Download The Biology of Limpets, part 2, Branch

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
…continued from Biology of Limpets part 1
REPRODUCTION
Methods of reproduction and larval development
Patellacean limpets have comparatively simple reproductive systems. The sexes are normally separate
and a large gonad underlies the gut and visceral mass, swelling in size during maturation and eventually
constituting up to half the body weight. Gametes pass via the right kidney to the right renal papilla
(Davis & Fleure, 1903; Fisher, 1904; Fretter & Graham, 1962; Walker, 1968).
The reproductive organs are a lot more complex in the Siphonariidae (see Hubendick, 1945, for a
detailed comparative study). All species of Siphonaria are hermaphroditic, and most are protandrous
although male and female phases are not separable (Marcus & Marcus, 1960). The ovotestis leads via a
short hermaphrodite duct to the common duct, via albumen and mucous glands. Fertilization is internal,
spermatophores being transmitted by the penis. As in other pulmonates, there is a bursa (spermatheca)
that receives the sperm, a flagellum that may break down the spermatophore, and a small seminal
receptacle in which fertilization is assumed to occur (Marcus & Marcus, 1960). Another siphonariid,
Kerguelenella, has a similar but simpler structure (Simpson, 1977).
All patellacean limpets have external fertilization, although there have been suggestions that males and
females of Helcion pellucidus, Patella caerulae (Ankel, 1936) and P. lusitanica (von Medem, 1945) came
together in pairs during spawning, and Nacella concinna is unique in that mature animals from temporary
“stacks” of two to six animals which last only for the duration of spawning (Picken, 1980). Most
Patellacea have free swimming trochophore and veliger stages the latter is planktotrophic in Patella
vulgata (Dodd, 1957) and Collisella testudinalis (Kessel, 1964), but Cellana tramoserica and four acmacids
examined by Anderson (1962, 1965a) proved to be lecithotrophic. Brooding of young has been recorded
in Arctic species, such as Acmaea rubella (Thorson, 1935) and in the genus Problacmea (Golikov &
Kussakin, 1972; Lindberg, 1979b), in which the young are retained in the nuccal cavity above the head
and mature there into crawling shelled individuals. This is in line with the general theory that species at
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
high latitudes tend to brood their young and to dispense with the dispersive larval stage. The usual
explanation of this is that planktonic food is available only for short periods and that low temperatures
slow development of the larva, prolonging its stay in the plankton. Some of the most successful highlatitude species have, however, a planktonic larva, including Nacella concinna (Picken, 1980).
Detailed descriptions of larval development in a number of patellaceans are available (Patten, 1886;
Smith, 1935; Dodd, 1957; Anderson, 1962, 1965a; Kessel, 1964; Balaparameswara Rao, 1975a), and
Crofts (1955) has described muscle morphogenesis in Patella vulgata larvae.
All siphonariids lay eggs embedded in mucous ribbons, which in almost all cases are attached to the
rock. In contrast to most pulmonates, some species have a planktotrophic veliger larva (Knox, 1955;
Anderson. 1965b; Fioroni, 1971; Mapstone, 1978), but others undergo complete development in the egg
mass and only emerge as crawling juveniles (Thorson, 1940), as is true for the Antarctic Kerguelenella spp.
(Knox. 1955; Simpson. 1977). Siphonaria virgulata is unique in forming a globular egg mass that is not
deposited on the rock face but is released into the water. Creese (1980a) suggests this relates to the highshore habitat of this species, and showed that if the benthic egg ribbons of S. denticulata are
experimentally transplanted up the shore to the zone occupied by S. virgulata, they suffer high mortality
due to desiccation. As fertilization is internal in siphonariids they aggregate temporarily for sperm
transfer (Abe, 1940; Olivier & Penchaszadeh. 1968; Creese. 1978).
Reproductive cycles
The annual cycle of gonad development has been recorded for a large number of limpets, including
detailed analyses of Patella vulgata and other British species (Evans, 1953; Orton, Southward & Dodd,
1956; Orton & Southward, 1961; Choquet, 1968; Blackmore, 1969a; Bowman & Lewis, 1977;
Thompson, 1979, 1980), several Australian patellids, acmaeids, and siphonariids (Underwood, 1974;
Parry, 1977; Creese, 1980a,b), seven South African Patella spp. (Branch, 1974a), a large number of North
American acmaeids (Fritebman, 1961a,b,c, 1962; Seapy, 1966; Sutherland, 1970), four Cellana spp.
(Balaparameswara Rao, 1973; Underwood, 1974; Kay & Magruder, 1977), and four Algerian Patella spp.
(Frankiel, 1975).
Most species have a single spawning each year, as typified by Patella vulgata. In an impressive analysis
covering six localities and periods of over four years, Orton et al. (1956) showed that this species was
sexually dormant in early summer (to the extent that most animals cannot be sexed), and that
development begins in about July and spawning occurs from October to March, being highest in
November. The timing of spawning was fairly consistent from year to year, and strikingly similar over a
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
wide range of latitudes in Britain, although the start of maturation occurred earlier in colder localities.
Spawning is normally remarkably synchronized, and Ballantine (1965) showed that 80%, of the
population may spawn over a two-day period. While all patellids seem to have marked annual cycles
several acmaeids have scarcely any change in their gonad, suggesting that they spawn almost continually
or at least for prolonged periods and without any obvious synchronization within the population
(Creese, 1980b).
Fritchman’s (1962) observations on a large number of North American aemaeids revealed a relationship
between the time of spawning and the geographic distribution of the species. Northern cold-water
species bred in winter, while their southern counterparts bred in spring or summer. A similar
relationship exists in South African Patella spp. (Branch, 1974a). In South Africa this may have some
significance in limiting the penetration of warm water species around the Cape of Good Hope and onto
the cold-water west coast, since their spawning occurs at a time when differences between the water
temperatures of the warm and cold coasts are at their greatest.
Temperature has often been suggested as a cue for spawning, but this cannot be assumed solely from
field data, since if temperature fluctuates annually it is almost inevitable that spawning can be associated
with a change in temperature - either a rise or a fall! Nevertheless spawning of Nacella concinna is closely
linked to the spring rise of temperature, occurring about three weeks after sea temperatures exceed –
l.4oC (Picken, 1980). In this case seasonal changes of temperature provide a reliable cue and furthermore
are linked with increased light intensities and increased phytoplankton on which the limpet’s larvae feed,
and Shabica (1971) has shown experimentally that only after three weeks of warming can fertilization be
achieved. Shabica also suggests that release of eggs by the female may initiate spawning by the male.
In an analysis of several prosobranchs, including Patella peroni and Cellana tramoserica, Underwood (1974)
could find no correlation of the time of spawning with geographic distribution, nor with phylogeny or
zonation; but he did find that species with planktotrophic larvae spawned just prior to the time when
plankton was maximal (hence ensuring food for the larvae), at a time of rising or high sea surface
temperatures. Species with lecithotrophic larvae had no need to coincide with plankton blooms, and
bred at different times of the year; and in Patella peroni, at very different times in successive years.
Orton et al. (1956) suggest that while the development of the gonad in P. vulgata is probably linked to
temperature, the act of spawning is triggered by violent on-shore storms. Subsequent workers
(Ballantine, 1965; Bowman & Lewis, 1977; Thompson, 1980) have tended to support this suggestion.
Gravid P. vulgata are so turgid with gametes that it is easy to imagine a violent storm triggering release of
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
the gametes. Two advantages may accrue as a result. Storms keep the shore damp, hence reducing
desiccation of newly settled limpets; and onshore winds may prevent the larvae from being washed out
to sea. Bowman & Lewis (1977), however, could find no correlation between success of recruitment and
wind direction. Spawning of Notoacmea peterdi occurs when storms are frequent. As this limpet lives on
the extreme high shore it may depend on these storms to allow larvae to reach this zone when they
settle (Creese. 1980c).
Bacci & Sella (1970) have asked whether differences in the breeding season of coexistent species may
achieve reproductive isolation, but show that for Patella coerulea and P. aspera there is too much overlap in
their timing to isolate the two. Most of the South African patellids that coexist have almost identical
spawning periods, so that reproductive isolation cannot be one of the objects of the annual cycle and its
timing.
