
moving progressively up the shore during winter and similar movement has been reported for Patella
vulgata (Hatton, 1938; Lewis, 1954) and Collisella digitalis (Frank, 1965a), followed by a less obvious
downward movement in summer. The pattern of movement in C. digitalis has been analysed by Breen
(1972) who shows that movement of individual animals is very variable, but that there is a net upward
movement of 56% of the population in winter (compared with 3% moving downward) while in summer
26% moved downward and 2%
upward (Fig. 1). As settlement (or
survival after settlement) was highest
at lower levels on the shore, the more
marked upward movements of the
population led to a size gradient on
the shore, largest animals being
highest. Similar size gradients are
established in Patella granularis by the
same process (Branch, 1975c).
Not all limpets migrate, however, in response to seasonal changes. C. scabra (Sutherland, 1970) and
Notoacmea petterdi (Creese, 1980c) have very rigid homing habits and remain faithful to a home scar for
most of their lives. Incidentally, N. petterdi also has a strong size gradient, larger animals being uppermost
on the shore, but as discussed below, this is related to intraspecific competition and not migration, so
that size gradients should not be interpreted as necessarily being due to migration. Seapy & Hoppe
(1973) have recorded seasonal migrations in Collisella strigatella, but in this case there is a dramatic mean
upward movement of 17.2 cm in summer. This is not in contradiction to the hypothesis that migration
relates to desiccation stress, for the midday and early afternoon insolation probably provides the greatest
stress, and as midday low tides only occur in winter at the site examined by Seapy & Hoppe, summer
conditions may actually be less stressful.
The tolerance of limpets to desiccation stress has been related to zonation patterns on numerous
occasions, revealing that high-shore species tend to have a great tolerance (Allanson, 1958; Davies,
1969a; Bannister, 1970; Wolcott, 1973; Branch, 1975a; Hoffman, l976; Dixon, 1978). Even in the subantarctic where desiccation stress is presumably low, this trend is quite clear (Simpson, 1976). Fewer
intraspecific comparisons have been made, but all reveal the same pattern, with the high-shore
individuals being more tolerant than low-shore animals (Davies, 1969a; Balaparameswara Rao &
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
Ganapati, 1972; Wallace, 1972; Smith, 1975). As an example, Davies’ (1969a) data for two British Patella
spp. are shown in Figure 2B. Unfortunately in several cases there were size differences in the animals
tested, or the sizes of animals were
not recorded. As size influences rate
of water loss and also tolerance, we
are
left
uncertain
whether
intraspecific differences in tolerance
are a function of zonation or of
body size. Branch (1975a) has
compared the rates of water loss
and tolerance of a series of Patella
spp. and shown that size has a
strong influence on the tolerance of P. granularis, a species that migrates up the shore, so that larger
animals occur higher on the shore and have a higher tolerance to desiccation in addition to losing water
at a proportionally slower rate. On the other hand, P. cochlear remains close to the site of settling
throughout its life and its tolerance changes little (Fig. 3). In the case of Cellana radiata, smaller animals
are found higher on the shore (Balaparameswara Rao & Ganapati, 1971a), yet this species increases in
tolerance upshore: so at least in this case increased tolerance of high-shore animals is not simply related
to increased size.
Intraspecific gradients in size in an upshore direction have
been recorded for several limpets, and are summarized in
Table 1. Vermeij (1972) has reviewed the trends in shore-level
size gradients and concludes that there are basically two
patterns: those species which increase in size upshore and
those that do the reverse - decrease in size. Vermeij points out
that the first pattern is typical of high-shore species, while the
second pattern is confined to low- and mid-shore species. He
suggests the reason for this dichotomy is that different causes
of mortality are important in the low and the high shore.
Desiccation increases towards the top of the shore so that the
more vulnerable smaller individuals should occur below the
more robust larger animals. There are firm grounds for
suggesting this. In the low shore the reverse size gradient is
more difficult to explain. Vermeij ascribes it to increasing
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
predation in the low shore, arguing that pre-reproductive animals should thus occur above the adult
population where predation is reduced. Reproductive animals may then have to move downward into
the zone of high predation to gain enough food to successfully reproduce. This argument, however,
ignores the fact that adults in high-shore species tend to move upwards and not downwards. If it were
necessary for mid-shore animals to move downward to gain enough food, surely it would be even more
important for the higher-shore individuals, living in a zone that supports even less food, to move
downwards as well? A more serious point that is overlooked in the discussion of size gradients is that
they may not be related to migration or differential mortality. They may simply be due to densitydependent growth rates resulting in a greater size in the sparser upper sectors of the population, as
Creese (1980c) has shown for Notoacmea petterdi.
The most convincing evidence that
desiccation is of great importance to
intertidal limpets is the many records of
periodic mass mortalities that follow
days of calm or exceptionally hot
weather when limpets are subectcd to
unusually
stressful
desiccating
conditions (Orton. 1933; Borland. 1950;
Hodgkin,
1959;
Frank,
l965a;
Sutherland,
1970;
Wolcott,
1973;
Creese, 1980c). Curiously, although such deaths have been recorded even in subantarctic limpets
(Simpson, 1976), they have not been documented in the tropics. Probably this is a combination of
relatively little research work in the tropics, coupled with the sparsity of limpets there. In all recorded
cases mortalities have affected only high-shore individuals and species: a point we return to below in
considering the role of desiccation as a limiting factor.
Physiological effects of desiccation
Wolcott (1973) has suggested that deaths caused by desiccation are actually due to osmotic stress. Loss
of water concentrates the tissue ions. Immersion in a hyperosmotic solution can also kill the animal,
having the same effect as desiccation in concentrating the ions, but without removing as much water.
The reason for this is that limpets have limited ability to regulate their body volumes and consequently
gain ions in a hyperosmotic solution without losing as much water as they would if desiccated to the
same level of ionic concentration. If water loss is not the critical common factor causing death, we must
conclude that ionic concentration is.
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
Chaisermartin (1971) has produced interesting data which show that even at sublethal levels desiccation
may have effects that are tantamount to killing the animal. After transplanting Patella depressa up the
shore, Chaisermartin found that ionic imbalance, particularly hypermagnesia, reduced muscle action and
adhesion, to the extent that the limpets were washed away. This is an important result, largely ignored in
the literature, and in need of confirmation. If correct, it has relevance for the concept of desiccation as a
limiting factor, for it may mean that even at sublethal levels desiccation can restrict the upper limits of a
species. The influence of desiccation on heart rates has also been studied. Kristensen (1969) compared
this effect in P. coerulea and Diodora nubecula. Despite having a lower rate of desiccation, D. nubecula died
after only three hours of desiccation at 22% relative humidity at 32oC, because its heart rate decreased
and eventually ceased, while that of Patella coerulea remained constant.
Morphological adaptations
If body proportions are held constant, then an increase in size should result in a proportional decrease in
surface area relative to volume. If water loss by evaporation depends on the surface area while water
content of a body depends on its volume, then larger bodies should desiccate more slowly (in relation to
their total water content) as shown in Figure 2A. While there is no hint that higher-shore species are
larger than their low-shore counterparts, the numerous cases of intraspecific increases in size as one
moves upshore (Table 1) are probably partly related to an increased tolerance of desiccation.
Several authors have considered the ‘extravisceral’ space (i.e. that between the body and the shell) to be
adaptive in terms of resistance to desiccation. Shotwell (1950a) found the volume of water stored in the
extravisceral space to be relatively greater in small animals and concluded that this extra store of water is
important in desiccating conditions. He noted that smaller specimens of Acmaea mitra, Notoacrnea scutum,
and Collisella pelta occur higher on the shore than large individuals, and that in this order they also
decrease in size interspecifically and occur at successively higher levels on the shore. C. digitalis occurs
even higher on the shore and is even smaller. The first three species are low to mid-shore animals and
thus conform to Vermeij’s generalization regarding size gradients.
Segal (1956a) has supported Shotwell, showing that although high-level C. limatula have thicker shells
(and hence smaller internal volumes) their smaller body sizes result in a larger extravisceral space,
presumed to ease the stress of desiccation. In support of this, Segal transplanted low-shore animals to
the higher shore and found that they retreated to damp shaded sites, while the high-shore individuals
remained on top of boulders. Unfortunately, no description is given in this paper of the ‘control’
animals: the movement of low-shore animals into protected sites may simply reflect disturbance or the
lack of a home scar in these transplanted animals. Seapy & Hoppe (1973) showed a similar pattern in C.
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
strigatella: high-shore animals having a greater extravisceral space relative to body weight. The same is
true of Notoacmea scuturn, which also has a greater extravisceral space, if it occurs on the landward
(presumably more desiccating) face of boulders than on the seaward face (Seapy, 1976). In
Mediterranean Patella spp. Bannister (1975), however, showed quite the reverse: high-shore individuals
being larger and having a smaller extravisceral space.
Wolcott (1973) has criticized the idea that the extravisceral space is an adaptation to desiccation. He
points out that the total amount of water an animal holds (i.e. body fluids plus extravisceral water) is
what influences its resistance to desiccation. If the body is larger and the extravisceral space
consequently smaller, there is no reason why the water-holding capacity need change. It is a pity that
earlier authors have expressed the size of the extra-visceral space relative to the wet body weight and not
calculated the total water-holding capacity relative to dry body weight. Rough calculations from Segal’s
(1956a) data show that for equal shell volumes of 1ml, high-water animals have only about 30 more
water, although their extravisceral space is much greater. Slightly larger animals (shell volume 1.6 ml)
have virtually identical water-holding capacities in high- and low-shore specimens. Shell shape, however,
can have a substantial influence on the rate of water loss. As early as 1907 Russell pointed out that P.
vulgata from high levels have taller, more domed shells, and Orton (1932) suggested this was because in
dry desiccating habitats the limpet has to clamp down more tightly, pulling in its mantle so that, if the
mantle glands deposit the shell while in this position, the shell circumference will be reduced and the
shell taller. Moore (1934) verified the relationship between dryness of the environment and height of
shells by transplanting animals from dry rocks to pools and finding the shells developed shelves and new
growth resulted in a flattening of the shell. Since then a string of authors have shown this trend for taller
shells to be linked with drier habitats in a number of species (Abe. 1932: Hamai, 1937; Ino, 1935; Voss,
1959; Ebling et al., 1962; Punt, 1968; Olivier & Penchaszadeh, 1968; Sella & Bacci, 1971; Shabica, 1971;
Balaparameswara Rao & Ganapati, 1971b; Walker, 1972: Bannister, 1975). In Collisella testudinalis,
however, no differences in shell shape exist (Wallace, 1972).
Davies (1969a) related this trend to desiccation rates. He reasoned that as surface area (from which
evaporative water loss occurs) varied with the power of – 0.33 of the volume (proportional to the body
weight), that: rate of water loss ∝ body weight
body weight
-0.33
, but to body weight
-0.44
-0.33
. In actual fact the rate is not proportional to the
in Patella aspera, a low-shore species, and also in low-shore
individuals of P. vulgata.
The reason for this is that the animals change shape as they grow, becoming taller and hence increasing
their body weights more than the surface area from which water loss occurs. Higher on the shore, P.
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
vulgata has a taller shell and water loss is proportional to body weight 0.55 (Fig. 2A). Similar interspecific
differences exist in the Mediterranean Patella spp. (Bannister, 1975; Davies, 1969b), and in Cellana radiata
(Balaparameswara Rao & Ganapati 1972). The influence of changing shell shape can be quantified
further. Shell height (h) and length (L) are related by the function h = cL∝.
Where ∝ (the constant of allometry) = 1 if the two factors change proportionally but ∝ > 1 if shell
height increases faster than length
during growth. Comparing seven
South African Patella spp., Branch
(1975a) showed that in species
where ∝ = 1, water loss was close
to the predicted body weight
-0.33
but as ∝ increased, so the
exponent increased (Table II).
Vermeij (1973) has reviewed interspecific differences in shell proportions and texture in limpets,
neritids, and littorinids, relatiwe to their zonation and geographic distribution. Amongst the limpets he
found a tendency for high-shore species to have taller shells, although no patterns in shell sculpturing
were evident, and his data were too sparse to draw any conclusions regarding the influence of latitude on
shell proportions or texture. The pattern he reveals in terms of zonation is, however, by no means
general; amongst South African Patella spp. the species with the tallest shells are low on the shore, and
one of the high-shore species, P. oculus, has an extremely flat shell (Branch, 1975a). Thus, an intraspecific
increase in relative shell height usually occurs in animals that occur higher on the shore, and achieves a
reduction in the rate of water loss, but the same pattern is not always true when different species are
compared. Obvious exceptions to the rule are species that live on plants or on other animals: these have
conspicuously tall shells, presumably because there is a limited area available for attachment, so that shell
breadth is restricted.
Wolcott (1973) has shown that the rate of water-loss in three high-shore acmaeids is nearly ten times
slower than that of two low-shore species. He calculates that this is partly due to shell shape: for
instance the lower-shore Notoacmea scutum has a shell circumference about 2500 greater than the highershore Collisella digitalis. This is not nearly sufficient, however, to explain the ten-fold difference in rates of
water loss. This is mainly due to the higher-shore C. digitalis and Notoacmea persona secreting a mucous
sheath between the shell and the substratum, which reduces water loss seven-fold. Dixon (1978) has
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
found a similar sheath in higher-shore Collisella strigatella. This is clearly of greater importance than any
changes of shell proportion can be.
Physiological adaptations to desiccation
There are striking increases in tolerance to water-loss, both intra- and interspecifically, in animals living
at higher levels on the shore (see above). The mechanisms permitting this are unknown, although they
are likely to relate to tolerance of osmotic stress, and some possible mechanisms are discussed below in
relation to salinity stress.
Davies (1969a) has raised an important issue: it may not only be the rate and tolerance of water-loss that
dictate how high a limpet can extend up the shore, but the rate at which the animal recoups its losses.
He desiccated specimens of Patella vulgata and then replaced the limpets in sea water, and by extracting
blood from these animals and determining its ionic concentration at various time intervals he could
calculate the rate of water uptake. From this he developed a theoretical relationship between the amount
of the initial water-loss and the time taken for the animal to return to its original water content after
being replaced in sea water. The relationship is interesting. For instance, it shows that after 27.8% waterloss, 3.8 h are required for recovery of this water. This raises an interesting possibility that the balance
between rates of water-loss and rates of recovery are more likely to determine zonation patterns that
either factor alone.
Webber (1969) has begun analysing the actual process of water uptake in Notoacmea scutum. When placed
on its back in sea water, the limpet takes up water, swelling in the process, until after 6 to 12 hit has
doubled its volume. As the blood ionic composition remains the same as the sea water, both ions and
water must have been taken in. Webber could detect no pores in the foot through which water uptake
could have occurred, and as the gut stains blue when the animal is placed in methylene blue sea water,
Webber concluded that sea water must be taken up directly through the gut. He suggests that this
compensates for water loss in intertidal limpets. While the process allows uptake of sea water and hence
a more rapid return to original body volume, it does little to explain how ionic balance is restored in the
blood, after the quite astonishingly high ionic concentrations built up during desiccation (see above).
Other possible mechanisms are described below in terms of salinity stress, but none of them really
explains how ionic levels are restored in the blood.
Behavioural adaptations reducing desiccation
Short and long-term movements down the shore at times of high desiccation stress have already been
discussed, and probably serve to avoid this stress. Although this seems the most likely reason for such
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
movements, no one has critically tested this hypothesis, and in some cases there may be other
explanations - such as a reduction of food at high levels leading to a downward movement of the
limpets.
Another oft recorded phenomenon is that of clustering in the high shore. Millard (1968) and Willoughby
(1973) describe the condition in Collisella digitalis which forms large clusters when the limpets are
exposed at low-tide, but disperses to feed when the tide wets the limpets. Each cluster is persistent, but
the individuals in it do not necessarily return to it each tidal cycle. The position of the cluster slowly
moves. Strong ‘contact behaviour’ exists, about 85% of the limpets being in contact with other limpets
in the cluster. Dummy clusters (shells filled with plaster of paris and fixed in a position occupied by a
cluster) elicited no response from returning limpets, nor did the limpets join a dummy cluster, so some
chemical recognition of other limpets is likely.
There is circumstantial evidence that clustering relates to desiccation stress. Only high-shore species
indulge in it: and often only high-shore populations of species such as C. digitalis, Patella granularis, and
Siphonaria denticulata that range across different zones of the shore (Frank, 1965a; Branch, 1975c; Creese.
1980c). Abe (1932) found Acmaea dorsuosa formed clusters in summer, but with the advent of winter
storms they moved up the shore and dispersed. Patella granularis forms aggregates when it occurs on bare
rock, but amongst barnacles (where desiccation is likely to be less) it is randomly distributed (Branch,
1975c).
These are all indirect hints that clustering is important in
reducing desiccation (and hence absent when there is
less threat of desiccation) but no real proof of the
function or adaptive value of clustering exists. It should
not be difficult to test experimentally whether clustering
really is effective in reducing desiccation.
The orientation of a limpet may influence its rate of
desiccation by changing the incident radiation and hence
the rate the body heats up. (Sec also below, under
temperature effects.) Several papers have been devoted
to the microhabitat differences between the coexisting
high-shore Collisella digitalis and C. scabra, including
Collins’s (1976) work on the influence of angle of
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
substratum on desiccation. C. digitalis increases in number as the angle of inclination increases, while C.
scabra occurs mainly on flat, exposed surfaces, but tends to occupy more angled rocks when it is small.