Several species of Siphonaria show a striking rhythmicity to their egg-laying (Abe, 1940; Mapstone. 1978;
Parry, 1977, Creese, 1978, 1980a), maximum numbers of egg ribbons being deposited about 4-5 days
after spring tides. As the larvae are released about 6 days after egg deposition, their emergence is just
prior to the following spring tide.
Age of sexual maturity, sex ratios and sex change
Considerable differences exist in the age at which different species become sexually mature which, as
expected, parallel the differences in growth rate discussed above. Species such as Notoacmea insessa,
Helcion pellucidus, and Collisella asmi, which are essentially annual, mature in a few months, but seldom
survive to reproduce again Vahl, 1971; Choat & Black, 1979). A larger number of limpets mature during
their first or second year and live about five years increasing in fecundity each year due to an increase in
body size (Blackmore, 1969a; Creese, 1978, 1980a,b, 1981 Dixon, 1978). At the other end of the scale,
Patella longicosta matures after two years. P. cochlear after 3-7 years (Branch, 1974a), and Nacella concinna
after only eight years (Picken, 1980). The age of maturity thus correlates closely with longevity (r = 0.87
for l4 species), and inversely with the growth coefficients (r = -0.72 for the same species).
In P. cochlear, age of maturation is also inversely correlated with growth rate, which in turn is largely
influenced by intraspecific competition (Branch, 1974a, 1975b). Thorson (1965) records an interesting
phenomenon in the limpet-like Capulus ungaricus. Normally it lives on bivalves, stealing food by inserting
its proboscis into the bivalve’s mantle cavity, but forms are often found on the gastropod Turritella.
These latter forms never develop their normal adult features, but still mature sexually. Thorson suggests
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
this neoteny is ecologically determined by the restrictively small host shell, and energy diverted into
reproduction rather than further growth.
As a special case of sexual development, a number of
limpets may be consecutive hermaphrodites, almost all
being protandrous (male first, then female). Orton (1920,
1928a) first suggested that this is the case for Patella vulgata
in view of the preponderance of males in the smaller size
classes and females in the larger size classes, and later more
detailed work confirms this (Das & Seshappa, 1948; Orton
et al., 1956; Dodd, 1956; Blackmore, 1969a; Thompson,
1980). For similar reasons, other species may be protandric
hermaphrodites, including Acmaea fragilis (Wilcox, 1898),
Patella coerulea (Bacci, 1947a,b; Pellegrini, 1948), Lottia
gigantea (W. G. Wright, pers. comm.), Notoacmea petterdi
(Creese, 1978), and Patella aspera (Thompson, 1979). In
some of these cases the only reason for suggesting
protandry is the change of sex ratio with age (Fig. 32).
There are other explanations for this effect: females may grow faster than males; or males may suffer a
higher mortality rate. In P. oculus the case for protrandry is probably stronger, for the species rarely lives
longer than two years and all juveniles are neuter for about six months, then become male in their first
year, and female in their second year. There is no overlap between the sizes of neuter and female
animals. After spawning, males can histologically be shown to develop oocytes which enlarge and
replace the remnants of the sperm, during which phase the limpets have been termed transitional
hermaphrodites (Branch, 1974a). In this species the case for protrandry seems secure.
Individuals that appear to be functionally male and female simultaneously have been recorded in a
number of species, including all three British Patella spp. (Dodd, 1956), P. oculus (Branch, 1974a), and
Cellana radiata (Ganapati & Balaparameswara Rao, 1967), and are considered to be unrelated to a change
of sex.
In an elegant series of experiments Choquet (1965, 1967, 1971; and see Streiff, 1971, for a summary) has
revealed how sex change in P. vulgata is controlled. Choquet & Lemaire (1969) histologically demonstrate
neurosecretory cells in the cerebral ganglion and nerve terminals in the tentacles, also suspected of being
neurosecretory. In addition, there is a juxta-ganglionar organ that lies above the cerebral ganglion and is
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
apparently endocrinal, regressing during sexual inactivity (Martoja, 1965, 1972; Choquet & Lemaire,
1969).
By culturing undifferentiated germinal tissue in the presence or absence of the suspected neurosecretory
organs, Choquet established that the cerebral ganglion
stimulates mitogenesis. In its absence, gametogenesis
ceases. In addition there is an inhibitory factor released
by the tentacles which suppresses spermatogenesis
during the resting phase. A vitellogenic factor from the
cerebral ganglion is necessary for oogenesis to be
completed (Fig. 33). Most pulmonates (including
Siphonaria) have an endocrine gland embedded in the
cerebral ganglion, but its function is unknown (Van Mol.,
1967).
The adaptive significance of protandry in limpets is still not known. If the female gains more in
fecundity with an increase in size than the male does, then it will pay to be male first and then female. It
is difficult to see, however, why this should be the case in patellacean limpets which practise external
fertilization; both sexes stand to gain in fertility with an increase in size. Possibly there is a threshold of
size below which it is uneconomical to produce the energetically more expensive eggs in comparison
with sperm, but some very small species of limpets seem capable of egg production. Branch (1974a) did
find that males predominated in populations of those species in which intraspecific competition is
greatest. Another suggestion is that as each animal produces many more sperms than eggs, there may be
an overabundance of sperm. Under these conditions a female will benefit greatly from an increase in
body size and hence egg production, but a male will benefit proportionally less.
Again the problem is to explain why some species show no hint of protandry. An examination of seven
Patella species revealed no tendency for protandry to be more developed in species which live at high
densities and presumably would be more likely to suffer from an over-abundance of sperm, because
fertilization would be more certain (Branch, 1974a). W. G. Wright (pers. comm.) has tested for
protandry in Lottia gigantea by removing all animals above a certain size (the size at which females
appear) and then examining the population 10 months later to see if any of the remaining animals had
developed into females. As only 1 out of 27 animals had become female at this stage, sex change seems
unlikely. On the other hand, he could find no evidence of differential growth rates or mortalities
between the sexes, that could explain the predomination of males in small animals and females in the
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
larger size groups. Wright hypothesises that sex change does occur in L. gigantea and that it may be
linked with the attainment of a dependable and sufficient food source in the form of a territorial grazing
area, so that the energetically expensive egg production can be based on a secure source of food.
In species like Crepidula fornicata, with internal fertilization and brooding of eggs, the advantage of
protandry is more obvious. A small male can adequately fertilize all the females within reach, while a
female needs to be larger to produce and brood sufficient eggs to justify being female. Sex change in this
genus has been studied in detail by Coe and Gould (see Coe, 1953, and Gould. 1952, for their most
recent work and other references). Hoagland (1978) has compared several species of Crepidula and
shown that species with plankton larvae suffer from an unpredictable recruitment. They are
consequently gregarious and avoid competition for space by stacking one on top of another. Newly
settled individuals are male first and when large enough they transform into females. The size at which
transformation occurs is controlled partly by the presence of other animals; a high proportion of females
retards transformation. Thus sex change is also beneficial in regulating sex ratios. Hoagland contrasts
this with species which brood their young and lack a planktonic larva. Recruitment is thus predictable,
and in these species transformation is genetically fixed (presumably at an optimal size).
The large number of patellacean limpets which have biased sex ratios with females dominant in larger
size groups (e.g. see Fig. 32) suggests protandry may be more common than at present realized. An
analysis of seven Patella spp. has shown that in six, oocytes can be found in the testis immediately after
spawning (G. M. Branch, unpubl.). At the least this suggests sex determination in limpets is very labile,
and the potential for sex change may exist in all or many limpets. In P. cochlear the proportion of females
in the population declines as density rises, and the dominance of large size classes by females diminishes
(G. M. Branch & V. Stuart, unpubl.). Choat’s (1977) experimental analysis of density effects showed the
reverse for Collisella digitalis; the proportion of males dropped from 0.55 in low density sites to 0.22 in
high density sites.
It is tempting to suggest that sex is partly determined by environmental conditions, but the data available
are circumstantial. Wright & Lindberg (1979) have devised a simple method that will allow more critical
testing of these ideas; they have used a syringe to suck small quantities of gonad out of limpets without
killing the animal. This method will allow sampling of the same animal at various time intervals, and a
direct test of sex change and its possible relationship with environmental conditions.
Energy budget studies of reproduction
The ‘cost’ of reproduction has always been difficult to measure but is perhaps easier to assess in limpets
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
which are comparatively simple and generally lack complicating features such as parental care. I have
used the ratio of gamete output to flesh weight as an index (Branch, 1974a, 1975c) but a more realistic
measure is the proportion of annual energy intake (or production) devoted to reproduction (Parry,
1977). Figure 35 (p. 316) shows in Patella longicosta, for example, that up to the age of two years, no
energy is used in reproduction, but thereafter up to 10.8% of the energy ingested and 62.5 % of the
production (Pr + Pg + Pmuc) is channelled into reproduction.
Parry (1977) has adopted a different approach, measuring the energy content of reproductive output in
relation to the total energy flow through the limpet population. As a percentage of production (Pr + Pg :
Parry did not measure mucus production) Cellana tramoserica devoted 72.6%, to reproduction, Patelloida
alticostata 63%, Siphonaria diemenensis between 43 and 83%, Notoacmea petterdi 74%, and Patella peroni 75.5%.
When the energy devoted to reproduction is recalculated as a fraction of assimilated (= absorbed)
energy (A) (i.e. reproductive effort, Pr/A) the values for the five species become, respectively, l2.0%,
l0.3%, 5.7 - l4.3%, 8.5% and 19.7%. The last two values must be used with caution as Parry estimated
the respiratory rates of the last two species from the rates of other limpets and may have introduced
substantial errors into these two calculations of reproductive effort. Hughes (1971) calculates values of
10.4% and 2.8% for Pr/(Pr + Pg) and for Pr/A respectively, in Fissurella barbadensis: values much smaller
than those of Parry.
Sutherland (1972) analysed energy flow through high and low-shore populations of Collisella scabra.
Previously he found that the high-shore population had a low density, better survival and higher growth
(Sutherland. 1970). His energy budget study was to assess whether energy flow was greater in the centre
of the species range, lower on the shore. At the high-shore site, spawning occurred once a year and the
regression of the gonads could be used to measure the energy content of reproductive output, which
varied substantially in successive years, from 10 to 68 kcal.m-2.yr-1. At the low-shore site a more constant
output of 22 to 26 kcal.m-2.yr-1was recorded. The net sum of the energy budget showed that energy flow
was fairly similar in the two zones, in spite of the fact that potential production of microalgae is greater
lower on the shore.
Sutherland (1972) questions why C. scabra does not migrate up the shore like C. digitalis. As the latter
clearly benefits from this migration, growing faster if it migrates, why does C. scabra remain at one
position? Sutherland suggests that C. scabra depends more on its home scar (presumably because it lives
on horizontal surfaces and is more susceptible to desiccation), and that there is no clear reproduction
advantage to be gained by migrating upshore as there is, on average, an equal flow of energy through
both populations in terms of reproductive output. This latter argument is incorrect, for although the
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
flow through the population is the same, there are fewer high-shore animals, so the output per
individual will actually be much greater. Since reproductive output is probably equivalent to fitness it
would seem that the high-shore limpets are reproductively at an advantage.
Giesel (1976) refers to Sutherland’s data, and points out that the patterns of reproduction in the two
populations accord with ecological theory: animals living in an environment that is only occasionally
suitable for reproduction should devote more energy to reproduction during those few suitable
occasions (as the high-shore C. scabra do, once a year) but also withhold this if conditions are poor
(hence the year to year difference in high-shore C. scabra). Low-shore populations have a more constant
food supply and environment and should in theory spawn more continuously but at a lower level at any
given time (which they do). Notoacmea petterdi occurs in the extreme high-shore, and it too has a high
reproductive output, synchronized to suitable conditions (Creese, 1980b).
Reproductive effort differs between species and the optimal reproductive effort should be determined
by natural selection. While it might be expected that the maximum amount of energy be devoted to
reproduction, if food is limited, this is only possible at the expense of other functions such as growth.
Consequently reproduction may carry some cost. As an example, Creese (1981) showed that growth of
N. petterdi all but ceases during gondal maturation. Thus, it may pay to invest less in reproduction at any
one given time if this increases the adult’s chances of survival or increases its growth (and hence,
subsequent fecundity).
Choat & Black (1979) have contrasted the reproductive patterns of N. insessa and Collisella digitalis. The
former inhabits the alga Egregia, which is an annual, and consequently the limpets have a low life
expectancy. This being so, a high reproductive effort can be anticipated in Notoacmea insessa. It matures at
a very small size, and its reproductive output is about 64% of its somatic body weight. It contrast,
Collisella digitalis inhabits rocks and consequently has a higher life expectancy. It matures at a shell length
of about 12 mm (twice the size in Notoacmea insessa) and its reproductive output is only 36% of its
somatic body weight.
Branch (1974a, 1975b,c) has compared the reproductive output of several Patella spp.; it ranged from 9
to 92% of the somatic weight in different species. In general the mid- to high-shore species, which
migrate progressively up the shore as they age, have very high reproductive outputs while the more
specialized or territorial species, living in the lower shore and subtidally, have much lower reproductive
outputs. It is speculated that high-shore migrant species, because they have lower life expectancies
(Branch, 1974b) should have higher reproductive efforts while the lower-shore species have a greater
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
longevity and may also suffer more from competition, thus making it more important to channel energy
into growth.
As limpets get larger and older there is probably less need to devote energy to body growth and,
furthermore, the changes of survival to the subsequent year also diminish. We, therefore, might
anticipate an increase in reproductive effort with age. Figure 35 (p 316) shows for P. longicosta that Pr/(Pr
+ Pg) does increase markedly in older animals.
Two major theories have been put forward to explain the patterns of life history (see Stearns, 1976, for a
review.) According to the r-K theory species occupying unstable environments will often have the
opportunity to recolonize their habitat (indeed they may depend on recolonization for their existence)
and will benefit most from a large investment in reproduction. Continued survival of the adult is unlikely
and recruitment of subsequent generations of greatest importance. Notoacmea insessa, discussed above,
exemplifies this situation. A second theory, ‘bet-hedging’, suggests that if adult mortality is low in
comparison with juvenile mortality, it will be preferable to devote less to reproduction at any one given
time, improving adult survival and the chances of repeated breeding, and not risking a single substantial
reproductive output that might fail totally. Conversely, if adult mortality is high relative to that of
juveniles, then the bet-hedging predicts the same outcome as the r-K theory; high reproductive effort is
the best option if the adult is in any case unlikely to survive long enough to reproduce again.
Existing data on limpets do not allow us to favour either theory above the other. While it is true that
species with high reproductive outputs such as Patelloida insignis, P. mimula (Creese, 1978), Notoacmea
insessa (Choat & Black, 1979), Patella granatina, and P. granularis (Branch, 1974b) have a low adult survival
relative to that of juveniles, they also live in unstable or short-lived habitats or habitats that limit adult
size. Thus both theories can be supported, but for different reasons.
Parry (1977) has discussed how it is necessary to distinguish sources of mortality when considering
reproductive patterns. Adults that are killed by external factors such as desiccation (extrinsic factors)
should have a high reproductive output. If, however, mortality is linked to the act of reproduction
(intrinsic) then it may be preferable to reduce reproductive effort to increase the chances of survival.
Separating intrinsic from extrinsic mortality and quantifying their relative importance is a formidable
task, so far only attempted by Parry (1977). He determined the energy budgets of four patellacean
limpets and attempted to measure the causes of mortality. In the low-shore P. peroni and Patelloida
alticostata predation by parrot fish was high, and food availability always high. Parry concluded that these
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
species were limited by predation and that reproduction did not contribute to this mortality. Extrinsic
factors thus accounted for most mortality.
Sources of mortality in Notoacmea petterdi could not be determined (although Creese, 1980c, records
mortality that was probably related to desiccation). Living in the extreme high-shore, N. petterdi has no
known predators, and its mortality seems unrelated to reproduction (Parry, 1977). In contrast, the midshore Cellana tramoserica alternates between periods of food abundance and extreme shortage, as
indicated by its declining body weight and energy content during the summer ‘die-back’ of algae. C.
tramoserica is preyed on by parrot fish and by oystercatchers, but the recorded rates of predation suggest
only 52-61% of all the limpets (and l3-22% of adults) suffer this death. Parry considers that the rest die
of starvation. As reproduction precedes the period when starvation is most likely, Parry suggests
reproduction contributes to death because it prevents the limpets from building up the reserves
necessary for the summer.