Wolcott (1973) has shown their desiccation tolerance to be very similar (Fig. 4). Using limpets placed in
desiccators, Collins revealed a decrease in the rate of desiccation of C. scabra with an increase in the
angle of inclination, possibly explaining why small C. scabra tend to occur on more sloped rocks. There
was, however, no significant difference in the rate of water-loss between the species and hence no
reason in terms of desiccation why the species segregate and occur on rocks of differing slopes. One
unfortunate aspect of Collins’s experiment is that it excluded the effects of solar radiation on desiccation
rate so that we cannot be certain that in the field there are not differences in desiccation rate between
the two species resulting from their differing orientation.
Homing behaviour
Homing to a fixed scar is well-known in limpets and often considered to reduce desiccation. Extensive
work has been done on homing, and in this section 1 review the evidence for homing, possible
mechanisms for homing, rhythms of movement, and finally the possible role of homing in reducing
desiccation. Homing behaviour is unlikely to have a single function and is mentioned again later in this
review, but it is convenient to deal with it as a unit here, although this is partially a digression from
desiccation.
Numerous authors have described the existence of homing, summarized in Table III. Clearly there are
great differences between species, and even within species the rigidity of homing behaviour, or the
proportion of the population homing can be influenced by the size of the animals, the texture and
stability of the rock, availability of food, and the amount of desiccation. In general small individuals do
not home, territorial limpets home rigidly, and homing is more precise in high-shore species and highshore individuals.
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
There are, however, low-shore and even subtidal species that have well developed scars and homing
behaviour, so desiccation cannot be the only factor promoting such behaviour: The mechanism of scar
formation is reviewed by Lindberg & Dwyer (in prep.). Previous authors have suggested chemical
dissolution of the rock; excavation by the radula; or abrasion by the shell. The last possibility can be
abandoned as the shell is too soft and, in any case, does not fit the deep inner (pedal) scar formed under
the foot of species such as C. scabra. Both Lindberg & Dwyer (in prep.) have shown that the pedal
mucous glands contain mucopolysaccharides, and the mantle edge has carbonic anhydrase, both capable
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
of chemically etching and softening calcium carbonate. They suggest that rocks are dissolved in this way
and then scraped away by the radula. Analysis of the acmaeid and patellid radula (Lowenstam, 1962) has
revealed that the radular teeth are capped with goethite, with a hardness of about 5 units on the Mohs
scale. Although calcium carbonate has a hardness of 3, most sedimentary rocks exceed 5 and would
need to be chemically softened before being removed by the radula.
The actual mechanism of homing to the scar is still much debated. Many limpets follow their outward
trails home to the sear, as in Siphonaria japonica, S. atra, and S. sipho (Abe, 1939, 1940), S. normalis and S.
alternata (Cook, 1969), S. capensis (pers. observations), and Callisella scabra (Hewatt, 1940). At least as
many may, however, vary the return route and home without using the outward path, including Patella
granularis and P. vulgata (Stephenson, in Thorpe 1962; Beckett, 1968; Cook, Bamford, Freeman &
Teideman, 1969). Furthermore, if homing limpets are removed from their sears, and replaced nearby on
the rock, they still succeed in locating their sears (e.g. Davis, 1885, 1895; Edelstam & Palmer, 1950;
Cook, et al., 1969), so that simple trail-following is not an adequate explanation of the homing process.
Pieron (1909) proposed a kinaesthetie memory for homing limpets: in other words the limpet retraces its
outward path by following a ‘memory’ of the distances, angles, and directions of movement on the
outward path. There is no evidence to support this idea, for by this process, displaced limpets would be
unable to locate their scars. Furthermore, the path that displaced limpets follow is never the reverse of
the outward passage, as required by the kinaesthetic theory (Cook, 1971).
External clues such as polarized light, the position of sun or moon, coastal landmarks and even inertial
navigation have been suggested. These were prompted by Bohn’s (1909) finding that after he shifted the
rock on which a limpet occupied a scar, the limpet moved to a new home that had the same position in
space as the original home. Several repetitions have failed, however, to yield this result: rotation of the
rock having no effect on homing ability (Hewatt, 1940; Punt, 1968; Cook, 1969, 1971; Cook el al., 1969),
so that the rock surface itself must provide the clues allowing precise homing. Gailbraith (1965), Jessee
(1968), and Cook et al., (1969) all attempted to alter the rock surface by scrubbing the face or applying
strong detergents or sodium hydroxide, to eliminate any mucous trail laid by outgoing limpets, but
although they reduced the incidence of homing they failed to prevent it. By chipping the rock around
the scar to alter the topography, they further reduced the numbers successfully homing; but again at
least some limpets succeeded in finding their scars. Gailbraith (1965) and Jessee (1968) concluded that
the limpets were not following outward trails to the scar, for they reasoned that these would surely have
been eliminated by the scrubbing or chemical treatment. Consequently, they suggested that the limpets
have an appreciation of local rock topography allowing them to recognize the direction of the scar.
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
There is, however, strong evidence that limpets do follow mucous trails. Not only do several species
follow their own outward paths on the way home, but if P. vulgata and Siphonaria alternata (Cook et al.,
1969; Cook, 1971) are transplanted well away from their scars they will follow trails of other limpets of
the same species, and may occupy empty scars. Interestingly, they will even orientate on these new scars
in the same way as the original occupant (Cook el al., 1969). As their shells do not fit the new scar, this
orientation implies a recognition of the ‘footprint’ left by the predecessor, as Funke (1968) has
suggested. Nevertheless, individual limpets seem able to
recognize their own trails as distinct from those of
conspecifics. Trails often cross one another without
confusing the limpets. As part of his extensive analysis on
homing, Funke (1965, 1968) established Patella spp. in
aquaria on an array of square glass sheets. In this way he
could remove any particular sheet and replace it with
another. For example, after limpets had made their
outward trails, he transposed two sheets that two
different limpets had traversed, so that on their return
they encountered the other limpet’s trail (Fig. 5). This was
enough to block or slow their return home, establishing
specific recognition of the limpet’s own trail.
Siphonaria alternata can even distinguish the direction a trail has been laid down. By removing the limpets
from their trail and replacing them at right angles to the trail, Cook & Cook (1975) showed between 75
and 90% followed the trail in the direction from which they had come. This implies a polarity in the
trail, but the nature of the polarity is unknown. Once the trail is retraced its polarity is lost. Not
surprisingly, S. alternata only uses fresh outward trails to retrace its path; but Patella vulgata (Cook et al.,
1969) and Siphonaria pectinata (Thomas, 1973) may use old trails - possibly following them without being
able to determine their directionality.
Cook (1969) and Edelstam & Palmer (1950) show that transplanted limpets only succeed in locating
their scars if placed in an area they have previously explored. Cook considers this is due to the limpets
following old trails back to their scars, but of course, it could be due to a topographical ‘knowledge’ of
the locality. There is thus impressive evidence of complex trail-following, including the use of old trails,
and necessitating a very persistent trail marker; of polarity in trails and an ability to detect that polarity;
and of individual specificity in trails. If trail-following, however, is the only method of locating a scar,
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
the chemical and physical removal of that trail should prevent homing; yet it does not. Thus, we are left
with no certainty that trail-following is the only method of homing, although it is clearly of great
importance.
The role of homing and scar formation as devices reducing desiccation has been widely assumed, but
with surprisingly little experimental proof of its importance. Orton (1929), Eaton (1968), and Hirano
(1979a) considered homing in Patella vulgata, Collisella limatula, and Cellana nigrolineata to be least
developed in moist habitats; and in several species such as C. exarata and Patella granularis homing is best
developed in the high-shore (Branch, 1971; Kay & Magruder, 1977). Siphonaria normalis often fails to
home in damp localities, and the survival of transplanted animals (which lack scars due to the transplant)
is high in such areas but much less in exposed sites (Cook, 1976). Notoacmea petterdi, an extreme highlevel species, has a very rigid homing behaviour (Creese, 1980c), and limpets transplanted away from
their scars suffer 92.5% mortality in comparison with 17% in controls that are lifted up and replaced on
their scars. Although desiccation is the likely cause of death in scar-less animals, no significant difference
could, however, be found in the osmotic concentration of the body tissues of surviving experimental
and control animals (Branch, unpubl.). The only direct evidence of the role of homing in reducing
desiccation is that of Woelfl, Cook & Cook (1980), who measured the chloride concentration of fluid in
the mantle cavity of Siphonaria alternata. Submerged animals had a chloride concentration of 0.619 equiv.
1-1, (in comparison with the sea water level of 0.629). After 8 h exposure, animals on the scar lost 47%
of their water, the Cl- level rising to 1.18; while experimental
animals which were prevented from homing lost 57% body
water, Cl- levels being as high as 1.40 equiv 1-1.
Activity rhythms
Most limpets feed al fixed periods during the day and in
relation to tidal cycles. Table IV summarizes the records and
shows that there are three common patterns: species that feed
while submerged (day and night); those that move while
awash during the rising and falling tides but not while exposed
or completely covered (also during day and night) (Fig. 6); and
those that feed only at night and at low tide. These patterns
conform to the concept that feeding rhythms are geared to
reduce desiccation. The fourth pattern, however, involves
movement only during submergence, and only at night. If
desiccation dictates rhythms, why should there be no
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
movement during the day-time period of submergence? The final pattern, movement during lowtide,
during day and night, is an unusual one, but occurs in populations of S. capensis that are confined to
high-shore intertidal pools where there is no threat of desiccation.
Another feature is that different patterns are
recorded in the same species under different
conditions or in different areas. For example, in
Patella vulgata, four patterns have been recorded.
These do not seem to be artifacts of recording but
probably reflect differences in the habitats. The
rhythms are persistent and evidently endogenous, as
shown by Punt (1968) who fixed rocks (with P.
vulgata attached to their scars) under a floating
pontoon. Even under conditions of continual
submergence the limpets continued their rhythm of
movement at the time they would have experienced
high-tide, and returned to their scars prior to the
anticipated low-tide.
For those several species that feed while awash, the duration of the wash at any given point on the shore
will be greatest during neap tide when the tidal excursion is less. Cook & Cook (1978) found that
Siphonaria normalis moved further and for longer periods during neap tides than spring tides (Fig. 7). This
pattern broke down, however, in low-shore, slowly draining sites where there was no difference between
spring and neap tide excursions. At high or fast-draining sites, animals were more active on the flooding
tide than on the ebb, presumably because there was no danger of being stranded and left exposed to
desiccating conditions during the rising swash period. S. alternata ‘anticipated’ the following tide,
returning to its scar before being exposed. This ‘anticipation’ was most obvious in fast-draining sites again a possible adaptation to reduce desiccation. All the evidence linking patterns of movement to
desiccation is circumstantial and, as discussed below, there are other reasons for these rhythms.
Fig 7 – The distance and duration of
movements
of
Siphonaria
normalis
decrease with tidal amplitude (after Cook
& Cook, 1978).
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
Movement is also strongly directional. Nearly always movement is up the shore during the flooding tide
and then down-shore with the ebb, as in Cellana radians, C. ornata (Beckett, 1968), C. nigrolineata, C.
toreuma (Hirano, 1979a,b), Collisella pelta (Craig, 1968), and Notoacmea scutum (Rogers, 1968). Collisella
digitalis moves upward with the daily high high water, and downward with the daily low high water tide
(Miller, 1968). Finally, C. limatula moves upward with the night-time high-tide and downward with the
day-time high-tide. In all cases the direction of movement can be construed as minimizing the risk of
desiccation, but again there is no direct evidence that this is the underlying cause.
Are there critical limits set by desiccation?
Evans (1947) analysed the distribution of plants and animals at a series of British localities, and
concluded that there were certain ‘critical levels’ on the shore where there are abrupt changes in the
fauna and flora: particularly from M.L.W.S. to M.L.W.N.; from M.H.W.N. to M.H.W.S.; and just below
M.L.W.N. Similarly Shotwell (1950) set the upper limits of three acmaeids at the level of lowest higher
high tide and a fourth at lowest higher low tide and considered this as evidence for critical tide levels and
the r6le of desiccation in setting upper limits to the zonation of these species. The concept arises from
earlier work (see Underwood 1978a for a review) in which the proportion of time spent emerged or
submerged at different heights on the shore was calculated for a period of a year. This revealed abrupt
changes in the proportion at certain heights, later correlated with changes in the faunal and floral
composition. Underwood (1978a) has reappraised the concept by recalculating the emersion curve and
showing that it changes smoothly and sinusoidally with intertidal height, without any abrupt changes, at
least on British shores where the two daily high tides are almost equal in height. Furthermore, his
analysis shows that statistically there are no zones where the upper or lower limits of species coincide
more often than expected by chance. He thus refutes the concept of critical tidal levels. There are,
however, two situations where critical levels may exist. One is the height of high water neaps, above
which organisms are exposed for longer than a tidal cycle; and the other is where semi-diurnal inequality
of tides results in differences in the height of successive high tides. The zone between lower high water
and higher high water tides is thus exposed for up to 24 h and may be exposed for the full midday
period when desiccation is most stressful. Even so, there is no quantitative evidence that these cases
establish critical levels.
A different question is whether desiccation sets limits on the zonation of individual species. Correlations
between tolerance and zonation, and size gradients, may relate to desiccation, but are not proof that the
desiccation determines zonation; they may simply be adaptations to conditions. Nevertheless, mortality
due to desiccation does occur (see above) and is usually confined to high-shore animals. Wolcott (1973)
in his detailed assessment of limiting factors, concluded that desiccation was the only physical factor
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
regularly to impose limits on the zonation of limpets, and that it only affected high-shore species.
Desiccation may also limit zonation indirectly. For instance, predators such as mice and isopods eat
limpets weakened by desiccation (Frank, 1965a; Simpson (1976). Loss of muscular action following
desiccation can also result in death (Chaisermartin, 1971). Finally, the cumulative effects of successive
periods of desiccation have never been assessed; the balance of water loss and water uptake discussed by
Davies (1969a) deserves fuller consideration in relation to field conditions.
While desiccation is likely to set the upper limits of high-shore limpets, only Hoffman (1976) has
hypothesized that lower limits may also be set by a physical factor, i.e. submergence. He points out that
at their lower limits Collisella digitalis and C. scabra are only submerged once a tidal cycle, while C. strigatella
is always submerged twice a cycle. The mechanism whereby submergence imposes lower limits on
zonation is very difficult to visualize. Underwood (1979) concludes in his review that there is no
evidence that desiccation or temperature can determine the lower limits to zonation.
TEMPERATURE
The effects of high temperature are often coupled with and augment those of desiccation so that
comparable responses and adaptations can be expected. Temperature may have direct effects by killing
limpets, and important sublethal effects, such as influencing metabolic rates and feeding rates. The latter
are considered later (pp. 288-296).
Temperature tolerance and zonation
Temperature tolerance has been measured in two ways: by slowly raising the temperature (usually 1oC
every five minutes); or by placing the limpets at different temperatures and recording survival after a
given period of time. The latter is probably more useful when making comparisons with field
conditions.
High-shore limpets are usually more tolerant of high temperatures, as revealed in comparisons of
Siphonaria spp. (Allanson, 1958), Patella spp. (Bannister, 1970), acmaeids (Hardin, 1968; Wolcott, 1973;
Hoffman, 1976) and between Kerguelenella lateralis and Nacella macquariensis (Simpson, 1976), although a
correlation is not obvious for the three British Patella spp. (Evans, 1948). In some cases intraspecific
differences exist between high- and low-shore populations, as for example in Collisella scabra and C.
digitalis (Hardin, 1968) (Fig. 8A) and Cellana radiata (Balaparameswara Rao & Ganapati, 1972), but not
between intertidal and subtidal Nacella macquariensis (Simpson, 1976).
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
Tolerance to low temperatures is less often considered in relation to zonation although high-shore
subantarctic limpets have a greater tolerance than low-shore species (Simpson, 1976).
Body temperatures and field conditions
Comparison of limpet body temperatures with environmental conditions reveal that the body is always
hotter than the surrounding air and often hotter than the rock substratum.(Fig. 8B), implying that solar
radiation is the major input of
heat (Lewis, 1963; Hardin, 1968;
Davies, 1970; Vermeij, 1971;
Wolcott, 1973; Simpson, 1976).
Body
temperatures
are,
however, lower than those of
inanimate bodies and much less
than black bodies (Southward,
1958). Lewis (1963) found this
to be true in Fissurella barbadensis
and suggested that evaporative
cooling is important keeping limpet body temperatures down. As external temperatures rose, F.
barbadensis lifted its shell, presumably to increase evaporative cooling. Wolcott (1973), however, in
comparing tolerances of five acmaeid species, only recorded this phenomenon in near-saturated air and
considered it of minor importance in keeping temperatures down.
Body temperature is strongly influenced by ambient conditions and equilibrates with water temperature
soon after the limpet is submerged. Consequently low-shore limpets that are exposed for shorter periods
may have mean body temperatures up to 14oC less than high-shore individuals (Davies, 1970). Patella
vulgata in shaded localities are up to 12oC cooler than those in exposed sunny sites; those on basalt can
be 4oC hotter than those on sandstone; and animals oriented obliquely to the sun’s rays are on average
4oC cooler than those perpendicular to the sun. Body size also affects body temperatures, P. vulgata of
20-30 mm shell length being 3oC hotter than those of 50-60 mm (Davies, 1970). The time of the day the
limpets are exposed is of great importance. For example, Grainger (1968) found temperatures of P.
vulgata varied from 5 to 34oC when the limpets were exposed at midday, but only 8 to 24oC if they were
covered by water at midday (Fig. 9). Grainger is one of the few people to record limpet body
temperatures for a prolonged period and his data reveal an impressive range of temperatures that must
be experienced daily.
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
Thermal death
Wolcott (1973) came to the conclusion
that none of his five aemacids could be
limited in zonation by temperature alone,
as
the
recorded
temperatures
never
environmental
approached
the
upper lethal temperatures determined for
the lirnpets. While this may be true for
his species, there are several records of
mortalities
due
temperatures.
to
Even
high
in
or
low
subantarctic
conditions Simpson (1976) found that Nacella macquariensis died on hot days, and as this mortality
included animals in pools, desiccation cannot be blamed. Death of Kerguelenella lateralis occurred at the
same time, but as body temperatures were well below the tolerance limit of this species, desiccation is
more likely to have killed K. lateralis. Severe
winters also cause mortalities as described by
Crisp and his co-workers (1964) for the
British
winter
of
1962-1963
when
temperatures dropped 5-6oC below average.
There was total mortality of Patella vulgata in
some areas, and in areas less badly hit it was
again the high-shore individuals that suffered
most (Fig. 10C). Mortality due to unseasonal
cold spells also occurs in the Antarctic.
Nacella concinna (= Patinigera polaris) suffered
heavy mortalities in April 1965, when air
temperatures dropped below the lower lethal
limit of the limpets (Fig. 10) (Walker, 1972).
The actual causes of heat death in limpets are
still
unknown.
Metabolic
disturbance
following the denaturing of enzymes may
occur. Metabolism characteristically increases with temperature to a critical point and then declines (see
below, p. 290), but if temperatures are raised further, oxygen uptake may increase enormously as if out
of control (D. Donnelly and G. M. Branch, unpubl.). Grainger (1975), however, found that after heat
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
death of Patella vulgata various tissues still had a steady oxygen consumption, indicating that cellular
respiratory systems were still functioning. On the other hand, the Na+/K+ ratio rose due to an increase
of blood Na+, and Grainger suggests that at high lethal temperatures cell permeability increases; the
breakdown of intracellular ionic regulation may lead to neuro-muscular blockade and death.
Behavioural adaptations to thermal stress
Many of the adaptations discussed above in relation to desiccation apply to heat stress: short-term
movements, diurnal feeding movements at times when there is no thermal stress, and seasonal
movements up or down the shore. One seasonal migration that seems specifically linked with
temperature is the winter downshore movement of Nacella concinna into the subtidal zone to avoid the
freezing air temperatures which drop to -20oC (well below the tolerance of N. concinna) and the pack-ice
that covers the rocks. Walker (1972) found that there are two populations of this limpet: an intertidal
population that migrates down subtidally in winter and penetrates the intertidal zone in spring and
summer, and a permanently subtidal population.
Orientation can also reduce heat uptake, suggesting that Collisella digitalis which occurs mainly on vertical
or sloped rocks, should heat up less than the co-occurring C. scabra which occupies horizontal surfaces
(Fig. 8C). Wolcott (1973) shows that its body temperature is indeed about 4.5oC less, and
correspondingly its tolerance is about 2oC lower (see Fig. 4). Evaporative cooling is another method of
reducing body temperatures (see above), but has doubtful value as it involves increasing the rate of
desiccation.
Morphological adaptations to thermal stress
Vermeij (1971, 1973) and Johnson (1975) have discussed the factors regulating the heat budget of an
intertidal organism. Heat exchange is governed by evaporation, conduction, convection, and radiation
and as heat-gain must equal heat-loss, can be represented as:
Radiation+ Metabolic heat = Re-radiation ± convection
± conduction + evaporation
Radiation absorbed depends on the surface area exposed, its orientation to the sun and the absorptivity
and emissivity of the surface. The surface area for absorption is effectively the surface area lying in the
plane of the sun’s rays, and hence equal to the base of the limpet shell. Orientation of the shell thus
affects heat uptake as discussed above. On the other hand, the entire surface area of the conical shell is
available for re-radiation. Consequently, the taller the shell is in relation to its circumference, the greater
its heat loss relative to heat gain. This exactly parallels the adaptiveness of a tall shell in a desiccating
environment, and trends in relation to zonation have already been described (see p. 242). Absorption
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
also depends on the absorptivity of the surface, determined in part by colour, so that pale shells should
absorb less heat. The amount of re-radiation can be increased if the shell has an irregular surface and is
sculptured. This increases the surface area available for re-radiation, and also may create a turbulent flow
of air over the shell, increasing convective loss of heat to the air. Vermeij (1973) has shown that highshore neritids and littorinids are commonly strongly sculptured, but this pattern is not obvious in
limpets.
Convection depends on the temperature differential
between the organism and the air. As limpets are
usually hotter than the air, they can lose heat in this
way. Convection also depends on the convection
coefficient. The latter is a function of air flow, relative
temperatures, and the geometry of the organism and
its substratum. Johnson (1975) outlines how the
dimensionless Nusselt and Reynolds numbers relate
to
the
coefficient,
and
can
be
determined
experimentally. Measurement of the coefficient
involves a gold-plated silver cast of the organism
which is electrically heated and used as a constant
current anemometer to determine the convection
coefficient. Figure II shows the Nusselt (Nu) and
Reynolds (Re) numbers for C. scabra and C. digitalis
shells, from which it seems likely that C. scabra will have a higher convective coefficient than C. digitalis.
Part of the reason for this is the more ribbed and spinose nature of C. scabra. Metabolic heat can be
calculated from the rate of oxygen consumption. Johnson (1975) calculates that for a 5 g Patella vulgata
consuming 100 ul O2⋅g-1⋅h-1 (see Davies, 1966), about 6.58 x 10-8 cal⋅min-1 ⋅cm-2 of heat would be
generated, which would be a negligible fraction of the limpet’s total heat budget. Consequently, although
high-shore limpets often have lower metabolic rates (Segal, 1956b; Davies, 1966, 1967; White, 1968) this
is unlikely to influence the heat balance.
Evaporation has been discussed above and is unlikely to be a useful means of cooling the body as it
increases the problems of desiccation. Conduction depends on the thermal properties of organism and
substratum, on the temperature difference between the two, and on the surface area of contact. The
latter is particularly large in limpets which have a broad flat foot. Vermeij (1973) has argued that contact
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
with the substratum should be as small as possible. In limpets, however, where the body temperature is
often higher than the substratum, this may be an avenue of heat loss, not heat gain.
That different species have different heat budgets is suggested by Wolcott’s (1973) finding that even
when sampled under the same conditions body temperatures of different species differed substantially.
Collisella scabra had a body temperature of 34oC, C. digitalis 29.5oC, Notoacmea scutum 27oC, Collisella
pelta 27oC, and Notacmea persona 20oC. With the exception of N. persona (which hides under rocks during
the day) this sequence parallels their temperature tolerances (see Fig. 4) and their sequence of zonation.
Antarctic and subantarctic limpets face different problems: freezing and abrasion and crushing by packice. Hargens & Shabica (1973) found that Nacella concinna secretes a copious mucous sheath (1 to 11 mm
thick) when it is trapped under the anchor or scale ice, which increases its tolerance to low temperatures.
Without the sheath, experimental limpets begin to die at -8oC and all are dead at -l5oC; while those with
mucous sheaths die between -10 and -20oC. Secretion of the isotonic mucus lowers the intercellular fluid
content, avoiding extracellular ice propagation because the “compressed cellular matrix effect” retards
ice propagation through the limpet tissues down to -8oC. The mucus also has a cryoprotective function,
possibly by inhibiting the growing surface of ice, and providing protection between -8 and -10oC. Both
processes differ from that in intertidal north Atlantic molluscs, which avoid freezing by reducing their
intracellular water and hence face dehydration problems. Shabica (1971) also describes the increasing
thickness of N. concinna shells in shallow water and in the intertidal zone: presumably to resist crushing
by pack-ice.
Physiological adaptations to thermal stress
Tolerance of thermal stress is related to the environmental conditions normally experienced, both in
relation to zonation (see above) and to geographical distribution. The underlying mechanisms for this
are only partly understood. Evans (1948) showed that the tolerance of three British Patella spp. changed
seasonally, being about 2oC higher in summer than in winter. Conversely, Wolcott (1973) found no
evidence of seasonal changes in tolerance in five acmaeids. He explains this in terms of environmental
conditions: water temperatures are at their lowest immediately before summer so that acclimation to the
cold-water pre-summer conditions would be maladaptive as a preparation for the heat of summer.
Metabolic thermal acclimation is a well-established phenomenon, discussed below in relation to
respiration (p. 291). Comparable acclimation of heart-beat rate also occurs. Collisella limatula and C. scabra
have higher heart rates in the low-shore than in the hotter high-shore; and the winter rate in C. limatula is
greater than that in summer (when rates are measured at the same temperature). Transplants of highReference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
level animals down the shore and vice versa, resulted in a reversal of rates, suggesting acclimation took
place. This interpretation is, however, obscured by the possibility of different amounts of food in the
two zones, and the fact that growth rates are faster in winter, so that temperature acclimation cannot be
isolated as the only factor causing the change (Segal, Rao & James, 1953; Segal, 1956b). Markel (1974),
using the same species, combined field and laboratory observations in an attempt to isolate the factors
influencing heart-beat. He confirmed that the rate-temperature (R-T) curve shifted to the right in highshore animals (i.e. at a given temperature the rate is lower in high-level animals) and also showed that
the curve was rotated clockwise relative to that of low-shore individuals. In the laboratory, animals held
at different temperatures showed a similar shifting of the R-T curve to the right in warm-acclimated
animals, but no rotation. This proved that thermal acclimation could explain much of the difference
between high and low-shore limpets. Seasonal changes in heartbeat were, however, more dramatic,
increasing from about 50 beats⋅min-1 to 66 beats⋅min-1 in winter. For acclimation to achieve this
difference would require a 32oC change of temperature! Clearly the seasonal change cannot be due solely
to acclimation, and Markel found that the increase coincided clearly with the reproductive cycle.
Evidently increased synthetic activity was mainly responsible for the change in heart-rate.
Acclimation to higher temperatures (18oC) took only ten days while that to low temperatures (8oC) took
23 days. Markel suggested that at low temperatures,
the synthesis of the new enzymes necessary for
acclimation will be slow relative to that at higher
temperatures.
Markel
(1976)
followed
the
biochemical change in malate dehydrogenase
(MDH) during acclimation. The rate of all
enzymatic
reactions
increases
with
the
concentration of the substrate (malate in this case),
the rate of increase declining to an asymptote (the
maximum velocity or Vmax). The concentration resulting in half this rate, Km, is a useful indication of the
enzyme’s affinity for the substrate. The lower the Km, the greater the affinity of the enzyme for the
substrate. Markel (1976) plotted Km against temperature and found it to be lowest at about 9 0C for
animals acclimated to 8oC; and lowest at 18oC. As Figure 12 shows, this involved not only a shift in the
temperature at which affinity was greatest (Km lowest) to coincide with the acclimation temperature, but
an increase in the affinity in animals held at 8oC relative to those at 18oC (i.e. Km is lower at 8oC animals
measured at 8oC then in 18oC animals measured at 18oC). This can account for the elevation of
metabolism experienced in cold-acclimated animals. Further work on the thermal stability of the MDH
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
suggested that in warm-acclimated animals a single isozyme is present, but with cold-acclimation a
second isozyme is synthesized and acts in concert with the first.
Several workers have shown that the pentose shunt is activated in cold-adapted animals, rather than the
usual glycolytic pathway. The former results in the C1 of glucose being converted to CO2 while in the
latter the C3 and C4 of glucose are released as CO2. The ratio of C1:C3+C4 in CO2 is thus an indication of
whether the pentose or glycolytic pathways dominate. By differentially labelling glucose, Markel showed
that the ratio was 9⋅2:1 in cold-acclimated animals, but only 3⋅93:1 in warm-acclimated animals. Even the
latter is surprisingly high. The significance of an increase in the pentose shunt is that it generates an
extra pair of electrons, carried by pyridine nucleotide to the site of oxidative phosphorylation to generate
ATP. Usually the pentose shunt is thought to be activated at times of increased synthesis, but Markel
showed its increased activity continued even after four weeks of acclimation, in animals apparently fully
acclimated, and may be a permanent feature of cold-acclimation.
Wilkins (1977) has compared the genetic variability of Patella vulgata and P. aspera at 10 gene loci, testing
the “niche breadth” hypothesis that species with the widest habitat (P. vulgata in this case) should have a
greater genetic variability than those with more restricted habitats (P. aspera). Contrary to the hypothesis,
he found almost all loci were more variable in P. aspera. A possible explanation came from examining the
thermal tolerance of phosphoglucose isomerase (PGI) in the two species. The PGI of P. vulgata was
much more tolerant of high temperatures than that of P. aspera. Wilkins suggests that there has been
selection in P. vulgata for the single allele that is thermally tolerant and functional in the high-shore
habitat occupied by P. vulgata.
Gresham (1976) could find no genetic differences at 23 enzyme loci of Collisella digitalis from three
different zones. As C. digitalis is also a high-shore species and migrates up the shore as it ages (Breen,
1972), perhaps its alleles have also been selected by thermal tolerance and a limited repertoire of alleles
remains.
Is temperature a limiting factor in zonation?
Few authors have provided detailed field measurements of body temperatures against which we can
assess whether temperature tolerances are ever exceeded in the field. Wolcott’s (1973) analysis of five
acmaeids provides such data and he concludes that temperature never rises high enough to limit the
zonation of limpets. Nevertheless, there are clear cases of mortality due to temperature. Death of poolinhahiting Nacella macquariensis during hot weather (Simpson, 1976); and the death of Patella vulgata, P.
depressa (Crisp, 1964) and Nacella concinna (Walker, 1972) during cold spells all testify to this. Crisp’s data
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
also show that it was the high-shore animals that suffered most (Fig. 10C), just as in the case of death by
desiccation. Furthermore, the methods used to assess thermal tolerance (including those of Wolcott) are
open to criticism for two reasons. First, they often define tolerance as survival over a short period of
time (5 mm in Evans, 1948; 15 mm in Wolcott, 1973). As tolerance decreases if animals are held at a
particular temperature, this may over-estimate tolerance. Secondly, to assess tolerance from survival rate
may not be meaningful biologically. Sublethal effects that set in well below actual death may be
tantamount to death in the field. Spontaneous movement ceases 10oC below the lethal point, and
irratibility is lost about 2-5oC below lethal temperatures (Evans, 1948; Balaparameswara Rao &
Ganapati, 1972). Subantarctic limpets become detached about 9oC lower than the temperature at which
they
actually
temperatures
die
may
(Table
also
V).
increase
High
the
vulnerability of limpets to desiccation
(Simpson, 1976). Thus, not only is there
evidence that temperature can limit limpets
by their immediate death, but sublethal
effects may be just as effective and it seems
likely that temperature can set limits on the
zonation of some species.
Temperature and zoogeography
Several authors (Bennett & Pope, 1953; Knox, 1963; Vermeij, 1973; Branch, 1976) have pointed out the
paucity of patellacean limpets in the tropics in comparison with temperate areas. Branch (1976) has
summarized some of the physical differences between tropical and temperate shores. Vermeij (1973) has
described the body form of limpets in relation to heat uptake. The flat cap-shaped shell exposes a large
surface area for heat absorption relative to that available for heat emission; limpets cannot withdraw the
foot, and have a particularly large foot, so that heat absorption from the substratum may be
unavoidable; the shell shape allows little storage of water (relative to coiled neritid shells, for example).
Vermeij concludes that the geometry of the limpet shape is poorly adapted to desiccation and heat stress
and suggests that this is why they are replaced by forms such as the neritids in the tropics. This is an
interesting hypothesis, in need of testing, but there are other possible reasons why limpets are not
common in the tropics: for example, herbivorous fish tend to graze the rocks clean of algal growth in
the tropics and may out-compete limpets; and pressure from predators is also probably higher. Any
explanation based on physical factors must also explain why Siphonaria species are abundant in the
tropics.
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
Nevertheless, particular species do seem to be limited in their geographical distribution by temperature.
Vader (1972a, 1975) has proposed that extension of the range of Patella vulgata in Norway (documented
in certain areas for the period 1933-1973) relates to the slow general warming of the surface waters of
the eastern North Atlantic. Changes in the species composition in archaeological sites also suggest shifts
from a cold- to a warm-water limpet fauna after the last glacial period. For example, Patella granafina (a
cold temperate species) dominates the lower layers of sites on the at present warm-water south coast of
South Africa; while the warm-temperate P. longicosta is common only in the more recent layers (Voight,
1975).
An interesting feature of temperature tolerances is that upper lethal temperatures do not vary much with
latitude. If one excludes Nacella concinna, species ranging from the tropics to the Subantarctic all have a
lethal temperature of between 4l.5 - 43.7oC; yet with sublethal effects such as detachment or loss of
movement a much clearer link with latitude is established (see Table V). This may imply that these latter
effects are of greater ecological importance, and tolerance to temperatures inducing these sublethal
effects more strongly selected for.