Parry (1977) plotted reproductive effort (Pr/A) against
adult mortality rate and found a poor correlation (Fig.
34A); but when he estimated the extrinsic rate of
mortality, this was more closely correlated (r = 0.88)
with reproductive effort (Fig. 34B). Thus the expected
correlation
between
adult
mortality
rate
and
reproductive effort is only realized when the act of
reproduction does not itself contribute to mortality.
When it does, then reproductive effort should be lower
than ‘expected’, as in C. tramoserica.
As with all other components of the energy budget, we
need to be cautious about ascribing a fixed reproductive
pattern to each species, for a variable amount of
flexibility will exist. The differences between high- and
low-shore C. scabra demonstrate this. Segal (1956a,b) also showed that high-shore C. limatula have
smaller gonads than low-shore animals, and that transplants from high- to low-shore resulted in an
increase in gonad size while the reverse transplant decreased gonad size. One of the challenges of future
research will be to determine how much the behaviour of different species is species-specific and how
much it simply reflects environmental conditions.
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
THE ENERGY BUDGET
Energy balance
The energy budget outlined above comprises production (P), which consists of elements that are
essentially ‘useful’ to the animal (Pr, Pg, and Pmuc) and a series of elements whereby energy is lost to the
animal (F, U, and R). To maintain itself in the long run, consumption (Q must exceed these latter
elements. In the short-term an animal can draw on its body reserves if there is a short-fall between C
and energy losses, but for growth and reproduction to occur, intake must be greater than losses.
Practically complete energy budgets are available for a number
of limpets (Hughes, 1971; Sutherland, 1972; Parry, 1977),
although in all cases consumption has been calculated as the
sum of Pg+Pr+R+F. Excretion (U) has always been ignored,
which seems justifiable in limpets, but the omission of
secretions (mucus) may be more serious. Figure 35 summarizes
the components of the energy budget for Patella longicosta of
different ages. It is obvious that respiratory losses account for
the largest part of the budget: about 68% in mature animals.
Faecal losses account for about 13.5%. The remaining 18.5 %
constitutes production, of which the largest fraction is devoted
to reproduction in large mature animals, a substantial portion
to mucus, and only a small amount to body growth. Shell
growth is a tiny drain on energy. Hughes (1971) found faecal losses to be far higher in Fissurella
barbadensis but also agrees that metabolic heat losses far outweigh the energy diverted into production.
Parry’s (1977) work on Cellana tramoserica and Patelloida alticostata also shows that respiration accounts for
about 83%, of assimilated energy (i.e. P+R).
Modification of components of the energy budget
Using a filter-feeding animal, Crepidula fornicata, Newell & Kofoed (1977a, b) were able to measure the
rate of consumption of suspended microalgae and to compare this with metabolic energy losses by
simultaneously measuring oxygen consumption. They first showed that in animals held at 10oC,
respiration rose steeply between 10oC and 27.5oC, while filtration rate rose between 5oC and 15oC but
then declined rapidly and progressively at higher temperatures. The result was that the cost of activity
(the ratio of oxygen consumption to filtration rate) increased greatly at higher temperatures (Newell &
Kofoed, 1977a), so that the slipper-limpets operated less economically at higher temperatures.
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
Further analysis showed, however, that both the metabolic rate and the filtration rate are modified by
acclimation to different temperatures. Acclimation to higher temperatures shifts the curve relating
oxygen consumption to temperature, moving it laterally to the right (lateral translation) (Fig. 36A) and
thus metabolism actually remains fairly constant. When measurements are made at the temperatures to
which animals have been acclimated (Fig. 36B). The curve relating filtration rate to temperature is also
altered by acclimation; it too is shifted to the right and, furthermore, the peak of the curve (which is at a
temperature about 5oC higher than the acclimation temperature) increases in height (Fig. 36C). The
consequence is that if filtration is measured at the temperature of acclimation, it rises with temperature
(Fig. 36D). The ratio of water filtered: oxygen consumed is an index of efficiency and Figure 36E clearly
shows that provided C. fornicata is allowed time to acclimate, it performs more efficiently at 20-25oC.
This is due to two compensatory changes that occur with acclimation: translation of both the metabolic
and the filtration rate-temperature curves. Knowing the rate of filtration, one can calculate the minimum
ration of food (as a concentration of carbon present in the water) that will maintain the animal; as
efficiency increases with temperature, so the minimum ration declines (Fig. 36F). Effectively this means
that more energy can be diverted into growth and reproduction.
Comparable data are not available for grazing limpets because of the difficulty of quantifying ingestion,
but it is tempting to suggest that similar principles may dictate seasonal patterns of growth and
reproduction.
Pechenik (1980) has applied the same principles to test whether the “delay period” that planktonic larvae
may have prior to settling is determined by entering into a phase of zero growth in which energy
demands are balanced against intake. He finds that food intake in C. fornicata larvae is linearly related to
size until the period when larvae become competent to metamorphose, when intake declines.
Metabolism increases with size. Even when the larvae enter the delay period when they are postponing
metamorphosis, they still continue to grow (i.e. intake must exceed energy requirements). Pechenik
suggests that the duration of the delay period is related to the rate at which energy is accumulated. The
more efficient the retention of energy, the quicker the development and the shorter the delay possible.
He proposes that species such as C. fornicata, which has a variety of substrata on which it can settle, will
have a short delay, as they can easily find a suitable substratum. Species with specialized adult habitats
may need a long delay period to allow larvae to locate the right substratum. This is an interesting
hypothesis, for it allows that inefficient retention of energy may be of selective advantage.
Each of the components of the energy budget can be adjusted. Of these, respiration is the most
important since it results in a substantial loss to the organism. The level of respiration differs between
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
species, some having conspicuously low rates such as Nacella concinna and Patella granularis (Ralph &
Maxwell, 1977; Branch & Newell, 1978), while others such as P. compressa and P. oculus have rates sevenfold greater (Branch & Newell, 1978; G. M. Branch & P. Bouchers, unpubl.). The dependency of
respiration on temperature also affects metabolic energy losses; a low Q10 can maintain a low respiration
rate in the face of rising temperatures, as for example, in some high-shore species like P. granularis,
Collisella digitalis, and C. scabra (Baldwin, 1968). In Patella vulgata this temperature independence operates
over the normal temperature range (Davies, 1966). On the other hand, low Q10 values can maintain a
high metabolic rate in the face of declining temperatures, as I have suggested for P. granatina (Branch,
1979a); other species such as P. oculus have very high Q10 values, increasing metabolism greatly as
temperature rises. A third factor influencing metabolic energy losses is the modification of respiration
rate by exposure to air or water. Here we can contrast P. granularis and P. granatina. Both migrate up the
shore, but P. granularis maintains a low rate of respiration because small animals respire faster in air than
in water (despite living low on the shore) while larger animals, living high on the shore, respire faster in
water. The reverse applies to P. granatina which thus keeps its oxygen consumption as high as possible.
Finally, respiratory energy losses can be influenced by the duration and time of activity rhythms, and
possibly by endogenous respiratory rhythms.
Both growth (Pg) and reproduction (Pr) vary greatly among and within species. While there are cases
where growth seems to be reduced to allow reproduction (see above), in general there is a strong
positive correlation between Pg and Pr. The growth rates of seven South African Patella species are
positively correlated (r = 0.89) with their reproductive effort (Pr/(Pr+Pg)). This implies that although
energy may be diverted from Pg to Pr (or vice versa) when food is short, in general, species have
‘strategies’ of high or low turnover. This is reflected in the negative correlation between production
biomass ratios and longevity, described by Robertson (1979) and updated by the addition of several
limpet species in Figure 37. This is an important generalization, for it allows prediction of production if
the longevity and biomass of a species is known. It also emphasizes that high turnover rates are linked
with low longevity, although as discussed above, we are not in a position to say which is the cause and
which is the effect (assuming the two are causally linked).