One of the few long-term studies of recruitment and population structure is that of Bowman & Lewis
(1977) on Patella vulgata. By following reproduction cycles and recruitment over eight years they could
relate the time of spawning and the success of recruitment to various environmental factors. No
correlation existed between intensity or timing of spawning and recruitment success. Desiccation stress
immediately after settling seemed to set the pattern of recruitment (i.e. more intense in the lower shore
and in damp areas) but not its success. Success was more clearly related to the number of frost-free days
after spawning (i.e. after settling of young limpets) (Fig. 13). Consequently, the earlier spawning takes
place, the greater the chance of a frost-free period long enough for the recruits to establish themselves.
The following autumn (a year later), young limpets emerge from their damp primary “wet-settlement”
sites on to “dry-settlement sites” (see Lewis & Bowman, 1975) and desiccation stress at that stage
determines how many of last year’s
recruits
contribute
to
the
adult
population. Thus adult population site
is not necessarily related to the success
of the previous year’s recruitment.
Bowman & Lewis (1977) speculate that
the northern limits of P. vulgata may be
set by recruitment failure due to an
increased incidence of frosts (although
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
spawning in Norway seems to occur earlier in the year, possibly as an adaptation to offset this problem).
They also speculate that the southern limits are set by increasing desiccation, and possibly competition
for sheltered sites with the better adapted southern species.
SALINITY
Tolerance to salinity stress in relation to zonation
The effects of a hypersaline solution on a limpet are comparable with those of desiccation, so it is not
surprising that some authors have found correlations between tolerance to reduced and increased
salinities, and zonation (Allanson, 1958; Simpson, 1976; Tarr, 1976). On the other hand, Wolcott (1973)
could find no relationship at all, and Bannister (1970) found the high shore Patella lusitanica less tolerant
to extremes of salinity than the low shore P. coerulea. As the former occupies bare exposed rocks it
probably never experiences salinity extremes while P. coerulea, being a pool inhabitant may do so. Cellana
radiata, a tropical species, tolerates between 20 and 40% for periods in excess of 24 h, being surprisingly
intolerant of high salinities in view of its tolerance of desiccation (Balaparameswara Rao & Ganapat;
1972).
Arnold (1957) tested the intraspecific variation in the responses of Patella vulgata to different salinities.
When sea water is dripped on the shell P. vulgata elevates its shell, but if fresh water or hypersaline NaCl
is used, it clamps firmly down. The frequency and intensity of shell elevation declines with salinity and is
thus a useful comparative measure. High-shore animals are less sensitive to a decline in salinity than lowshore specimens (Fig. 14). In part this is a function of
age. All young animals seem tolerant of reduced
salinities, but as they age the high-shore specimens retain
this tolerance while low-shore limpets lose this potential
(Arnold, 1972). Arnold (1959) shows the response to
different salinities is not due to osmotic concentrations
but to particular ions: isotonic NcCl and CaCl2 in
combination yield the most natural responses and Clmodulated by Ca2+ seem the most important ions.
Is salinity ever a limiting factor?
Simpson (1976) and Wolcott (1973) concluded that salinity never fluctuates widely enough to limit any
of the seven limpet species they investigated, with the exception that where freshwater seepage occurs
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
onto intertidal rocks, only Collisella digitalis and Notoacmea persona (the most tolerant of the five acmaeids
tested) can occupy these areas (Wolcott, 1973). Patellacean limpets are usually excluded from estuaries,
although they can extend into salinities of 20-22 0/00, (see Arnold, 1972) and even grow very rapidly
there (Fischer-Piette, 1931, 1941). Siltation may be more important than salinity in excluding limpets
from estuaries.
Osmotic response and adaptations to salinity changes
All limpets are osmoconformers, their body fluids conforming to the external salinity, as shown for
Siphonaria pectinata (McAlister & Fisher, 1968), Patella vulgata (Hoyaux, Gilles & Jeuniaux, 1976),
Collisella limatula (Segal & Dehnel, 1962), and Notoacmea scutum (Webber, 1969), although Siphonaria
zealandica has limited powers to remain hyperosmotic at very low salinitics (Bedford, 1969). Not only the
osmotic concentration conforms to the external medium, but the ionic composition also equilibrates
with the medium, with the possible exception of K+ which remains closer to, or slightly higher than, that
of sea water (Webber & Dehnel, 1968; Hoyaux et al., 1976).
The only defence limpets have against changing salinities is to clamp the shell tightly against the
substratum thus temporarily excluding the external medium and slowing the period of equilibration
(Hoyaux et al., 1976). MeAlister & Fisher (1968) analysed the effectiveness of this mechanism in S.
pectinata and found it could tolerate the range 20-40 0/00, but outside this range its survival was
drastically lowered by 43% if the limpets were prevented from clamping onto the substratum. Over the
range of tolerance the limpets did not clamp down, but above and below this range animals that
clamped down achieved some measure of osmoregulation in comparison with experimental animals that
were not allowed to clamp down (Fig. 15).
McAlister & Fisher suggest that not only is
increased muscular contraction involved in
sealing off the animal, but decreased ciliary
activity, so that pallial and mantle currents
are reduced. As described above, Arnold
(1957,
1972)
has
shown
intraspecific
variation in the clamping response.
Segal & Dehnel (1962) have proposed that the extravisceral water (EVW) has an osmotic function
parallel to that of its presumed function in reducing desiccation. If the EVW is removed from Collisella
limatula and the limpets are left to desiccate in the field, the osmotic pressure of the blood and the EVW
(which the animal has presumably renewed from tissue fluids) rises rapidly in comparison with that of
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
control animals (Fig. 16). In most cases the EVW
has an osmotic concentration slightly above that
of the blood and Segal & Dehnel suggest that it
acts as a buffer between the blood and the
external medium. The concept has been criticized
by Wolcott (1973) (see above), for although the
EVW clearly increases the animal’s capacity to
tolerate desiccation and osmotic stress, it only
does so by increasing the total reservoir of water
available to the animal, and the closeness of the
osmotic concentration in the EVW and the blood
(see Fig. 16) show that the EVW is not an
intermediary or buffer, but in equilibrium with the
blood.
Tarr (1976) has shown that C. digitalis is more tolerant of osmotic stress than Notoacmea scutum. Both are
osmoconformers, but after equivalent osmotic stress the wet body weight and tissue hydration of the
former changed less than in the latter. Tarr considers that this is due to their relative abilities to regulate
body volume and suggests this ability is an important aspect of withstanding osmotic stress.
If limpets (and marine molluscs in general) are osmoconformers, how do they maintain intracellular
ionic constancy? Hoyaux et al. (1976) and Schoffeniels & Gilles (1972) point out that intracellularly there
is a large pool of the ‘non-cssential’ amino acids and other amino compounds such as taurine, homarine,
and glycine betaine (Ackcrmann & Janka, 1954). Florkin & Bricteux-Gregoire (1972) list the levels of
these compounds in Patella vulgata and single out proline and arginine as the most important non-protein
amino acids. Simpson et al. (1959) describe the free amino acids in a number of gastropods, including
Siphonaria lineolata, and show that taurine is present in high concentrations in marine gastropods but not
in terrestrial or freshwater gastropods. During exposure to low salinities, levels of these intracellular
organic compounds drop, while they rise in hypersaline solutions. For instance, in P. vulgata exposure to
50% sea water reduces the taurine and arginine levels from, respectively, 106.5 and 10.03 micromoles⋅g-1
wet tissue weight to 28.8 and 30.8. It is suggested that by regulating the concentration of these amino
compounds within cells, the osmolarity is controlled and the exchange of ions and water with the blood
is minimized. Transferring P. vulgata from sea water to 50% sea water only changes its intracellular
water content from 72.5 to 80.3% (Schoffeniels & Gilles, 1972). Changes in the level of free amino acids
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
also occur in Siphonaria zealandica subsequent to changes of osmotic concentration of the medium, but
cannot be conclusively linked with cell volume regulation (Bedford, 1969).
The mechanism controlling the levels of amino compounds is little understood. Emerson (1969) has
tested the idea that free amino-acid levels arc controlled by enzymes, including glutamic dehydrogenase
(GDH). The activities of such enzymes are known to be affected by anions and cations and the binding
of reduced nicotinamide adenine dinucleotide to GDH is modified by ionic concentration. The activities
of such enzymes could thus regulate the free amino-acid pool. This should influence the rate of NH3
excretion. Testing a number of molluscs, Emerson (1969) showed that NH3 did vary inversely with free
amino acids in some species, but the two were poorly correlated in prosobranchs. In Notoacmea scutum
NH3 excretion dropped dramatically in 150% sea water relative to that in 100% sea water, but no
obvious differences existed in 50% and 100% sea water. Measurement of free amino acid showed a rise
in 150% but no significant difference between 50% and 100% sea water. Emerson concluded that
intracellular regulation of amino acids does exist in most molluscs but is poorly developed in N. scutum
which, like other prosobranchs, may have to tolerate hydration or dehydration rather than regulating
amino acids to any extent.
Nevertheless, Boddingius (1960) showed that neurosecretory cells in Patella vulgata emptied when the
limpets were placed in dilute sea water and, conversely, accumulated granules in concentrated sea water
suggesting some neurosecretory regulatory function. In the more advanced marine pulmonate, Onchidium
verruculatum, removal of the right pleural ganglion reduces the blood Cl- level while its re-implantation
restores the original level, suggesting a neurosecretory regulation of the re-absorption or elimination of
Cl- by the nephridium (Hanumante, Deshpande & Nagabhushanam, 1979). Such a regulation at the ionic
level is unlikely in patellacean limpets.
WAVE ACTION
The distribution and abundance of limpets
The presence of several limpets is related to intensity of wave action. Patella aspera increases in density
but decreases in size as wave action becomes intense; while P. vulgata dominates at intermediate
intensities (Ballantine, 1961; Thompson, l979); Cellana tramoserica similarly is most common at
intermediate levels of wave action (Meyer & O’Gower, 1963). More quantitative data show that numbers
of Helcion (= Patina) pellucidus peak at current speeds of 1.0 to 1.5 m⋅s-1 (Ebling, Kitching, Purchon &
Bassindale, 1948) and that numbers of Patella cochlear increase with wave intensity (Branch. 1975b).
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
Ballantine (1961) has proposed a biologically defined exposure scale to rank the intensity of wave action
(from 1 to 8, in order of increasing shelter) on the basis of the fauna and flora present. On a local scale
this may be useful for comparative purposes, but requires re-definition in other localities as species
change. Wave action may affect a number of factors including desiccation, abrasion, crushing, and the
danger of detachment. Increased wave action may increase the rate of settling in P. vulgata (Hatton,
1938), and Wright (1978 and pers. comm.) has shown that the incidence of feeding in Lottia gigantea
declines when wave action is violent. He ascribes this not to the danger of the limpet being torn off the
rock, but to an increase in the cost : benefit ratio. If more energy is spent on clinging to the rock than is
gained by feeding, then feeding excursions may not be profitable.
Most of the effects of wave action are anecdotal. No attempts have been made to simultaneously
quantify wave action, to test the drag of water movements over limpet shells, and to measure the power
of limpet adhesion in relation to that drag, the three variables needed to assess whether wave action is
ever a direct threat in terms of limpet detachment. The individual factors have, however, been studied
separately.
Adhesion
Several authors have measured the powers of attachment in limpets (Aubin, 1892; Menke, 1911; Abe,
1931; Pelseneer, 1935; Thomas, 1948; Miller, 1974; Branch & Marsh, 1978). The results are very
variable, not only because of differences between species but because of the relatively crude apparatus
used in some cases. With more sophisticated methods (Grenon, Elias, Moorcroft & Crisp, 1979)
measurements should improve. The force of adhesion varies from 484 g⋅cm-2 in Acmaea dorsuosa (Abe,
1931) to 6900 g⋅cm-2 in Patella argenvillei (Branch & Marsh, 1978). The total force necessary for
detachment may approach 100 kg in the latter species. In a comparison of adaptive design of the foot in
a large number of prosobranchs, Miller (1974) showed that limpets rank high in their powers of
attachment, that when they are moving their tenacity is only about a third of that of stationary animals,
and that (although not measured for limpets) normal forces (perpendicular to the attachment) need to
be about four times greater than shear forces to detach an animal. She also showed that the optimal
shape of the foot for attachment is a length : width ratio of l ⋅ 3 and a foot length slightly less than the
shell length. Limpets conform to these optima. Interestingly these relationships also allow rapid
locomotion, and although speed is not normally associated with limpets, P. oculus can move at 3⋅72
mm⋅s-1 placing it in the top 6% of 148 species tested by Miller.
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
The mechanism of attachment has been ascribed to suction, but as the force of attachment regularly
exceeds that of atmospheric pressure (1008 g⋅cm-2) this is not an adequate explanation. Adhesion is now
generally accepted as the mechanism. The force of adhesion (F) is described by the equation F = 2AS/d
(where A = surface area of contact, S = surface tension of the adhesive, and d = thickness of the
adhesive fluid.) Obviously an increase in foot surface area will increase adhesion, as Branch & Marsh
(1978) demonstrated. Miller (1974) has shown that in areas of high wave action, the foot of Collisella pelta
has a larger surface area (relative to shell length) than in sheltered areas. When foot surface area is
allowed for, however, different species still have significantly different powers of attachment. Nothing is
yet known about surface tensions of the adhesive mucus in different species, but Grenon & Walker
(1978) have histochemically revealed nine types
of mucocytes in Patella vulgata, and six in
Acmaea tessulata; of which three produce acidic
mucopolysaccharides with a high viscosity
which are probably used in adhesion; while
three other types of mucocytes are probably
involved in locomotion (Fig. 17). Lindbcrg &
Dwyer (in prep.) and Dwyer (1980) confirm
the presence of pedal mucocytes in Collisella
scabra.
Grenon & Walker (1980) describe the biochemistry of pedal mucus from Patella vulgata, and its response
to constant stress. The mucus contains proteins and carbohydrates, possibly linked by electrovalent
bands. The proteins are electrophoretically separable into eight bonds with molecular weights ranging
from 23500 to 195000 daltons, suggesting that the mucus contains aggregates of protein formed from
monomers of about 23 500 daltons. Under constant stress, mucus first reacts elastically as a solid, then
has a retarded elastic response, and finally behaves in a viscous manner.
These three phases of response may be due to an initial extension of the network of molecules, followed
by an elongation of the mucoprotein chains, and ultimately a sliding of the chains past one another. The
viscoelastic nature of the mucus means that it can behave as both a solid and a liquid: and only if the
time taken to detach a limpet lies within the phase of elastic response will the mucus act as a solid and
hence be an effective adhesive. It also seems that the tenacity of limpets cannot be explained by Stefantype adhesion, which applies only to liquids.
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
Branch & Marsh (1978) showed that the amount of
mucus produced by stationary individuals of five Patella
spp. varied inversely with tenacity (Fig. 18) in agreement
with the above equation. In support of this they found
that the number of mucocytes was higher in active
species with low powers of adhesion.
It is well known that if limpets are caught ‘unawares’ they
are comparatively easy to dislodge, so muscular tension
must also influence adhesion. Branch & Marsh (1978)
found that fast-moving species with low powers of
tenacity had a very flexible foot, which could be
correlated with a small area of muscular attachment to the
shell and the presence of larger and more haemocoelic
spaces (Fig. 18). It seems that in these six South African Patella spp. there is a trade-off between speed of
movement and power of adhesion.
Shell shape and drag
In some species shells are more streamlined in areas where water movement is great. Cook (1979)
showed that when Siphonaria alternata occurred in pools with an undirectional strong surge they had
flatter shells than in calm pools. As desiccation cannot have influenced this difference, water movement
is more likely to account for it. Cook did, however, also find the tallest shells on dry rocks. S. lessoni has
taller shells when permanently submerged on raft than in the intertidal zone, and Bastida, Cappezzini &
Torti, (1971) concluded that tall-shelled forms are associated with calm waters. Fishlyn (1976) reports
two forms of Notoacmea paleacea: one occurring on the narrow blade Phyllospadix torreyi in calm water and
having a narrow but tall shell, and the other on the broader P. scouleri in washed localities which has a
broader slit but is much flatter, presumably because of the wave action. In contrast, Ebling et al. (1962)
and Bacci & Sella (1970) find shells of Patella spp. to I taller in areas of stronger wave action or water
movement. This divergence of results is coupled with contrasting explanations. It can be argued that
flatter shells are adaptive where wave action is strong; or alternately that strong water currents demand
that the limpet clamps down tightly and consequently deposits its shell in a tall conical form
(comparable with the argument concerning desiccation stress and shell height, see above).
Berry & Rudge (1973) compared the amount of variability in shell proportion of Nacella concinna. They
failed to find the inverse correlation between variation and duration of ice cover that they had sought,
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
but they did find variation decreased in older animals on wave-beaten shores. They suggest that the wide
variation of juveniles is due to larval recruitment from a range of habitats followed by elimination of
some variations on harsher (wave beaten) shores. They could not, however, find any relationship
between wave action and relative shell height. When comparing different species, Branch & Marsh
(1978) could find no relationship between shell profile and the range of wave action each species
normally encountered.
Warburton (1976) has made a detailed analysis of adhesive forces au shell structure in relation to water
movement, in Helcion (= Patina) pellucidus As this limpet lives on kelp plants it can rely on a unidirectional
current as the kelp sways away from the current. By regulating water currents on hydraulic bench the
tolerance of H. pellucidus was measured. The time remained attached increased as flow-rate dropped, and
Warburton established 1⋅104 m ⋅ s-1 as his “critical velocity” close to the current speed which maximum
numbers are found in the field (Ebling et al., 1948). Vail (1972) showed that H. pellucidus had a marked
pattern of orientation in the field. Nearly all animals orientated with their longitudinal axis parallel to the
laminarian blade, those situated at the distal end of the blade face towards the base (hence into the
current) while those at the basal end face towards the tips of the blade (Fig. 19). Warburton (1976)
confirmed a w defined longitudinal orientation in the field, but there were seasonal changes in the
proportion facing distally and proximally. In the laboratory there was a very marked longitudinal
orientation, with more animals facing into the current when water speed exceeded 0.5 m ⋅ s-1, but at
lower species there was no preferred orientation. Patella compressa also orientates into current in the field
(Branch, unpubl.). Notoacmea paleacea, while orientating longitudinally (almost of necessity because of the
narrow blades it lives on faces away from the current (Fishlyn, 1976). Gadinalea nivea orientates very
strongly with its head away from the current, but this relates to its peculiar method of feeding, and not
to any reduction of drag on the shell (Walsh, Norton & Croxall, 1973). Other authors have reported
orientation in relation to water flow in Acmaea dorsuosa (Abe, 1931), Lottia gigantea (Abbott, 1956) and
Patella spp. (Funke, 1968); but as these limpets inhabit turbulent shores the direction of water movement
usually will be unpredictable, and the orientation of less obvious value than in limpets living on large
host plants.
Warburton (1976), by making simplifying assumptions, calculated the theoretical drag of Helcion pellucidus
shells of two different sizes, in different positions and at different water velocities. Animals facing into
the current are theoretically streamlined because the apex of the shell is closer to the front of the shell,
and these animals have the lowest drag; limpets facing longitudinally but away from the current may
have more than double the drag on their shells, and those orientated transversely, almost double again.
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
Naturally drag was greatest at higher velocities and in larger animals (Fig. 20). Vahl (1971) recorded that
the large H. pellucidus survived better in
deeper
waters
individuals
while
survival
was
for
smaller
greater
in
shallow waters (Fig. 19A). This puzzled
him for he reasoned that the attachment
power of larger animals was greater
because of their larger foot (as confirmed
by Warburton, 1976), and that large
animals had proportionally lower shells
and should, therefore, be more tolerant
of the greater wave action in shallower
waters. He, however, neglected the
boundary layer effect (decrease of water currents close to a substratum). Warburton (1976) using
theoretical values of drag showed that relative to the surface area of the aperture (a measure of foot size
and hence power of adhesion), large animals are at a disadvantage when compared with small animals
(Fig. 20), which explains the pattern of survival Vahl (1971) recorded.
Only one set of measurements has been made of actual shell drag, and involved a comparison of six
Patella spp. (Branch & Marsh, 1978). These confirm
Warburton’s (1976) theoretical calculations that
drag increases with size and with current strength,
but they also show that although drag substantially
greater in transversely oriented shells, there is little
differcence between shells facing into or away from
the current. Drag (D) is determined by the formula:
D = ½ pu2 ACD . where p is the density of the fluid
(and beyond the animal’s control); u is velocity of
the water; A equals the frontal area (cross sectional
area at right angles to the water movement); and
CD is the coeficient of drag, a dimension-less
quantity that can be determined empirically in test
chambers, depending in part on the geometry of
the body.
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
Drag depends partly on the ratio of shell length : width (the fineness ration RF), higher values yielding a
more streamlined shape. In Helcion pellucidus RF decreases with size, so smaller animals are more
streamlined (Warburt 1976). Streamlining also depends on the shell apex being fairly far forward as it is
in H. pellucidus, where the eccentricity index (ratio of shell apex front : shell apex to posterior) is 0.59. In
another kelp-dwelling species Patella compressa it is 0.55 (Branch, unpubl.) while in six shore-dwelling
species which cannot depend on unidirectional currents it varies from 0.-4 to 0.814 (Branch & Marsh,
1978).
The frontal area of shells depends on their size and relative height, and both factors correlate poorly
with wave action in six Patella spp. The coefficient of drag (CD), however, relates directly to the range of
wave action normally experienced by each species.
The shell texture influences CD a good deal. Irregular
large costae increase CD, substantially, as in P.
longicosta and to a lesser extent, P. oculus and P.
granatina (Fig. 21). An interesting point is that slight
texturing such as granules or ribs can be an
advantage over a completely smooth surface, as it
induces a turbulent boundary layer over the shell,
preventing the water from separating from the shell
and hence reducing the wake. At low water velocities
such texturing is a disadvantage but at higher
velocities it reduces CD, even below that of a smooth
cone (Fig. 21) (Branch & Marsh, 1978).
Only when the drag is related to the adhesive power of the limpet can its tolerance to water movement
be assessed. Branch & Marsh (1978) found that this polarized six Patella spp. into two groups: those in
which drag was low relative to tenacity, and which occupied extremely turbulent wave-beaten areas; and
those with higher drag relative to tenacity, which were more common on shores with moderate wave
action.
PHYSICAL STRESSES AS LIMITING FACTORS
The idea that physical factors such as desiccation limit the zonation or distribution of organisms is well
established, almost to the point of dogma. Comparatively recently it has been shown that many species
live well within their tolerance limits. The many correlations between tolerance and zonation described
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
above are not proof that physical conditions limit the species; they may simply reflect adaptations to
prevailing conditions.
Of the factors considered above, desiccation quite clearly limits some limpet species, and mortalities due
to desiccation often occur. Of course, it is difficult to separate the effects of desiccation from those of
heat stress, as the two often act together, and heat may lower resistance to desiccation. Wolcott (1973) in
his detailed appraisal of physical factors or limiting factors, concluded that heat could never limit any of
the five acmaeids he examined, for environmental temperatures never exceeded their tolerances. As
discussed above, sublethal effects of temperature such as detachment or neuromuscular failure, may,
however, be just as effective in limiting an animal. Temperature per se less often causes deaths, but there
are well-documented instances of heat death (Simpson, 1976) and cold death (Crisp, 1964; Walker,
1972). Thus we cannot dismiss temperature as of no consequence in determining the upper limits of
zonation.
Salinity, on the other hand, probably seldom restricts zonation. The only recorded exception is
Wolcott’s (1973) finding that freshwater seepage may limit some species. We lack the data to draw firm
conclusions about wave action as a factor limiting the local distribution of limpets. Few reliable readings,
and no continuous recordings, of wave force have been related to limpet tolerances. Only in the case of
Helcion pellucidus has tolerance been related to known field conditions, showing that this limpet can
indeed be limited by current speed.
In each case these physical factors cannot be properly assessed because there are so few long-term data,
either on the factors themselves or on the responses of limpets to them. In particular, we need to know
more about the physical conditions that limpets actually experience, and not to extrapolate from
meteorological records or macro-scale weather records (see Johnson, 1975). Wolcott’s (1973) research
stands out as one of the few studies with long-term data; but there is need for comparable information
elsewhere, to test Wolcott’s conclusions.
With few exceptions, mortalities due to desiccation or temperature have been limited to high-shore
species, and Wolcott (1973) found that only in high-shore species did environmental conditions ever
exceed the limpet’s tolerances. He hypothesized that this was because high-shore species might border
on an unexploited food source, so that it would pay them to extend their range to the limits of their
tolerance to capitalize on this food. The increased risk of death during unfavourable physical conditions
can thus be offset by increased reproduction, gained by using the unexploited food. On the other hand,
low-shore species will be flanked above by high-shore species which are better adapted to the harsher
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
conditions, and which will be utilizing the food there; so there is little for low-shore limpets to gain by
expanding their range upwards. Wolcott proposes that in low-shore species selection will favour
behavioural traits that keep the species well within their physiological tolerances. Consequently physical
factors are likely to limit the zonation of high-shore species, while biological factors restrict low-shore
species. We would also expect from this that it will be the high-shore species that are likely to move up
and down the shore as seasonal conditions improve or deteriorate. From the examples given above this
does seem to be the case. A parallel can be made for subtidal Antarctic species, where upward migration
occurs into the intertidal during spring, following the unexploited spring bloom of algal growth, and
where again physical factors can cause mortalities and limit zonation (Walker, 1972). Manipulative field
experiments provide some tests of Wolcott’s hypothesis and are described later in this review in relation
to interspecific competition.
Underwood (1979) makes an important distinction between mobile forms such as limpets, and sessile
species. The latter depend on larval settling to establish populations on the shore, and at least initially,
physical factors are likely to set upper limits to where these vulnerable larvae can settle. The pattern may
later be modified by competition or predation, but the adults of sessile species cannot change position
to seek more favourable conditions as the mobile limpets may do. Physical factors such as desiccation
are thus likely to be more important in setting limits for sessile species.
COMPONENTS OF ENERGY FLOW
Energy that is consumed (C) by limpets will only partly be absorbed by the gut, the remainder being lost
in the faeces (F). Of that absorbed, part is again lost during excretion (U) while the rest is used in
metabolic processes, a large fraction being lost as metabolic heat during respiration (R) while the
“useful” fraction is channelled into production in the form of growth (Pg), reproduction (Pr), and in
limpets a proportion being diverted into secretions, of which mucus may be important (Pmuc). The
familiar energy budget equation is thus: C = F+U+R+Pg+Pr+Pmuc. Clearly the more energy that can be
channelled into reproduction, the better. This is, however, partly dependent on body growth and
maintenance, so that Pg + Pmuc are prerequisites for successful reproduction. On the other hand, F, U,
and R represent energy losses. Obviously any reduction in these will increase production if C remains
constant, so that the animal should minimize these functions and maximize Pr, Pg, and Pmuc. Of course,
some of these functions are not independent, but at this stage a simple polarization is convenient.
ACQUISITION OF FOOD
Methods of feeding
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
Most of the ‘true’ limpets are herbivorous grazers, some on macrophytes, but a majority on microflora
including diatoms, algal spores, and detrital deposits. These foods are scraped from the substratum using
the radula which is operated like a rope over a pulley (Eigenbrodt, 1941) by the complicated radular
muscles described in detail by Graham (1964) for Patella.
These are the only muscles in the body to be supplied with myoglobin in Patella and Siphonaria (Read,
1968; Terwilliger & Read, 1970). In the Patellacea the buccal mass is supplied by salivary glands, and the
oesophagus passes back to a small stomach which has ciliated ridges that sort the food. Ducts from the
digestive gland enter the stomach and in the Patellacea most of the digestion takes place in this gland.
The intestine is remarkably long, coiling three to six times around the visceral mass before exiting at the
anal papilla on the right of the mantle cavity. As the intestine seems to have no digestive or absorptive
function its great length is intriguing. It has been suggested that it is necessary to compact the faecal
material to prevent the faeces from fouling the mantle cavity. This may be necessary in intertidal species
where the faeces cannot be released directly to the exterior during low-tide. Descriptions have been
given of the digestive system in Patella (Graham, 1932; Fretter & Graham, 1962), Cellana
(Balaparameswara Rao, 1975b) and acmaeids (Righi, 1966). Walker (1968) also describes the
development and structure of the gut in nine acmaeids.
In the Patellacea the radula has relatively few teeth in each row: a maximum of one central, with three
laterals and three marginal teeth flanking this on either side (see Fretter & Graham, 1962; Purchon,
1977). Reduction in the number of teeth has allowed
development of a few very strong teeth with a broad
attachment to the odontophare which rasp the radula
over the substratum. The body of each tooth is made
of protein (probably tanned to harden it) and chitin,
with a silica skeleton, capped with iron oxide (Fe2 O3)
cusps (Jones, MeCance & Shackleton, 1935; Runham,
1961). Lowenstam (1962) has identified the iron
oxide as Goethite (Fe2O3 ⋅ H2O), present in all
aemaeid and patellid radulae examined, but not in
fissurellids or any other prosobranchs considered. Goethite has a hardness of 5 on the Mohs scale,
making the radula harder than some, but not all, rock types. Runham, Thornton, Shaw & Wayte (1969)
reveal that the front of the cusps are rich in iron (47% Fe, 3% Si) and the back richer in silicon (30% Si,
26% Fe), and that the whole cusp is covered by a hard enamel-like material. The fibres in the cusp run
normal to the substratum in the leading edge of the cusp but parallel to it in the back face (Fig. 22). As
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
the back edge is softer and the fibre orientation more subject to wear, the tooth acts as a self-sharpening
device, keeping the front, harder edge sharp.
The patellacean radular teeth are thus formidable structures, capable of excavating rock and removing
microflora growing in crevices or even embedded in the rock surface. By contrast, the radula of
Siphonaria consists of numerous fine teeth, uniform in size, and capable of rasping macroalgae but not of
cutting into rock. This difference is probably of fundamental importance, influencing diet and affecting
the interactions between Siphonaria and patellacean limpets that are described below (p. 343).
The radular fraction (ratio of radula length to shell length) varies intraspecifically with zonation, being
greatest high on the shore (Brian & Owen, 1952; Ebling et al., 1962; Balaparameswara Rao & Ganapati,
1967; Davies, 1969b). Brian & Owen explain this by the fact that low-shore individuals can feed for
longer periods and, therefore, wear away the radula faster. Sella (1976) shows, however, that subtidal
individuals of two Patella spp have longer radulae than their low-shore counterparts. There is also a
tendency for high-shore species to have larger radulae than low-shore species, in Patella (Koch, 1949),
and in acmaeids (Creese, 1978). This trend is, however, not obvious in Walker’s (1968) analysis of eight
acmaeids.
While most limpets feed conventionally by rasping up microalgae or feeding on macroalgae, Lepeta
probably depends on detritus as it lives at fair depths (Yonge, l960a). The pulmonate Gadinalea nivea
feeds in a novel way, hanging upside down from the roofs of caves or under boulders, and orientating
away from currents. The anterior mantle produces a mucous sheet that is billowed out when currents
pass forwards under the shell, trapping particles in the water. The mucous net and its entangled particles
are then eaten (Walsby et al., 1973). Trimusculus reliculatus operates in a similar way (Walsby, 1975). Both
species have digestive tracts that are surprisingly unmodified from that of Siphonaria, except that the
radula is smaller and the teeth more slender and hook-like to handle the mucus. Filter-feeding is also
well known in Crepidula (see Newell & Kofoed, 1977a for references).
Diets of limpets
Most limpets are generalist grazers feeding on any microflora or detritus available on the rock face
(Branch, 1971; Shabica, 1971; Simpson, 1976; Creese, 1978), but some species specialize on particular
macroalgae. For example, Eaton (1968) found that Collisella limatula fed mainly on Hildenbrandia or
Peyssonellia while the co-existing Collisella pelta fed on a wide range of macroscopic frondose algae (Craig,
1968). Siphonaria spp often feed on macroalgae such as Enteromorpha and Ulva (Parry, 1977; Creese,
1978). A surprising number of species feed on encrusting corallines (or on the microflora settling on the
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
corallines): Patella miniata (Branch. 1971) and Patelloida virginea (Clokie & Norton, 1974), P. corticata
(Raflaeli. 1979). Collisella testudinalis (Steneck, 1977 and in prep.), and Acmaea sp. (Sneli, 1958).
More specialized associations occur in territorial limpets, such as Lottia gigantea which defends and feeds
on a green algal film; Patella longicosta and P. tabularis on Ralfsia expansa (Stephenson, 1936; Branch, 1971,
1975c, 1976); and Patella cochlear on Herposiphonia heringii or Gelidium micropterum (Branch, 1975c, 1980).
Finally there is a substantial number of limpets living and feeding on large host algae. Those in the north
western Pacific are listed by Carlton (1976); and other species include Helcion pellucidus (Graham &
Fretter, 1947), and Patella compressa (Stephenson, 1936; Branch, 1971, 1975c), and Scurria scurra (Vermeij,
1978).
Thus there are four basic feeding patterns in limpets: generalists feeding mainly on microalgae and
detritus or any suitable material on the rock face; species eating macroalgae, including encrusting
corallines and upright frondose algae; territorial species which are closely linked to particular food
plants; and epiphytic species that feed on their host plants. These different options have different
consequences for both limpet and plant and will be explored further on pages 357-367 of this review.
Digestive enzymes
Several studies have shown amylase activity to be very high in the digestive gland and in the foregut of
patellacean limpets, including Patella vulgata (Graham, 1932), Cellana radiata (Balaparamesware Rao,
1975b), Collisella pelta (Jobe, 1968), and four other acmaeids (Beppu, 1968). The salivary glands contain
no enzymes and are probably only lubricatory in function, and all other digestive enzymes are confined
to the digestive gland. Balaparameswara Rao (1975b) found small amounts of proteases, glycogenase,
and several enzymes digesting disaccharides. He concluded that Cellana radiata relies largely on the
simple storage products of algae, such as sugars and starch, but could not digest any of the complex
polysaccarides. Beppu (1968), however, identified alginase in four acmaeids, and smaller quantities of
fucoidinase, agarase, and laminarinase in three species, and of carageeninase in two species. Interestingly
the activity of these enzymes was drastically reduced in low-shore species that were starved for 4-6 days,
but starvation had little effect on high-shore species; a fact that is recalled below in relation to digestion
rates. Details of the activity of α- and β-glucuronidase, β-D-fucosidase, and β-n-galactosidase in Patella
vulgata are given by Marsh & Levvy (1958) and Levvy & McAllan (1963). Cellulase activity has been
recorded in the same species by Stone & Morton (1958) although Balaparameswara Rao (1975b) failed
to detect it in Cellana radiata. Jeuniaux (1963, cited by Hyman, 1967) found chitinase in Patella vulgata, and
suggests that it is generally present in gastropod digestive glands. No other authors record chitinase, but
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
principally because tests are not normally made for this enzyme. Hass (1979) describes a
carboxypeptidase in P. vulgata.