The amount of mucus produced by different species also seems to differ, and those species producing
large amounts are the fast-growing species with a high reproductive output, while species with a low
turnover produce little mucus. This can be seen in the same light as metabolic costs: species needing to
conserve energy produce little mucus, while those with high growth and reproductive output may need
more mucus for locomotion, and will need to move further to obtain sufficient food (Branch & Marsh,
1978).
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
Faecal production is also high in species with a high production (see Fig. 23, p. 285), as one would
expect from the higher food intake necessary to sustain high growth and gamete production. Estimates
of absorption efficiency also show a decline in efficiency in species with a high turnover (see above).
Beppu’s (1968) data show that digestive enzymes of high-shore limpets are less affected by starvation
than those of low-shore animals, and he suggests that this is because clearance time through the gut of
high-shore animals is lower (and presumably absorption efficiency higher).
Conservation versus exploitation
The rates of production exhibited by different species range widely, and we can recognize that some
species that are consistently short of food may need to
conserve their energy resources by efficient absorption
(and hence a lowering of faecal losses)2 reduction of
metabolic heat losses by various devices described
above, and reduction of mucus output. This requires
that the animals have a pattern of slow growth and low
reproductive output. Branch & Newell (1978) and
Newell & Branch (1980) have coined the term
“conservers” to describe such species. Species such as
Nacella concinna epitomize this condition (Ralph &
Maxwell, 1977; Picken, 1980). Conversely there are
“exploiters” with a very high growth rate and a high reproductive effort, which are seemingly profligate
in their use of energy, having very high metabolic rates, low absorption efficiencies with consequently
high faecal losses of energy, and a high mucus production. Conservers are usually faced with a food
shortage and their conservationist adaptations are of obvious value: but why should exploiters be
apparently wasteful of energy? All known exploiters seem to have an abundance of food, as for example
in the case for limpets living on host plants, which have a very high production and reproductive effort
(and a correspondingly short life) (Vahl, 1972; Choat & Black, 1979).
In a simple model relating feeding rates and rates of production to food availability, it has been
suggested that if food is abundant, a rapid intake of food is the best policy, even if this results in an
inefficient use of energy. If the absolute amount of energy channelled into reproduction is increased in
the process, the animal is better adapted, even although it is ‘wasting’ energy to achieve this end. Thus
high, inefficient, turnover is associated with abundance of food (Branch, Newell & Brown, 1979). When
food is short, the costs of attaining higher quantities of food may, however, exceed the gains, and a
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
pattern of lower intake can be more profitable. This brings with it a lower growth and reproductive
effort, and makes it important to conserve energy.
The conserver-exploiter hypothesis draws together some other approaches. The distinctions between
rand K-selected species (Stearns, 1976) and between energy maximizers and time minimizers (Schoener,
1971) have obvious parallels with the present hypothesis.
While it is convenient to polarize these two patterns of exploitation and conservation, obviously
intermediate conditions exist. More important, we still need to determine how much these patterns are
genetically fixed and how much they are simply reflections of prevailing environmental conditions
(particularly food availability). At present it seems that each species has a degree of flexibility in
responding to conditions. Some species may be very adaptable, moving between conservation and
exploitation as circumstances demand. Others seem relatively constrained to a particular pattern, as
suggested by the growth-rate experiments on Patella cochlear and P. oculus, described above (p. 304). One
of the challenges that must face us relating to reproductive and growth behaviour is to unravel the
genetic and environmental components of such behaviour and to determine whether the range of
flexibility each species has, is itself adaptive and genetically fixed.
INTERACTIONS BETWEEN LIMPETS AND OTHER ORGANISMS
PREDATORS
Predator species
A wide range of organisms has been recorded preying on limpets. Starfish rank high in importance
(Bullock, 1953; Feder, 1959, 1963; Margolin, 1964b; Menge, 1974; Simpson, 1976; Dayton, Rosenthal,
Mahen & Antezana, 1977; Branch, 1978). Flatworms also eat acmaeids (Dixon, 1978; Phillips &
Chiarappa, 1980) although Frank (1965a) suggested that this only happens when the limpets are
weakened by desiccation. Similar predation on weakened animals, by the isopod Exosphaeroma gigas, is
recorded by Simpson (1976). Crayfish (Engle, 1979, cited by Wells, 1980) and crabs also eat limpets, and
Chapin (1968) has shown the chelipeds of Pachygrapsus easily capable of crushing acmaeid shells, which
usually fracture at the weakened edges of the muscle-scar. A large number of predatory gastropods,
particularly thaids, which can drill through shells, feed on limpets (Marcus & Marcus, 1960; Walker,
1972; Menge, 1973; Kay & Magruder, 1977; Branch, 1978). Menge (1973) has suggested that Thais
armigera is responsible for the small size of Siphonaria normalis in intertidal pools, for in dry areas where
the thaid can forage less easily S. normalis is larger. Black (1978) has studied the tactics of Dicathais aegrota
preying on Patelloida alticostata. The whelk accounts for about 41% of the deaths of this limpet, its drillReference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
holes are not directed at the thinnest areas of the shell but predominate on the regions covering the
energy-rich gonad and digestive gland, and in positions allowing the whelk to fit more closely onto the
limpet’s shell, thereby reducing the chance of dislodgement. Octopus may also be an important predator
(Wells, 1980). With the exception of the octopus, all these invertebrates are comparatively slow-moving
predators, probably depending on chance encounter or chemical detection of prey. They contrast with
the fast-moving visual hunting vertebrates such as fish, birds, and mammals.
Several birds are recorded as predators, the most important being gulls. Larus spp. and oystercatchers
Haematopus spp., but terns, Sterna spp., turnstones Arenaria spp. and sheathbills, Chionus alba, also eat
limpets (A, R, Test, 1945; Giesel, 1970; Shabica, 1971; Walker, 1972; Branch, 1978). Feare (1971)
analysed the incidence with which the European oystercatcher (Haematopus ostralegus) attacked different
sectors of the shell and found the front end was attacked 80%, of the time. Hockey (1980) found the
South African H. moquini more often attacked the back of the shell. Feare suggested the front of the
limpet would be less strongly attacked because of the horse shoe shaped arrangement of the shell
muscle; while Hockey proposes that the larger South African limpets may need to be attacked from
behind, with minimal warning so that the limpet has no chance to clamp down. G. M. Puttick (pers.
comm.) estimates that H. moquini eat about 12 limpets per hour. Harris (1965) compared the size range
of Patella spp. eaten by Larus spp. and Haematopus ostralegus; the former eats only small limpets (5-35 mm
shell length) and the latter larger limpets (15-55 mm); there is only about 12% overlap in the size
composition of their diets and hence little competition.
An array of fish feed on limpets (Shabica, 1971; Walker, 1972; Parry. 1977; Paine & Palmer, 1978; Choat
& Black, 1979; Cook, 1980). Chorisochismus dentex specializes on a diet of limpets although small
specimens cannot eat limpets and large individuals may include echinoids in their diet (Stobbs, 1980).
This giant sucker-fish waits until limpets are moving and then wrenches them off the rock with its
enlarged canines. The limpets are swallowed whole and the largest limpet shell found in the sucker-fish
was a 90-mm Patella oculus in a fish 210 mm long! Helcion pectunculus is the most important prey, and
patellids collectively make up 74% of the diet. Interestingly, Siphonaria spp. are almost completely
excluded from the diet, despite being abundant and easy to detach. Possibly the thick mucus they exude
is noxious.
Only Parry (1977) has tried to quantify the amount of limpet mortality due to bird and fish predation.
Sooty oystercatchers (Haematopus fuliginosus) account for about 39% of Cellana tramoserica deaths, and
parrot fish (Pseudolabrus spp.) for 13 to 23% in Cellana tramoserica, 53 to 71 % in Patelloida alticostata, and
98% in Patella peroni.
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
Mice attack limpets at times (Frank, 1965a; Dixon, 1978) but possibly only when the limpets are stressed
by desiccation. Feral island rats eat small molluscs including P. granularis (Branch, 1978). Baboons (Papio
ursinus) can pull healthy limpets off the rocks and eat them (Hall, 1962). Human consumption can have
substantial effects on limpets populations (Branch, 1975d) and limpets are commercially exploited in
some parts of the world (Kay & Magruder, 1977) although de Villiers (1976) assessed stocks on the west
coast of South Africa and concluded that even these rich limpet grounds would not sustain exploitation.