Thus, starch and simple sugars are probably generally digested by limpets, enzymes digesting more
complex polysaccharides are frequently present, and proteases may be present, but the activity of
cellulase and chitinase is known only in single species. Lipases have not been recorded. With one
exception (amylase) all the digestive enzymes of the Patellacca are confined to the digestive gland. This
has profound consequences, for while digestion in this group is almost entirely intracellular, that in
pulmonates (including Siphonaria) is largely extracellular (Runham, 1975). This influences the nature of
the food and the method of feeding, for while the patellaceans rasp off small particles and are often
microalgal grazers, Siphonaria can bite oil large fragments from macroalgae and often has large pieces of
frond in its gut (Parry, 1977; Creese, 1978). This in turn may influence the ecological interactions
between the two groups.
Only a single analysis has been made of the enzymes present during larval development: that of
Muchmore (1968), on Notoacmea scutum. Interestingly, amylase is absent, so starch cannot be one of the
storage products in the egg and larva. Unexpectedly, laminarinase occurs in the egg, trochophore, and
veliger, despite the fact that it is seemingly useless until feeding starts in the veliger stage. Algae detritus
may be taken in by the veliger and converted to sugars, and hexokinase activity only occurs in the
veliger, perhaps being used to break down the sugars that are yielded from laminarin.
Storage products
A detailed analysis of the body composition of Patella vulgata and its seasonal changes is given by
Blackmore (1969b), and related to the reproductive cycle (Blackmore, 1969a). Comparable studies in
Cellana radiata were undertaken by Suryanarayanan & Balakrishnan (1976). Blackmore (1969b) shows
that the dry body weight of a standard 36-mm animal is minimal (about 0.24 g) in winter, but rises
rapidly in spring to a peak of 0.37 g in males and 0.40 g in females in late summer. To this summer peak
an extra 0.3 g of gonad weight can be added in autumn when the female reaches its maximum size.
The polysaccharide content of Patella vulgata is lowest in winter and comprises mainly glycogen. This
rises to a maximum just before spawning in autumn. The lipid content follows a similar pattern and at
its maximum makes up a massive 20% of the body weight in females, seemingly being the most
important storage product. There is an extensive literature on the nature and structure of lipids and
sterols, including many references specifically on limpets (see Voogt, 1972 for a review and references).
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
Build-up of glycogen and lipids in the body precedes gonad development, and gonad maturation
proceeds at the expense of these stored products; but because stored products are being drawn on,
growth continues at a high rate during reproductive maturation (Blackmore, 1969a,b). Barry & Munday
(1959) found that if glucose was injected into P. vulgata, the blood sugar levels returned to normal within
four hours, although no glucose was excreted. They suggested that glucose was deposited in a nonreducing form, probably as glycogen. Prior to sexual development they found starvation had little effect
on glycogen levels, but that once the gonads started developing, maturation could continue, even if the
animals were starved, at the expense of these performed reserves. The gonads do not themselves
contain glycogen but have lipids as a reserve. As pre-reproductive juvenile P. vulgata do not lay in stores
at the time that adults do, it seems that glycogen and lipid storage are a specific adaptation for
reproduction (Blackmore, 1969b).
White (1968) analysed the glycogen content of high- and low-shore populations of Collisella scabra and
found much higher levels in the former than the latter. He related this to the lower metabolic rates of
high-shore individuals, suggesting energy saved by having a low metabolic rate may allow greater
storage. Blackmore (1969b) also found higher polysaccharide levels in mid-shore Patella vulgata than in
low-shore animals, and also suggested that this was due to the lower metabolic rate in the higher-shore
animals described by Davies (1967, 1969b). Both White and Blackmore neglected the fact that although
high-level limpets may respire at a lower rate at a given temperature, they are probably exposed to higher
temperatures for longer periods, thus elevating their metabolic rate to an unknown extent. The higher
levels of glycogen in upper-shore animals may be an insurance against possible times of shortage, which
are more likely in the upper-shore (see Sutherland, 1970).
Surprisingly high levels of carotenoids are found in the gonads of P. vulgata (Goodwin, 1950; Goodwin
& Taha, 1950, 1951) possibly derived from precursors present in the algal food. Vitamin A, derived
from carotenoid precursors, is also common in the digestive gland and gonads (Fisher, Kon &
Thompson, 1956) but the function of these compounds is not known.
Rates of feeding
The rate of food consumption in herbivorous limpets has proved the most intractable part of the energy
budget, mainly because it is difficult to quantify, under natural conditions, the intake of microflora.
Moore (1938) found a linear relationship between the area grazed and the volume of the limpet, and
Black (1977) gives equations for three species relating the area grazed to the size of the limpet. These
relationships tell us the area required by a limpet, but little about the food available or consumed.
Stimson (1970) found that the area of defended territorial algal film increased in Lottia gigantae if the
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
amount of food declined. Southward (1964a) measured the intake of a microalgal film by Patella vulgata
by allowing it to graze on a glass slide covered by an algal film, weighing the slide before and after
feeding had occurred. His results reveal some of the problems of using aquarium experiments to get a
consumption rate that is meaningful in terms of field conditions, for he found that while the limpets ate
86 mg⋅day-1⋅g-1 body weight in the first few hours, this declined to 6 mg during the first week and was
only 1.8 mg in the second week. Nevertheless, this approach is worth pursuing.
Eikenberry & Wickizer (1964) used a different approach. They capitalized on the fact that Collisella asmi
feeds on the algae growing on Tegula shells, and measured the oxygen uptake of these algae in the dark,
before and after grazing by Collisella asmi. They estimated that between 2.7 and 7% of the algae was eaten
each hour, explaining why the limpet changes from shell to shell so frequently.
I have recently tried a third approach, using territorial species (Patella longicosta and P. cochlear) which feed
on specific algae that grow in regular easily defined “gardens”. By removing the limpet (and excluding
other grazers), the rate of growth of the algae in the period immediately after removal of the limpet
could be measured. As the size of the “garden” remains static when the territorial limpet is in residence,
the algal growth rate is a measure of its consumption by the limpet. The results are discussed later in this
review, in relation to limpet-algal interactions.
The problems of measuring food intake are much less when dealing with filter-feeders, as Newell &
Kofoed (1977a,b) have shown for Crepidula, and Walsby et al (1973) for Gradinalea. The rate of removal
of unicellular algae from a suspension gives a direct measure of consumption.
In grazing limpets the pattern of movement may be important in maximizing food intake. Abe (1939)
has suggested that although Siphonaria atra follows its outward trail home, it keeps to one side of the trail,
maintaining contact at its mantle edge, but allowing it to graze adjacent to the one side of the trail, hence
avoiding covering exactly the same ground on the return passage. No-one has, however, confirmed this
pattern. Hartnoll & Wright (1977) show quite a different pattern in Patella vulgata, which moves rapidly
away from its scar, followed by a slower feeding movement and then a rapid return to the scar. It
appears that the rapid outward movement may quickly take the limpet to an ungrazed rich food source,
where it moves slowly while feeding and then returns quickly over the previously grazed area to its scar.
It would be worth pursuing this movement to test experimentally if speed of movement is linked with
food availability. Calow (1974) showed that Ancylus fluviatilis moved regularly back and forth when food
was available, but completely randomly in its absence. Random search probably improves the chance of
finding a new patch of food.
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
Cook & Cook (1981) have shown that two species of Siphonaria may make several excursions from their
scars each tidal cycle. If the interval between excursions is less than four hours, the limpets avoid
heading in the same direction as their previous journey. Presumably this prevents retracing areas recently
grazed. If the trips are separated by one or two tides the directions the limpets ‘head out’ are random.
Funke’s (1968) photographs of movement in Patella vulgata and P. coerulea also suggest a similar pattern in
limpets kept in aquaria: their grazing paths radiate out from the scars with little overlap in successive
trails. Further analysis is, however, needed to check this.
Finally Hirano (1979b) shows that Cellana toreuma moves vertically up the shore with rising spring tides
and vertically down with the falling spring tide; but during neap tides its movement is much more
random and it tends to move laterally rather than vertically. This pattern, too, will minimize grazing over
the same area until the algae have had opportunity to recover; but again there is no proof that this is the
reason for this pattern.
There are also several intraspecific and interspecific responses between animals or in relation to density
that will increase food intake, and these will be discussed below in relation to competitive interactions
(pp. 337-340).
FAECAL PRODUCTION
The contribution of faeces to the energy budget
of limpets is seldom measured, although it may be
a significant fraction. Branch & Damstra
(unpubl.) have measured faecal output in five
Patella spp. and found the rate of production to
be very different in the different species (Fig. 23).
Furthermore, they found a linear correlation
between the growth rate of the animals and the
faecal production. P. granatina and P. oculus which
are fast-growing, short-lived, species had the
highest production; P. granularis was intermediate, while the slow-growing, long-lived, territorial species,
P. longicosta and P. cochlear, had clearly the lowest output. Because consumption has never been adequately
measured we cannot accurately assess the absorption efficiency, but by summing the components of the
energy
budget
I
have
estimated
%
absorption
efficiency
(AE)
as:
AE
=
[(Pg+Pr+Pmuc+R)(Pg+Pr+Pmuc+R+F)] x 100. Even although this leaves much to be desired, the results
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
are interesting. For the fast-growing species (P. oculus and P. granatina) AE is 72-79%; for P. granularis it is
78-82%; for P. longicosta, 86%; and for P. cochlear, 93%. There is thus an inverse relationship between the
rate of faecal production (some indication of feeding rate) and the efficiency with which food is
absorbed. Newell & Branch (1980) have suggested that species with an abundant food supply may be
“exploiters”, using food rapidly but inefficiently while those short of food are “conservers”, depending
more on minimizing energy losses because intake cannot be high. The efficiencies given above conform
to this suggestion. Beppu (1968), in comparing the digestive enzymes of several acmaeids found that
starvation, strongly influenced the enzyme activity of low-shore species but not of high-shore species,
and he suggested that this was due to a more rapid gut clearance rate in the low-shore species. This too,
conforms with the above hypothesis.
Parry (1977), in perhaps the most complete energy budget studies done so far on limpets, found the rate
of faecal production was strongly seasonal in Cellana tramoserica, being reduced in summer. He related
this to depressed standing stocks of algae in summer. In Patelloida alticostata the trend is less obvious but
the organic content of the faeces rises during winter and spring and is inversely correlated with the rate
of faecal production (r = -0.67). This can either mean more efficient absorption with a slow passage
through the gut, or ingestion of food with a higher organic content during winter and spring.
EXCRETION
The patellaccan limpets have an enlarged right kidney that lies over the visceral mass emptying into the
right papilla next to the rectum, while the left kidney is very small, although still discharging via a left
papilla. Reno-pericardial ducts traverse from the pericardium to each kidney, and the right kidney also
links with the gonad (Davis & Fleure, 1903; Walker, 1968). Nuwayhid et al. (1978) suggest that the gills
of Patella vulgata may function as an accessory excretory organ, as phagocytic cells are quite common in
the gill haemocoel, and processes from these cells interdigitate between the epithelial cells, seemingly
releasing granules to the exterior. They cite Cuenot (1914) as showing that particles injected into P.
vulgata accumulated in phagocytes in the gill, as does radio-opaque dye (Brown, 1967).
Nitrogenous excretory products have been investigated in several acinaeids by Baribault (1968) who
found that all excreted ammonia, urea, and uric acid. Substantial variation between individuals obscured
any trends, but there was certainly no relationship between zonation and the proportion of these three
nitrogenous excretory products. Uric acid accounted for 40-44 % of the nitrogenous excretion in most
of the species. Duerr (1968) also recorded ammonia excretion in Collisella digitalis and Notoacmea scutum,
but could not detect any urea. He too, concluded that the amount of ammonia excreted was unrelated to
zonation, or to body size, diet, or metabolic rate. Duerr (1967) showed that the uric acid content in
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
Collisella digitalis was positively correlated with body size and inferred that the limpet stores uric acid and
may use it as a nitrogen depot.
As Campbell (1966) has failed to find arginase in acmaeids, the origin of urea in these limpets is
speculative. If the ornithine cycle really is absent in limpets, the ammonia may be derived directly from
protein catabolism and the urea and uric acid from purines. Our knowledge of nitrogen excretion in
limpets is so fragmentary, however, that it would be dangerous to generalize. As described above,
Emerson (1969) has investigated the rate of ammonia excretion in relation to osmotic stress.
The contribution of excretory products to the total energy budget of limpets is difficult to estimate,
since no one has measured energy losses through this path in relation to total energy flow. But from the
rates of excretion described in the above papers it is likely to be a very small fraction of the total budget.
RESPIRATION
Numerous accounts of respiration rate exist for limpets, mainly because of the ease of taking
measurements of oxygen consumption. Methods used include Winkler titrations of oxygen levels,
oxygen probes, polarographic methods, and respirometers of various kinds. Comparisons between the
results quoted by different authors are often complicated by the failure to state the size of limpets
investigated and to specify the precise conditions under which measurements were made.
Morphology in relation to respiration
Acmaeids all have a single (left) ctenidium in the mantle cavity over the head. In most of the family this
is the only gill, but in Lottia it is supplemented by a cordon of accessory gills running around the pallial
cavity and interrupted only over the head. In Scurria the cordon is complete. The patellids all lack the
ctenidium but have an incomplete cordon of pallial gills in Helcion and a complete circle of these gills in
Patella and Cellana (Yonge, 1947). The gill arrangement may have profound consequences. The lepetids
lack gills and are all very small; most acmaeids have only a ctenidium and are larger; but Lottia or Patella
spp. achieve by far the greatest sizes and possess pallial gills.
The Siphonariidae have, of course, a totally different structure: the mantle cavity forms a lung, richly
supplied by blood vessels and lying over the visceral mass with a pneumatophore opening laterally.
Presumably evolved for aerial respiration, the roof of the mantle has secondarily been thrown into folds,
forming gill-like structures. Water can be circulated past these gills by cilia on the dorsal and ventral
ridges in front of the gills (Yonge, 1952; Marcus & Marcus, 1960). In Trimusculus the mantle cavity is
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
simpler, there being no gill-like folds; presumably because the animals are sedentary filter-feeders there is
no need for a sophisticated gill structure (Yonge, 1958).
Details of the structure of the pallial gills in Patella vulgata are given by Nuwayhid et al (1978), who show
the pallial gills to be remarkably parallel in structure to the ctenidial arrangement, despite being
independently derived secondary gills. Each gill has a series of lamellae that are crossed by a prominent
ciliated groove that is presumed to eliminate large particles from the gill surface. Dense cilia on the outer
margin create currents of water that run counter to the blood-flow through the gill. Nuwayhid, Davies &
Elder (1980) describe the effects of oil and dispersants on the microstructure of the gill.
Yonge (1947, 1962) summarizes the pattern of water flow through the pallial cavity of an array of
limpets, and terms these “cleansing currents”. In P. vulgata continual inhalant and exhalant currents
occur right round the gill cordon, but in addition, currents travel around the foot to deposit wastes
(including faeces) on the mid-right side of the animal, whence they are expelled by muscular movements
drawing the shell down. In small animals wastes are consolidated by a glandular peripheral streak around
the foot (see Fig. 17) which Yonge (1947) suggests is functionally equivalent to the hypobranchial gland.
This is lost in larger animals. In aemacids there is a respiratory inhalant current on the left of the mantle
cavity and an exhalant current on the right. In addition pallial cleansing currents move around the pallial
cavity, depositing wastes either posteriorly or on the left of the animal. Only in Notoacmea paleacea do
these currents pass forwards, and wastes are cast out on the right of the mantle cavity in the exhalant
respiratory current. This peculiarity relates to the habitat; N. paleacea lives on narrow blades of
Phyllospadix and its shell has a small notch to the right of the head through which exhalant currents pass
(Yonge, 1962), and gametes are released (Fishlyn, 1976). Acmaeids living in turbulent water, including
Lottia gigantea (Abbott, 1956) lack these cleansing currents, evidently relying on water movement to
perform the task (Yonge, 1962). In Siphonaria there are no cleansing currents around the foot. Yonge
(1952) suggests that the cilia were lost during the limpet’s terrestrial existence and are no longer needed.
Kingston’s (1968) work on acmaeids has cast a new light on respiratory surfaces in limpets. He showed
that the mantle edge has a fine capillary network capable of allowing oxygen exchange; and he suggests
that the “cleansing currents” of Yonge may be respiratory in function (possibly in addition to cleansing)
for they flow counter-current to the blood flowing through the pallial network. To prove the respiratory
function of this network, Kingston inserted minute platinum/silver electrodes into various parts of the
vascular system to measure oxygen levels. Between the visceral sinus and the anterior efferent vessel,
oxygen rose from 1.08 ml⋅-1 to 1.40 ml⋅-1, an increase that could only be due to oxygenation in the
circumpallial network. Further oxygenation occurs in the ctenidium, raising levels to 1.67 ml⋅-1. Kingston
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
also suggests that in high-shore species the ctenidium is relatively small and the circumpallial vessels
more important than in low-shore species, and that the ctenidium functions mainly in aquatic respiration
but the pallial network in aerial respiration. He proved that if the ctenidium is clamped off, survival in
water is poor, but in air all animals survived more than 48 h. Furthermore, in air the level of blood
oxygenation remained as high as in controls, while in water it was lower in the experimental limpets.