Records from middens show that prehistoric man reduced the mean and maximum size of limpets quite
considerably in certain localities (Speed, 1969; Parkington, 1977).
Defences against predators
Many species of acmaeid and patellid limpets (but so far no siphonariids) have a “running” response,
usually preceded by a “mushrooming” in which the pallial tentacles are extended and the shell lifted high
off the substratum. Rapid movement away from the predator follows this mushrooming (Bullock, 1953;
Clark, 1958; Margolin, l964b; a review by Ansell, 1969: Mackie, 1972; Dayton et al., 1977; Branch, 1978).
A more specialized response is the mantle reaction of Diodora aperta (Margolin, 1964a) in which the
mantle is extended, then folded back on to the external surface of the shell and slid upwards to
completely cover the shell. The mucus-covered surface thus presented seems difficult for starfish to
grip. The same mantle response occurs in all Cellana spp. that have been tested (Branch, 1978; Creese,
1978; and pers. obs. on 12 species), and in Collisella strongiana (Yensen 1976). Branch & Branch (1980)
have described the structure of the mantle in Cellana tramoserica in relation to this behaviour. The mantle
has an extensive haemocoel, allowing great hydrostatic expansion, and a peripheral sphincter-like muscle
that we surmise acts like a drawstring, pulling the mantle up to cover the shell. The mantle is also richly
supplied with mucus-secreting cells, the secretion of which seems repulsive to gastropod predators.
An offensive function has also been ascribed to the often elaborate gland found in the mantles of
Patelloida virginea, Siphonaria sp. (Fretter & Graham 1954), Crepidula sp., and Calyptraea sp. (Graham, 1954).
The profusion of such glands in Siphonaria spp. (Yonge, 1960b) may explain why they an seldom eaten in
comparison with other limpets, being ignored by the limpet specialist, Chorisochisinus dentex, (Stobbs,
1980) and by oystercatcher (Parry, 1977; Hockey, 1980). Wrasse do, however, eat Siphonaria (Cook
1980). On a speculative note, the apparent undesirability of Siphonaria as prey item may be responsible
for the success of the genus in tropical water where predation is high and where other limpet genera are
poorly represented.
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
Some limpets react quite differently. While small Patella oculus and P. granatina have a typical running
response to starfish and predatory gastropods, large animals react aggressively, lifting their shells and
smashing them down on to the predator, often inflicting damage (Branch, 1979b). Not only do large and
small limpets respond differently, but the threshold of response is different with different predators.
The whelk Thais dubia is attacked by quite small limpets, while the large starfish Marthasterias glacialis is
only attached by relatively larger limpets (Fig. 38). Lottia gigantae may also be aggressive towards
predators (Stimson, 1970) as may Crepidula fornicate (Pratt, 1974).
Bullock (1953) has suggested that defensive responses
will only occur if the predator and prey species normally
encounter one another. In testing seven acmaeids, he
found high-shore species and limpets occupying large
algae displayed no response to predators. Margolin
(1964a) supported this conclusion, but Clark (1958)
found no correlation between the degree of habitat
overlap between predator and prey and the intensity of
the prey’s escape response. Branch (1978) also showed
the kelp-dwelling Patella compressa to be extremely reactive
to predators it is unlikely to meet in nature. Limpets do,
however, distinguish between predatory and nonpredatory species and only react defensively to the former (Bullock, 1953; Phillips. 1976). Dayton et al.
(1977) have even shown that limpets can detect the difference between foraging and non-foraging
predatory gastropods, and react accordingly.
The nature of the substance eliciting escape responses has been analysed by Mackie (1970, 1972; Mackie
& Turner, 1970). In the case of the starfish Marthasterias glacialis it is a steroid glycoside and it produces a
similar escape response to synthetic non-ionic surface-active agents. As such metabolites are likely to be
widespread in predatory starfish, this may explain the responses of limpets to some predators they never
meet in nature (Feder, 1972). Feder (1967) suggests that responses are strongest when the prey is
relatively large, but this is not the case in South African Patella spp. (Branch. 1978).
Phillips (1975a) has shown that Collisella limatula and Notoacmea scutum can detect a predatory starfish
(Pisaster ochraceus) at a distance, and move downstream if they are on a horizontal surface, but vertically
upwards when the substratum is angled (even if this means moving into the current). This upward
movement (negative geotaxis) may be more useful to the limpets in the field than a negative rheotaxis,
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
first because the turbulent intertidal zone will make
currents unpredictable, and secondly because the limpets
are zoned above Pisaster and upward movement will more
certainly result in escape. The receptors responsible for
this distance chemoreception are located in the mantle
margin, and recordings of discharges in the pallial nerves
reveal different responses to distance and to contact
reception, suggesting two different receptors (Phillips,
1975b). Contact response results in movement away from
the predator, and overrides the responses that follow
distance reception. Phillips (1977) describes the detailed
structure of mantle tentacles and surmises that the tufts of
non-mobile cilia have a sensory function. Phillips (1976)
also showed that the intensity of response was greatest to
predatory starfish that actually prey on the limpets, and
much less to non-predatory starfish or to predatory
species they never encounter. The average vertical upward
movement also increased if the predator was closer to the
limpet. This minimizes the time and energy spent on avoidance. The zonation of the limpets may also be
influenced by escape responses, upward movement displacing them up the shore. Phillips (1976)
suggests the responses allow limpets to exploit the richer feeding grounds lower on the shore and to
escape into the upper areas where the starfish do not occur.
While the above escape responses may be effective against slow-moving invertebrate predators, they are
unlikely to be effective against visually hunting mobile predators. Avoidance of detection is one
alternative. Giesel (1970) has described how there are two morphs of Collisella digitalis: a dark heavily
striped form on bare rock and a lighter coloured form in amongst the barnacle Pollicipes. These could be
ranked on a scale of 1 to 10 (lightest to darkest). To a certain extent these forms retain their colour and
pattern if transplanted from one habitat to the other, implying genetic control of colour and pattern.
When the limpets first settle, populations are unimodal with respect to the (ranked) colour morphs, and
randomly distributed between the two habitats, but within 6 months they are bimodal: a dark mode
associated with rocks and a light mode with Pollicipes (Fig. 39). In part this seems to be due to selection
(by bird predators) against limpets that do not match their background (although direct evidence of this
is lacking). The rate with which the Pollicipes population changes from a mixed pattern to a
predominantly light pattern is related to the amount of exposure to predators. In high-shore sites with
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
presumably greater intensity of predation, the change is quicker than in low-shore sheltered sites (Fig.
39C). This is matched by a greater variability of shell pattern in the protected sites, and reduction in the
tendency for limpets to migrate to the ‘correct’ substratum. In exposed sites ‘Pollicipes-type’ limpets
actively select and migrate to Pollicipes, while the dark forms prefer the rock surface. Giesel suggests that
this behavioural difference is genetically linked with shell pattern. Giesel (1969) also proposes that slow
growth is selected for in the ‘Pollicipes-forms’, to avoid the problem of space shortage on the barnacles.
Thus in this case Giesel (1970) feels the two morphs are adaptations for avoiding detection by predators.
Interbreeding must occur, but disruptive selection maintains the bimodal distribution of colour pattern.
In Patella granularis a comparable situation exists with a dark brown uniform patterning on limpets
among brown mussels (Perna perna) and a pale disruptively striped form among barnacles (Octomeris
angulosus) but we have no evidence of how this difference is maintained (Branch, unpubl.). Colouration is
also related to habitat in Collisella ochracea (Lindberg, 1979a) and in C. pelta (Jobe, 1968).
Crepidula convexa has three colour morphs: dark purple, brown, and tan, presumed to be genetically
controlled. Hoagland (1977) has shown that these morphs predominate on matching background rocks,
and has found that fitness (mean size, which is
correlated with brood size) is greatest in forms that
match the colour of the rock (Fig. 40). Again, visual
predators are held responsible, but simple transplant
experiments are needed to verify this conclusion, and
that of Giesel (1970).