Jones (1970) has investigated the heart mechanism in Patella vulgata. The general theory of heart filling in
gastropods is that when the ventricle contracts, the pressure inside the pericardium reduces to levels
below that in the auricle, consequently sucking the auricle open. It has often been questioned whether
the pericardial wall is rigid enough to sustain such pressure differentials. but Jones’s data clearly
demonstrate that this mechanism does operate. The pericardium also houses a third chamber, the
bulbus aortae, which receives blood from the ventricle and leads into the aorta. Jones (1968) showed
that the bulbus aortae acts as an auxiliary pump, contracting at about half the rate of the ventricle, and
only functioning when the limpets are under water. Jones surmises that the auxiliary pump is needed
when the limpets are active and feeding during submergence. De Baissac & Branch (unpubl.) compared
a series of Patella spp. and found the bulbus aortae was proportionally larger (relative to the ventricle) in
subtidal species than in low-shore species which, in turn, had a larger bulbus than high-shore species.
Factors affecting rates of oxygen consumption
A host of factors can influence rate of oxygen consumption. These include body size, temperature
activity, seasonal effects, oxygen tension, starvation, and endogenous rhythms. Newell (1979) gives a
comprehensive review. The effect of body size on respiration rate is well known. Rate of oxygen
consumption per individual (R) is related to body weight (W) by the function: R = aWb. Plotted
logarithmically this relationship has a slope of b, and Hemmingsen has suggested a generalized value of
0.75 for b in ectotherms (see Davies, 1966). Some limpets such as Nacella concinna conform closely to this
(Ralph & Maxwell, 1977), but only one species exceeds this value, while 14 have lower values (Davies,
1966, 1969b; Parry, 1977; Branch & Newell, 1978; Branch 1979a: Balaparameswara Rao, 1980), the
lowest recorded being 0.43 for Helcion pectunculus (Branch & Bouchers, unpubl.). The value of b is nearly
always lower in aquatic than in aerial respiration, and there is a suggestion that in aquatic respiration b
declines as one moves from the high to the low shore (Branch & Newell, 1978), but there are exceptions
and additional data are needed to test this idea. The implication of this system is that respiration is less
size-dependent in the high-shore which may be linked with a shortage of food there: so that metabolic
rates are related more to metabolite availability than to body size.
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
There is a tendency for authors to test whether the slopes derived at different temperatures or in air and
water are statistically different and to use a common slope if they are not. Statistically this is a valid
procedure, but it may obscure biological trends. For instance, during aquatic respiration in Patella
granatina b declines regularly as temperature rises, meaning that large animals respond less to a change in
temperature (Branch, 1979a). As P. granatina migrates up the shore, larger animals are found higher on
the shore, where temperature fluctuations are greater, so the change of b with temperature may have
some biological significance.
Temperature is one of the major factors affecting rate of oxygen consumption, and the subject is
reviewed by Newell & Branch (1980), and oxygen consumption in a number of marine limpets has been
related to temperature by Davies (1966, 1967), Baldwin (1968), Bannister (1970, 1974), Doran &
McKenzie (1972), McMahon & Russell-Hunter (1977), Parry (1977), Branch & Newell (1978), and
Branch (1979a). In general a doubling of metabolic rate is anticipated with a 10oC rise in temperature: i.e.
a Q10 of 2.0. In fact Q10 varies widely, not only between different species but at different temperatures.
Three interesting patterns emerge. First, Davies (1966) showed that for P. vulgata Q10 is lowest over the
range 15-20oC, and he suggested that this is a form of acclimation, keeping metabolism reasonably
constant over the usual environmental temperature range. Collisella scabra shows the same effect
(Baldwin, 1968), as does Helcion pectunculus (Branch & Bouchers. unpubl.); but tissue extracts do not
(Davies & Tribe, 1969).
Secondly, there are some species, such as Patella granularis (Branch, 1979a) and Collisella digitalis (Baldwin,
1968) which have generally low Q10 values in comparison with other species, making them much more
independent of temperature. In the past this has often been related to the need to minimize metabolic
costs at high temperatures which, of course, are usually experienced during daytime low-tides (see
Newell, 1979 for a review). This explanation is satisfying for a high-shore species such as Patella granularis
which is known to be short of food (Branch & Newell, 1978) but, on the other hand, low Q10, values
also occur in P. granatina which is a mid-shore species with an extremely fast growth rate (Branch,
1979a). I surmise that a low Q10 has the opposite effect in this case. This species lives in areas of
upwelling where sea temperatures may drop by as much as 10oC in very short time periods, and where
the differences between air and water temperatures are much greater. Consequently a low Q10 could help
to keep metabolism high in spite of a rapid drop in temperature. P. granatina is seemingly not short of
food. Branch & Newell (1978) and Newell & Branch (1980) have suggested that some limpet species are
“conservers”, being short of food, and a low Q10 may help in the conservation of their energy.
Conversely, species such as P. granatina have plenty of food and it may be better for them to exploit this
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
as rapidly as possible. “Exploiters” may maintain a high metabolic rate at low temperatures by having a
low Q10 but a high metabolic rate.
Thirdly, there are species, such as P. oculus with high Q10 values (Newell & Branch. 1978) which contrast
with P. granularis being “exploiters” that allow their metabolic rate to rocket at higher temperatures; and
they, too, have very fast growth rates and evidently are not food-limited. While oxygen consumption
rises with temperature, a critical temperature is reached beyond which it falls, and this temperature is
closely related to the upper extremes normally experienced by an animal. In the high-shore Collisella
digitalis it exceeds 25oC while low-shore Notoacmea fenestrata it is 15oC (Doran & McKenzie, 1972).
Similarly, Baldwin (1968) showed that even in coexisting species the critical temperature differs: in
Collisella scabra, which occupies flat surfaces where it is exposed to solar heating, it exceeds 25oC; while in
C. digitalis, which usually lives on sloping surfaces and presumably heats up less, Baldwin found the
critical temperature to be
between
20
and
25oC.
Measurements on seven South
African limpets (Table VI)
show a direct correlation (r =
0.88) between upper limits of
zonation
and
critical
temperature.
Critical temperature is not necessarily the same in air and in water, being 30oC in water and 25oC in air,
for C. testudinalis (McMahon & Russell-Hunter, 1977), although in all the species listed in Table VI there
were no differences between aerial and aquatic respiration. Critical temperatures can be raised by
acclimation to higher temperatures, as Newell & Kofoed (1977b) have shown in Crepidula fornicata.
Intraspecific differences in metabolic rate have been related to zonation, high-shore individuals of Patella
vulgata having lower rates than low-shore animals (Davies, 1965, 1966, 1967, 1969b). Smith (1975) also
showed this effect in Cellana ornata and White (1968) in Collisella scabra, although Sutherland (1972) could
find no differences between high- and low-shore C. scabra. Davies (1967) revealed that differences
between high- and low-shore populations were not apparent in winter, but in summer the high-shore
specimens remained constant while the metabolic rate of low-shore individuals increased. This is
interesting, for if the effect is due to seasonal acclimation this is a case of reverse acclimation (i.e.
metabolism is elevated after warm-acclimation rather than depressed). Davies (1970) also measured the
temperature difference between high- and low-shore Patella vulgata and concluded that the difference was
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
not enough on its own to explain the disparity in metabolic rates. His earlier work (Davies, 1967)
showed that other environmental differences (which probably amount to food availability) were at least
as important as temperature in setting the level of oxygen consumption.
Markel (1974) has shown in laboratory experiments that a reduction of temperature results in a
compensatory rise in the metabolic rate as acclimation occurs, and his parallel work on heart rates has
been discussed above. Like Davies, he concluded that temperature on its own was not an adequate
explanation of seasonal changes. Nevertheless, Catlett (1971) showed that as short a period as 24 h
exposure to 15oC can elevate the metabolism of Collisella scabra 37% in comparison with control animals
kept at 21oC. This extremely rapid acclimation (which seemingly was complete within 24h as prolonged
exposure to 15oC failed to change the rate any further) is taken by Catlett as an adaptation to short-term
environmental changes (i.e. tidal changes). It is doubtful, however, whether the six-hourly tidal changes
can be compensated for by acclimation, and in fact acclimation can have undesirable effects when shortterm fluctuations of temperature are experienced (see Calow’s 1975 argument, given below).
Seasonal changes in metabolic rate have been recorded in two aemacids and a siphonariid by Parry
(1977), and very marked changes occur in some freshwater limpets such as Ancylus fluviatilis (Berg,
Lumbye & Ockelmann, l958, Calow, 1975) and Laevapex fuscus (MeMahon, 1973).
Parry (1978) has attacked the concept of acclimation. He points out that there is “reverse acclimation” in
a number of species, which at first sight is maladaptive. He suggests that all seasonal changes of
metabolic rate are due to factors such as food availability and the amount of synthetic activity in the
form of growth and reproduction. Using known
data on the growth rate and reproductive
development of Cellana tramoserica, Parry calculated
the metabolic equivalent (in terms of oxygen
consumption) of these activities, over a period of a
year, and was able to show a close correlation
between the calculated and the measured oxygen
consumption (Fig. 24). This original approach is
the first demonstration that seasonal fluctuations
in respiration rate are related to growth of the body
or gonads. Markel (1974) came to the same
conclusion in relation to heart rate. By this argument, “reverse aecliniation” is not acclimation at all, but
simply greater metabolic activity during growth. Parry’s point is well taken, but he pushes his argument
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
too far in trying to discard the phenomenon of temperature acclimation in its entirety: under controlled
laboratory conditions, acclimation does occur (e.g. Catlctt, 1971; Markel, 1974) and even the underlying
biochemical processes are partly understood (Markel, 1976).
Both Calow (1975) and McMahon (1973) have suggested “reverse acclimation” has an adaptive value.
McMahon (1973) relates the phenomenon to the habitat occupied by the freshwater limpet, Laevapex
fuscus, which lives on rocks during summer but migrates down into low oxygen muds in winter. During
summer (and in warm-acclimated animals) oxygen consumption is directly related to oxygen availability
(that is, the animals are oxyconformers). In winter, however (and after cold-acclimation), oxygen
consumption is almost independent of external levels (oxyregulation), allowing the animals to keep up
their oxygen consumption in the oxygen-poor muds, hence avoiding anaerobiosis and using the stored
carbohydrates more efficiently (Fig. 25). Hence, McMahon
shows that “reverse acclimation” only occurs at high
oxygen levels, while normal acclimation occurs at lower
oxygen tensions, the difference being related to the need
to oxyregulate in winter. Newell, Johnson & Kofoed,
(1978) found quite the reverse response in Crepidula
fornicata: acclimation to higher temperature increased
oxyregulatory ability.
Calow (1975) has a different explanation for the role of
reverse acclimation in Ancylus fluviatilis, which occurs in
shallow wave-washed areas where oxygen levels are
always high, but where temperatures are low and can
fluctuate widely. Calow shows how A. fluviatilis that are
transferred from 4oC to 10oC do not have a rate that is
initially higher than that of animals acclimated at 10oC
(as would be expected, if acclimation had taken place)
and it takes about five days for the transferred animals
to reach the rate of those kept at 10oC (Fig. 26A). This is
typical of reverse acclimation. Animals held at 18oC have
initial rates higher than those held at 10oC (when both
are measured at 10oC): again due to reverse acclimation.
Had ‘normal’ acclimation taken place one would expect
the warm-acclimated animals to have overshot the rate
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
exhibited by 10oC animals and to have had a metabolic rate less than that of the 10oC animals. Calow
points out that “reverse” acclimation effectively damps down the metabolic oscillation that might have
been expected with rapid fluctuations of environmental temperature.
McMahon & Russell-Hunter (1978) have compared the respiratory responses of six marine
prosobranchs, including one acmaeid limpet, to reduced oxygen levels. Those species which experience
low oxygen tensions in their natural habitats did not build up an oxygen debt when exposed to low
oxygen levels and were able to regulate oxygen consumption over a wide range of oxygen tensions, and
subsequent to low oxygen stress had elevated metabolic rates. On the other hand, Collisella testudinalis
was one of the species showing neither response, and building up an oxygen debt at low tensions (and
presumably using the uneconomical anaerobic pathway). McMahon & Russell-Hunter show that these
species live in areas where oxygen is always readily available: in the case of C. testudinalis, due to vigorous
wave action. Consequently neither species has need for the above regulatory process.
Activity also influences oxygen consumption, although it is difficult to quantify. Houlihan & Newton
(1977) showed that metabolic rate could rise 250% in Patella vulgata that had to cling more tightly to the
substratum. They demonstrated this by hooking the shell up to a pulley and then measuring oxygen
consumption after the animal had been subjected to different tensions by loading the pulley.
Newell & Kofoed (1977a) showed that the rate of oxygen consumption in Crepidula fornicata almost
doubled when food was introduced and the animals started filter-feeding. They obtained a linear
relationship between filtration rate and oxygen consumption, and by extrapolating to zero filtration
could determine the “standard” rate of oxygen consumption which was very close to the level they
measured in water that lacked any food.
The only mobile grating limpet for which the cost of locomotion has been determined is the freshwater
limpet Ancylus fluviatilis. Calow (1974) constrained some animals while others were allowed to move
freely, and he measured their respective oxygen consumptions. If the animals were satiated with food,
they moved little and both sets of animals had similar metabolic rates. Within a few hours the rate in
constrained animals, however, dropped, almost exactly paralleling the rate of gut clearance (measuring
by retention of radio-actively labelled food). This implies that a fair proportion of the oxygen
consumption is due to the specific dynamic action (i.e. processing of food). In contrast, the mobile
limpets became very active and this activity raised the oxygen consumption about 30% over that of the
‘resting’ level (Fig. 26B). Only when internal reserves were depleted by starvation did levels of active and
mobile animals become similarly depressed (Fig. 26B). Calow suggests that this pattern of increased
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
movement in the absence of food will suit a grazing limpet which must search for food rather than
waiting for better times as a carnivore or scavenger might do. The influence of starvation on oxygen
consumption has never been experimentally investigated in marine limpets and badly needs
quantification, as a number of authors (e.g. Davies 1967; Parry, 1977) have deduced that seasonal
depression of metabolism must be due to a shortage of food, but as many variables may be affecting
oxygen consumption in the field we cannot isolate starvation as the only culprit.
Endogenous rhythms of oxygen consumption have not been satisfactorily shown in marine limpets,
although Gompel (1937) suggested that they exist in Patella vulgata, and Balaparameswara Rao (1980) has
shown that Cellana radiata consumes oxygen faster at high tide than at low tide, particularly at night. This
presumably correlates with periods of greater activity. Branch & Newell (1978) could find no striking
rhythmicity in three Patella spp.
Finally, exposure to air or water may have a substantial effect on oxygen consumption. Bannister (1970,
1974) found that the high-shore Patella lusitanica respires faster in air than in water, while in low-shore P.
coerulea the reverse is true. MeMahon & Russell-Hunter (1977) also found that the low-shore Collisella
testudinalis respired faster in water than in air. On the other hand, C. digitalis, despite being a high-shore
species, respires least in water, slower in damp situations and slowest in dry air (Baldwin, 1968). C. scabra,
which coexists in the high-shore with C. digitalis, shows this trend even more strikingly; its rate in water
is 2.25 times that in damp situations and 4.36 times that in air. Contrary to this, Doran & McKenzie
(1972) found that C. digitalis respired faster in air than in water and low-shore Notoacmea fenestrata respired
at the same rate in both media. They criticize Baldwin’s methodology, and suggest that his results were
due to excessive desiccation prior to measurements of aerial respiration. While it is true his “arial”
condition relied on drying the animals with blotting paper for 3.5h, the “damp” animals were not
excessively desiccated.
A comparison of several South African Patella
spp. is interesting in this context. Branch &
Newell (1978) found the extreme low-shore P.
cochlear indifferent to air or water in terms of
respiration rate. Mid-shore P. oculus varies in its
response depending on body size. Small animals
tend to be more aquatic, living in pools or damp
crevices, and respire faster in water than in air
over most of the temperature range. Large P.
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
oculus occur on dry rocks, and over the temperature range they experience when exposed, they respire
faster in air (Fig. 27A). Thus in this species metabolism is kept high by a shift in the air/water response
as the animals age. P. oculus is one of the species Newell and Branch (1980) suggest is an “exploiter” with
a high turnover rate. In contrast, the very high shore P. granularis shows exactly the reverse pattern. P.
granularis migrates up the shore as it ages, small animals occurring below mid-tide or in damp areas; and
respiring faster in air than in water (Fig. 27). Conversely, larger animals at high-levels are covered by
water only briefly, yet they respire raster in water than in air (Fig. 27B). As this limpet seems short of
food, Branch & Newell (1978) suggest that it is a “conserver” and that metabolic rates (and hence
energy losses) are kept low by this respiratory pattern.
Partly as a test of this idea, Branch (1979a) examined the respiration rate in P. granatina, which is
ecologically equivalent to P. oculus, also being a fast-growing mid-shore species. He found precisely the
same pattern as in P. oculus, but even more strikingly displayed. P. granatina also migrates up the shore.