Fishlyn & Phillips (1980) propose that Notoacmea paleacea has a novel method of avoiding detection by
the starfish Leptasterias hexactis. This limpet occurs only on surf-grass (Phyllospadix) and closely fits the
blades of its host-plant. The starfish seldom detects Notoacmea paleacea, often walking right over the
limpet without perceiving it, and the limpet in turn has no escape responses akin to those of most other
limpets. Its shell contains, however, a flavonoid chemical almost identical with one of nine flavonoids or
phenolic compounds present in Phyllospadix. Fishlyn & Phillips suggest that this flavonoid is extracted
from the limpet’s food-plant and incorporated into its shell where it acts as a chemical camouflage.
Homing to a scar may also reduce predation. Homing has traditionally been regarded as reducing
desiccation, but it also occurs in subtidal species in which it must have another function. Observations
on the limpet-eating Chorisochismus dentex show that it only attacks limpets when they are moving, and
hence off their scars (Stobbs, 1980). Vermeij (1978) suggests that the deeply sunken scars of tropical
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
limpets living on the stripes of macroalgae (such as Scurria scurra) are to reduce predation. Limpets which
adhere strongly to the rock and fit closely to their scars are also relatively seldom eaten (Branch &
Marsh, 1978). These are all indirect pointers to the importance of a home scar in reducing predation, but
Wells (1980) has produced direct evidence by recording the incidence of mortality of Collisella scabra in
experimental tanks where the limpets were kept with Octopus. Limpets which had home scars initially
suffered a much lower rate of predation than those lacking a scar (Fig. 41B). S. Garritty & S. Levings
(pers. comm.) have also shown that if Siphonaria is prevented from homing, its rate of mortality rises,
apparently due to increased vulnerability to predation. Limpets that are clamped tightly to their scars
have a better chance of retaining their position if attacked, while limpets caught unawares are easier to
dislodge. Arnold (1959) showed that Patella vulgata responds to shadows by clamping down, and Ross
(1968) demonstrated that in addition to their simple eyes, limpets can detect changes of light intensity
via their pallial tentacles. Notoacmea persona has a translucent pattern on its shell, allowing perception of
light directly through the shell (Lindberg, Kellogg & Hughes, 1975).
Descriptions have been given above (p. 252) of the activity rhythms of limpets. Many feed only while
awash with the rising and falling tides and not when exposed or completely submerged (see Table IV).
Wells (1980) describes this pattern in Collisella scabra and C. limatula and suggests its purpose is to reduce
predation. C. limatula lives under rocks and only emerges to feed during the period of wash. Wells
showed that animals kept in aquaria with a predatory
octopus suffered much higher mortalities if they were
prevented from hiding under stones (Fig. 41A).
Furthermore, if C. limatula were caged on the top of
rocks in the field they suffered 45 % mortality after 48
h in comparison with 12.6% in animals caged under
rocks.
In Patella miniata, small animals are confined to the under surfaces of rocks but animals larger than 38
mm in length occur on the upper surfaces (Branch, 1975c). I have suggested that this reduces
intraspecific competition as the larger individuals are always strongly dispersed, each rock carrying a
single P. miniata; but it is equally likely that the smaller, presumably more vulnerable, limpets are avoiding
predators.
Many of the activity patterns shown in Table IV make more sense if we view them as adaptations
reducing predation. Movements that are confined to the turbulent periods of wash or to the nocturnal
period will make it more difficult for mobile visual predators to locate the limpets or to feed effectively.
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
The size of a limpet, or its shell thickness, may be effective deterrents to a predator. For instance,
Stobbs (1980) showed that as the size of the limpeteating specialist Chorisochismus dentex, increased, so it
could eat larger limpets (Fig. 42), and incidentally also
tended to ignore smaller limpets. Evidently larger
limpets can escape the attentions of all but the largest
C. dentex. On the other hand, in limpets such as
Siphonaria that never achieve a large size, predators may
selectively eat the largest specimens (Cook, 1979).
Shell thickness in limpets has not been systematically investigated as an adaptation reducing predation,
but in South African Patellidae, low-shore and subtidal species that occur on open rock faces have the
thickest shells, while species that hide under rocks or occur in the folds of kelp fronds, or in the highshore, have much thinner shells.
Limpets that are damaged do have the ability to repair their shells quite quickly (Bulkley, 1968; Funke,
1968). Davies & Partridge (1972) describe how amoebocytes in the blood form long spikes, and
dependent on certain cations and a plasma factor, will then aggregate and form tight junctions when the
blood is withdrawn from the limpet. They suggest that the function of this is to seal and heal wounds.
Cooper-Willis (1979) has also shown that haemocyte numbers and acid phosphatase levels rise in Patella
vulgata that have been challenged by bacterial infection.
PARASITES
A number of internal parasites are known from British Patella spp., including a cestode and several
trematode cercaria (Crewe, 1947, 1951 ; James, 1968). Of these, Cercaria patellae is the most important,
with an infection rate of up to 20%. The incidence of infection increases in larger limpets, and may be
l00% in Patella depressa that are more than 65 mm in length. According to James (1968) the incidence also
increases in areas that are wave-beaten, possibly because more birds (the probable final hosts of the
parasite) nest or feed on the isolated exposed cliffs. Conversely, Thomas (1965) found infection highest
on sheltered gently sloping shores, which he ascribed to the numbers of birds resting at such sites.
The incidence of parasitism is low in South African Patella spp., and only in one localized population of
P. granatina has significant infection (up to 12 %) been recorded. Interestingly this was also Cercaria
patellae. A number of birds are possible final hosts for limpet trematodes, including oyster-catchers and
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
marine ducks, but the turnstone, Arenaria interpres, is a likely candidate in this case. It is known to eat
limpets (Branch, 1978), and the suggested adult stage of Cercaria patellae (Echinostephilla virgula) has been
found in the guts of turnstones in South Africa (G. M. Branch, unpubl.) and in Europe (D. I. Gibson,
pers. comm.). As these birds are migratory and also occur in Europe and America they are the probable
link between the two widely spaced areas where Cercaria patellae has been found.
Duerr (1968) has suggested that the reason why snails
(including limpets) often host trematodes is because they store
purines, which can form the base of protein synthesis of the
developing trematodes. C. patellae develops in the digestive
gland and gonad of limpets resulting in partial parasitic
castration (Rees, 1934) and in Patella granatina the size of the
gonad is reduced by 77% in parasitized limpets (Fig. 43).
Peritrich ciliates are known as external parasites attached to the gills and mantle of limpets (Brouardel,
1948, 1951). Details of their morphology and attachment organs are given by Hirshfield (1949) and Loin
& Corliss (1968). Acmaeids and Patella spp. are known hosts but the ciliates also occur on Cellana
tramoserica (Branch, unpubl.). Their effect on the limpet is unknown but not likely to be adverse, and
perhaps they should more logically be regarded as commensals. Debaisieux (1922) has described the life
cycle of Pseudoklossia patellae, a occidean infecting the digestive gland of Patella vulgata but gives no
particulars of its effect on the host.
Thus, only in few isolated cases are parasites known to be of importance in limpet populations; but this
may be a function of the paucity of research on the subject.
COMMENSALS
A number of small animals shelter under limpet shells on a casual basis and an even larger number may
live on the shell or bore into it (see Branch, 1975e for a list of those on South African Patella spp.). Many
of those living on the shell appear to do so in preference to settling on the rock-face, but this may
simply be a function of heavy limpet grazing on the rock. This applies particularly to algae (Bouxin,
1964; Branch, 1975e).
Other species are regularly associated with limpets and partly or wholly dependent on them. Scutellidium
patellarum occurs solely under Patella spp., particularly P. argenvillei and P. cochlear (Branch, 1975e), the
entire life cycle taking place there (Branch, 1974c). The numbers of this copepod rise exponentially with
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
the size of the limpet, the maximum recorded being 200 per limpet. They have no detectable effect on
the host. Interestingly, there are at least two free-living members of the genus that occur on algae
adjacent to the limpets but never under the limpets (Branch, 1975).
The flat worm Notoplana patellarum is regularly found under particular limpets, Patella oculus being the
preferred host (Stephenson, 1936; Koch, 1949; Branch, 1975e). It feeds on small Crustacea, including
Scutellidium patellarum and another commensal, the amphipod Calliopiella michaelseni, and not surprisingly
there is a negative correlation between the numbers of Notoplana patellarum and those of Scutellidium
patellatum that occur under the limpets. Choice chamber experiments demonstrate the preference of
Notoplana patellarum for Patella oculus over other Patella spp. but this preference is abolished if the P. oculus
is damaged or dead.