Small low-shore individuals respire faster in water than in air, and large high-shore specimens faster in
air than in water. At the size range spending 50% of the time emerged and 50% submerged, respiration
is the same in air and in water. Thus, again P. granatina has a respiratory pattern maintaining as high as
possible a metabolic rate, conforming to the predictions based on another “exploiter”, P. oculus.
Comparative rates of respiration
Branch (1979a) has attempted to compare the rates of respiration recorded in the literature for 10
patellacean limpets. Comparisons such as this must be treated with caution, for not only are
measurements made under different conditions, but intraspecific variability can be considerable.
Nevertheless, the comparison shows substantial difference between the species, covering about a
sevenfold range.
Six South African species have been compared over complete tidal cycles, and in light and darkness, to
simulate natural conditions. These analyses allow estimation of the total metabolic energy output by
animals of a standard size over a 24-h period. For each of the species, measurements have been made of
the standing stock of algae or microalgae available; and for four species production rates of food have
been measured (Branch, 1980 and unpubl.). These enable us to rank the species in terms of food
availability. P. compressa, living on kelp plants, has a superfluity of food. P. oculus and P. granatina are midshore species in an area of low algal biomass but high production. P. cochlear, although a low-shore
species, occurs at extremely high densities so that the food availability per animal is not high. P. granularis
and Helcion pectunculus are high-shore species occurring where algal biomass and productivity are low.
Figure 28 shows that the metabolic energy losses of these species decline in a similar sequence.
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
Branch & Newell (1978) and Newell & Branch (1980) have suggested that food availability is critical in
determining whether a species should conserve its energy as much as possible or can be seemingly
profligate, with a high turnover and rapid processing of food, and a consequently high loss of energy as
metabolic heat.
Forms like Patella granularis, that suffer from a food shortage, may reduce metabolic energy losses in a
number of ways, including having low metabolic rates in comparison with other species, low Q10 values
(and hence relative independence of temperature), and different rates in air and water that are capable of
minimizing energy losses. A similar case for energy conservation has been made out for Nacella concinna
by Ralph & Maxwell (1977). Conversely, Patella granatina, P. oculus, and P. compressa, with an abundant
food supply have quite the reverse patterns, and in various ways maintain very high metabolic rates.
Limpets are not unique in this dichotomy between conservers and exploiters, and a brief comparison of
other forms is given in Branch, Newell & Brown (1979), in which other methods of reducing energy loss
are also mentioned, including acclimation and endogenous rhythms. A number of limpets have rhythms
of movement which result in feeding only when the animals are covered by water, or if they feed when
exposed, it is only in the cool of the night (see Table IV). Traditionally this is seen as preventing
desiccation, but it may also minimize activity when heat would make the increased metabolic losses
more costly. When more complete data are available on the cost of movement at different temperatures,
this question can be examined more critically.
MUCUS PRODUCTION AND LOCOMOTION
The mechanism of locomotion in P. vulgata is described by Jones & Trueman (1970). Retrograde waves
move backwards on the foot while the animal is moving forward, and the waves on the left and right
sides of the foot are out of phase (ditaxic). The foot has strong dorso-ventral muscles but no
longitudinal muscles. Jones & Trueman suggest that movement of pedal waves depends vitally on small
subepithelial haemocoelic spaces. If the dorsoventral muscles lift the sole, these spaces will be
compressed, presumably increasing the pressure in the spaces, while under the foot a decrease of about
6 cm pressure can be recorded, Increased pressure in the spaces will expand the foot forwards. After the
dorso-ventral muscles relax, the pressure differential between the spaces and that beneath the foot will
return the sole to the substratum. Thus longitudinal muscles are not required. Grenon & Walker (1978)
point out that Jones & Truman’s “haemocoelic spaces” are a misinterpretation of pedal mucocytes, but
there are small blood spaces below the sole (Branch & Marsh, 1978) as Grenon and Walker themselves
describe, so the above mechanism is still feasible.
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
Miller’s (1974) analysis of foot-design in gastropods shows that the shape of the foot in limpets allows
both strong adhesion and relatively rapid locomotion (see above, 270).
The energetic cost of locomotion is described above in relation to rates of oxygen consumption, but
both adhesion and locomotion have a further cost: production of mucus. Branch & Marsh (1978) have
measured the amount of mucus secreted by stationary limpets; it varied between species, from 0.5 to
11.47 mg wet wt⋅cm-2 of sole. With caution, these results can be used to estimate the contribution of
mucus to the energy budget (Branch, 1980 and unpubl.). As an example, Figure 35 (see p. 316) shows
that in Patella longicosta, mucus accounts for
almost half the production. I have been unable
to obtain measurable amounts of mucus from
the trails of moving Patella spp. and surmise that
relatively little energy is spent on mucus
secretion during locomotion. Calow (1974),
however, collected the mucus produced by
Ancylus fluviatilis during locomotion, and showed
it was equivalent to 9%, of the energy intake.
Mucus is also used for other purposes. Helcion pellucidus produces copious quantities when it is detached,
and these sticky strings allow it to fasten onto algae (Vahl, 1971). Cellana spp. have a mantle edge richly
supplied with mucocytes that seem to have an offensive function (Branch & Branch, 1980) and
analogous glands occur in Siphonaria (Fretter & Graham, 1954) and Crepidula (Graham, 1954). Several
acmaeids produce a sheath of mucus between shell and substratum to reduce desiccation (Wolcott,
1973; Dixon, 1978). Faecal compaction requires mucus, estimated at 4-6% of ingested energy in Ancylus
(Calow, 1974). In Nacella concinna thick antifreeze sheaths are produced around animals caught under ice
(Hargens & Shabica, 1973). The amount of energy diverted into mucus for these purposes is unknown,
but apart from faecal compaction, adhesion, and locomotion, all the above events are intermittent and
unlikely to be very costly.
GROWTH
Measurement
Measurements of growth have been made on a large number of limpets (sec Table VII). A variety of
methods has been employed to measure growth, including measurement of labelled animals (Branch,
1974b) annual growth rings (Abe, 1932; Kenny, 1968; Picken, 1980), checks in growth due to known
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
changes of environmental conditions (Vahl, 1971), measurement of the mean size of cohorts at different
time intervals (Blackmore, 1969a; Branch, 1974a; Underwood, 1975a), but perhaps the most original
approach is that of Shackleton (1973). In the
deposition of calcium carbonate there is a
small isotopic discrimination,
18
O being
taken up more frequently than 16O, and this
abundance ratio is reduced by about 0.2
o/oo for every oC rise in temperature. Thus,
if the environmental temperature varies
seasonally,
seasonal
changes
in
the
abundance ratio will exist at different
distances from the edge of the shell. This has
proved a useful tool for archaeologists,
allowing determination of the season in
which death of molluscs occurred; it has also
allowed estimation of growth rate in Patella tabularis (Shackleton, 1973).
Intraspecific variation in growth rate
A number of factors may alter the growth rate of limpets. Other factors being equal, increase in tidal
height usually results in a decrease in growth (see Fig. 44) (Ballantine, 1965; Sutherland, 1970; Lewis &
Bowman, 1975; Black, Fisher, Hill & McShane, 1979). Seasonal changes are also well known in a
number of species, usually related to availability of food (Frank, 1965a; Kenny, 1968; Parry, 1977;
Picken, 1980). These changes are not always linked directly to algal standing stocks. For instance,
Sutherland (1970) showed that growth in high-shore Collisella scabra is reduced in summer when algae die
back, but low on the shore growth is least in winter when numbers of limpets rise due to recruitment,
and intraspecific competition is greatest.
In two Cellana spp. Kay & Magruder (1977) showed that growth is very rapid until sexual maturation
begins; and in Helcion pellucidus this pattern is even more marked, perhaps not surprisingly as the species
is essentially annual and further growth beyond sexual maturity will be misdirected (Vahl, 1971). Growth
of Notoacmea petterdi also virtually ceases as the gonad matures (Creese, 1980c). Conversely in Collisella
limatula, in spite of the fact that the gonad constitutes up to 36% of the flesh weight, growth is highest
during the period of gonad build-up (Seapy, 1966). Blackmore’s (1969a,b) work provides the explanation
of this: carbohydrate and lipid stores arc laid-up prior to sexual development and drawn on to allow
maturation to proceed while body growth continues at a high level.
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
Intraspecific competition often affects growth (see below for further details), and may influence some of
the patterns mentioned above. C. digitalis migrates up the shore during winter and spring, and migrant
animals grow faster than those that do not migrate (Breen, 1972). The presumed reason for this is that
fewer animals occur higher up and competition for food is less. High-shore C. scabra also grow faster
(and to a greater size) than their low-shore counterparts, and they too have a lower density (Sutherland,
1970). Experimental reduction of numbers confirms that density influences growth. Creese’s (1980c)
work on Notoacmea petterdi helps disentangle the effects of
density and shore-height. This species has a similar
pattern to that of C. scabra, and at any given height on the
shore, increased density reduces growth, while at given
densities growth is lowest high on the shore (Fig. 29).
The pattern that appears is that there is less food in the
high-shore, but because fewer limpets occur there, there
may be more food per limpet.
The presence of other species may also influence growth. Competition from other grazers or the
presence of sessile forms that reduce the area available for feeding will reduce growth (see below in
relation to interspecific competition). Giesel (1969) has shown that in some areas there are two forms of
C. digitalis: a dark form on bare rock and a paler form amongst the barnacle Pollicipes. The paler form
grows very slowly, about 0.5 mm⋅yr-1, in contrast to the 7 to 8 mm⋅yr-1 by the dark form. Giesel suggests
the slow growth is genetically determined as there is no evidence of food shortage, and proposes that
slow growth is necessary if the paler form is not to outgrow the limited space available on the slowgrowing barnacles. This is an important concept that needs to be experimentally tested, for it contrasts
with the other factors discussed above. Whereas these other factors ‘boil down’ to the relative
availability of food having a dominant influence on growth rate, Giesel’s suggestion implies that there
has been selection for growth rate.
Wave action may also modify growth. Thompson (1979) discusses how Patella aspera dominates wave
beaten shores while P. vulgata replaces it under more moderate wave action (Fig. 30). The growth rates of
P. aspera are generally lower than in P. vulgata and much less variable. Thompson suggests that P. aspera is
not very flexible in its growth responses and is out-competed by the faster-growing P. vulgata under
more favourable conditions (i.e. less intense wave action). On the other hand, the growth rate of P.
vulgata declines with more violent wave action while P. aspera maintains a comparatively constant growth.
In a subsequent paper, Thompson (1980) shows that the decline in the ratio of P. vulgata : P. aspera
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
numbers as wave action intensifies is accompanied by a decline in the growth of P. vulgata relative to that
of P. aspera (Fig. 30).
The underlying cause of this effect is
speculative,
but
as
oxygen
consumption rises in animals that are
forced to adhere more tightly because
weights are applied that pull upwards
on the shell (Houlihan & Newton,
1977), the increased energy losses may
reduce growth rate. As Branch &
Marsh
(1978)
have
shown
that
tenacity is greater in some species
than in others and that this is linked in part to the morphology of the foot, some species may need to
expend less energy in muscular effort to maintain their grip on the rock. Wright (1978) describes how
the activity of Lottia gigantea declines as wave action intensifies, and considers this an energy saving
device rather than an attempt to avoid being washed away (Wright, pers. Comm.).
Interspecific differences in growth rate
Substantial differences exist between the growth rates of different limpets. Growth rates range from that
of Nacella concinna, growing a few millimetres a year and maturing sexually after about seven years and
living in excess of 30 years (Picken, 1980), to fast-growing species like Patella oculus which reaches 60-70
mm and is sexually mature after a year of growth, but rarely lives longer than three years (Branch,
1974b).
Actual growth rate is not a very useful comparative measure, because naturally we expect larger species
to grow faster on an absolute basis. If size at time t is plotted against size at t + 1 (the Ford-Walford
plot) the slope of the line (in) is used in the Von Bertalanffy growth equation in the form of the growth
coefficient, K. (See Balaparameswara Rao, 1976, for its application to growth of Cellana radiata.) K is
derived as follows: K = - loge111 and is a useful comparative index of growth that is not dependent on
body size.
Figure 31 shows that both intraspecifically and interspecifically there is a striking inverse correlation
between K and longevity. This is a relationship that has been pointed out several times, particularly in
comparisons of Patella vulgata from different habitats (Fiseher-Piette, 1948; Choquet, 1968; Lewis &
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
Bowman.
1975;
Thompson,
1979,
1980).
Sutherland (1970) showed that the relationship is
not invariable, for high-shore Collisella scabra grow
faster than low-shore individuals, yet they suffer a
lower mortality and live longer. Nevertheless,
studies on a large number of other species suggest
that this relationship is of general occurrence.
There are two ways of looking at this inverse
correlation between growth rate and longevity.
Some species have a low probability of survival
because of the nature of their environment. Choat
& Black (1979) have argued that Notoacmea insessa,
living on the brown alga Egregia, is very unlikely to
survive more than a year because its algal host
plant is essentially annual and likely to be torn free
even before the year is complete. They contrast this with the stable dependable rock substratum
occupied by Collisella digitalis, and show that less than 10% Notoacmea insessa survive more than four
months, while about 80% Collisella digitalis survive the same period. Choat & Black argue that the growth
patterns of the two species are adapted to this difference, Notoacmea insessa growing nearly twice as fast as
Collisella digitalis so that it grows rapidly to sexual maturity and can survive the instability of its habitat by
continual recruitment. The same argument applies to Helcion pellucidus on laminarians: it too grows very
rapidly to sexual maturity and in most cases probably dies within a year (Vahl, 1971).
Other species may be compelled by shortage of space to remain small, so that growth beyond sexual
reproduction is futile and an annual life span a more obvious adaptation. This may apply to epizoic
species living on other shells, such as Patelloida mimula and P. insignis (Creese, 1978) and Collisella asmi, all
of which are space-limited, live only to reproduce once, and are small in size. In these species high
growth is again desirable, and they have high growth coefficient (see Fig. 31).
The converse applies in situations where food may be predictably in short supply. Pieken (1980) sees the
very low growth rate, low metabolic rate, and delayed sexual maturity of Nacella concinna as adaptations to
the Antarctic where food availability is low for most of the year. The extremely high-shore Notoacmea
petterdi is also very slow-growing (Creese, 1980c). Similarly some of the territorial limpets, such as Lottia
gigantea (Wright, pers. comm.), Patella longicosta, and P. cochlear are comparatively slow-growing and rely on
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
a dependable but limited food source which they cannot overgraze if they are to avoid eliminating their
food supply. Thus for different reasons in different species it is possible to view each growth pattern as
an adaptation to particular circumstances.
A second approach to the correlation between growth and longevity is to deduce a cause and effect
condition: that is, the act of growing fast may in itself lead to a shortened life expectancy. There are
several ways this could happen. Rapid growth and early sexual maturity may exhaust reserves so that any
subsequent shortage of food cannot be tolerated. Rapid body growth may also reduce the amount of
energy devoted to defensive structures such as the shell, and hence increase the chances of death.
One basic question that has not been satisfactorily answered is whether the different species really do
have different growth patterns or ‘strategies’, or whether the differences we record are simply
phenotypic variations due to differences in food availability. Several species have very plastic growth
rates: perhaps best documented for Patella vulgata (see Thompson, 1980). In all the cases mentioned
above, the implicit assumption is made that each species does have a characteristic range of growth rates
which is adapted to each species’ habitat, but there is no proof that the limpets are not responding
directly to the conditions in that habitat.
A start has been made on experimentally testing whether each species is so variable and plastic as to
obscure the adaptive patterns described above. Using two extreme forms, the slow-growing P. cochlear
and the fast-growing P. oculus, I have manipulated densities to test how much food availability is
dictating the growth patterns of the two species. The results show that both species are plastic: P. cochlear
increasing its growth if more food is available while P. oculus decreases its growth when crowded. The
range of responses that each species is capable of is different and only overlaps to a small extent. P.
cochlear never approaches the fastest rates exhibited by P. oculus while the latter dies at well below the
densities tolerated by P. cochlear and seems unable to achieve the low turnover rates that are essential for
survival of P. cochlear. Thus, the indications are that although growth may be flexible, each species has a
characteristic and genetically determined range of growth responses. I would speculate that some species
such as P. vulgata are capable of a wide range of growth rates while others are more inflexible.
Energy diverted into shell growth
The energy content of the organic fraction of the shell has been calculated for several species (Parry,
1977; Branch, unpubl.). In all cases the energy content is less than 7% of the production, and less than
2% of the ingested energy. Figure 35 shows the energy devoted to the shell of P. longicosta in relation to
other segments of the budget. There may, however, be other costs to the shell. The formation of the
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
organic material must involve metabolic energy losses, and we cannot assume that the calcium carbonate
matrix is laid down cost-free.
If the growth coefficients from South Africa Patella spp. are plotted against the ratio of shell energycontent to somatic energy-content, there is a significant negative correlation (r = -0.82) (Branch &
Damstra, unpubl.). The fraction of energy devoted to the shell is too small to explain the differences in
growth rate, but it is interesting that the long-lived, slow-growing species should channel more energy
into a thicker defensive shell, which may in part explain why they manage to be long-lived.
Continued in Biology of Limpets part 2…
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380