Two isopods, Dynamanella scabricula and D. australis, are most commonly found under limpets. The
former being a mid-shore species it associates with Patella granatina and P. granularis, while the latter
occurs lower on the shore and under Patella cochlear and P. argenvillei (Branch, 1975e). Although both can
be found free-living, they show marked preferences for limpets, in contrast to the completely free-living
Dynamanella huttoni. They lie in the pallial groove, heads buried amongst the gills, and may be feeding on
algal fragments left by the rasping of the limpet, but they also emerge to feed on algae on the shell.
Another member of the genus is commensal under the chiton Acanthopleura granulata (Glynn, 1968).
The amphipod Hyale grandicornis regularly occurs under acmaeids (Johnson, 1968) and under Patella
vulgata in Europe (W. Vader, pers. comm.). Only juveniles are associated with acmaeids, the adults being
free-living, but in South Africa both juveniles and adults occur under limpets, possibly a function of the
much larger size of the limpets (Branch, 1975e). Juveniles of the other Hyale spp. are found under Patella
vulgata, but seemingly on a casual basis (Vader, 1972b). As the tide rises, Hyale grandicornis leaves the
limpets to feed, and no specially close relationship exists. In contrast, another amphipod, Calliopiella
michaelseni, occurs almost exclusively under limpets. A positive correlation exists between limpet and
amphipod size. Furthermore, a high percentage of large limpets house a male and female pair of C.
michaelseni. After release from the brood pouch, juveniles disperse from the limpet occupied by their
parents and hardly ever do more than two adult amphipods occur under one limpet. As C. rnichaelseni
feeds on the faeces of the limpet, food may be limiting and the restricted numbers of amphipods per
host may relate to this. How the pattern is maintained is not known but territorial defence is possible, as
amphipods introduced into an aquarium will not move under limpets that are already occupied by a pair
of C. michaelseni (G. M. Branch, unpubl.). Polynoid polychaetes are well known commensals under
several limpets including Megathura crenulata, Diadora spp. and acmaeids and may also occur with sea
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
cucumbers and other hosts. They can distinguish between different host species from which they are
taken (Hickok & Davenport, 1957), although they can be conditioned to accept alternate hosts (Dimock
& Davenport, 1971). Hosts can be detected at a distance, by way of the sensory antennae, and on
contact, by the palps (Gerber & Stout, 1968). Arctonoe pulchra becomes aggressive as it grows, and
although up to seven small worms may share a limpet, large worms (> 20 mm in length) are always
solitary due to strong intraspecific aggression (Dimock, 1971). Of greater interest is the observation that
this polychaete will attack and repel predatory starfish that approach the limpet (Dimock & Dimock,
1969). This is the first indication that the association between limpet and worm may be mutually
beneficial.
INTRASPECIFIC COMPETITION
Effects of intraspecific competition
Intraspecific competition has often been demonstrated in limpet populations. Its influence on growth
rate has frequently been inferred. For example, mean and maximum body size declines as density
increases (Fig. 44A) in Patella cochlear and other species and
measurements of growth rates confirm a decline with an increase in
natural density (Hodgkin, 1960; Ballantine, 1965; Branch, 1975b.
1976; Thompson, 1979, 1980). The fact that growth of Siphonaria
pectinata is high after organic enrichment encourages algal growth
(Voss, 1959), and that Patella vulgata grows much faster under the
dense algal canopy that develops after oil pollution (e.g. Southward &
Southward, 1978), leads us to the same conclusion: that food is
normally short, and that intraspecific competition contributes to this
shortage. In P. cochlear. biomass rises with density up to a plateau of
about 125 g⋅m-2, but above a density of 450⋅m-2 no further increase in
biomass occurs and competition must become particularly intense
(Fig. 44B).
Black (1977) has experimentally confirmed the effect of density on growth by thinning some
populations of Patelloida alticostata and supplementing others with additional animals, and then following
the growth of recruits. Underwood (1978b) has shown Cellana tramoserica declines in body weight at
higher densities. The growth of Collisella onychitis is similarly depressed at higher natural and experimental
densities (Black et al., 1979) and its growth rate is reduced progressively up the shore, in parallel with the
mean standing stock of algae and the productivity of algae (Fig. 45).
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
Creese (1980c) has distinguished some of the interacting factors that influence growth by experimentally
modifying the density of N. petterdi at different heights on the shore, and showing that growth is greater
at lower densities and at lower heights on the shore, other factors being equal (see Fig. 29). N. petterdi is
an extreme high-shore species, and its densities are lowest high on the shore. Consequently, despite the
reduction of algal food at higher levels, growth is greatest there.
Intraspecific competition has variable effects on the mortality
of adult limpets. While N. petterdi has a greater mortality at
higher densities. Frank (1965a) and Choat (1977) found that the
mortality of Collisella digitalis was unchanged by alterations of
density, and mortality of Patelloida alticostata is largely due to
density-independent factors such as predation by Dicathais and
desiccation (Black, 1977). Patella cochlear is a special case, for its
populations are usually crowded, so that settling juveniles
survive only if they settle on the shells of other P. cochlear. The more dense the population is, the greater
the proportion settling on other shells. With growth, a point is reached where the limpets are too large
to occupy shells and must descend to the rock. This transition makes the animals vulnerable until they
establish a new home scar, and high mortality occurs during this period. In this way the indirect effect of
increased density is to cause higher mortality, but this is not a direct consequence of competition for
food (Branch, 1975b).
Branch (1975b) and Choat (1977) have shown that gonad weight (in relation to body weight) is little
affected by density. If competition reduces growth, and hence body size, then it has an indirect effect on
the reproductive output. In P. cochlear the gonadal output per individual drops as density rises (Fig. 44D),
but more interestingly, although the total output (per m2) rises initially with density, it peaks at a density
of 430⋅m-2 and then drops dramatically (Fig. 44C) (Branch, 1975b). The same effect occurs in P.
granularis but is complicated by the influence of barnacles (see below).
Whilst a few authors have found that recruitment of juveniles is adversely effected by adults, as in P.
vulgata and Cellana tramoserica (Lewis & Bowman, 1975; Creese, 1978), in most cases settlement has either
been independent of adult density, or is actually higher in areas where adults are common (Frank, l965a;
Black, 1977; Choat, 1977; Creese, 1978). Of course, this does not prove that the adults are not reducing
success of settling, for the settling larvae may select sites where adults are present (as Dixon, 1978,
suggests) or may survive better in areas where adults have previously succeeded. Juvenile Patelloida
latistrigata seem to do better in areas kept clean of algal growth by the grazing of adults (Creese, 1978).
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
Branch (1975b) showed that Patella cochlear settled (or survived) in highest numbers where densities were
high, which was also where wave action was highest. Subsequent work has shown that if the adults are
glued to the rock face settling is even greatel in these high density populations. Evidently two factors are
at play: higher settling in areas of high adult density, coupled with the removal of new recruit that settle
on the rock and can be grazed by adults. It is the elimination of this latter effect that results in the
boosted recruitment (Branch, unpubl.).
Intraspecific competition may also influence the range of habitat occupied (niche breadth). R. Black
(pers. comm.) has shown that as the density of
Patelloida alticostata rises, so it occupies a greater
number of shore level (Fig. 46). Interestingly, the
presence of a competitive chiton reduces the range
occupied by P. alticostata, so interspecific competition
may have the opposite effect, causing a contraction of
range (Fig. 46). Under more rigorous experimental
conditions, Black (1977) showed that P. alticostata
decrease the height to which it grazes if density is reduced.
Intuitively it might be expected that a species will do best at the centre its range, but two studies have
shown that this is not necessarily so, if interspecific competition is more intense there. Patella cochlear
ranges up to density of 1600⋅m-2 and achieves highest densities at the centre of its vertical range on the
shore and under conditions of strong but not violent wave action. At higher densities, growth, size and
survival are reduced and reproductive output drastically lowered (Branch, 1975b). Experiments show
that these effects are related to density and competition for food. In contra the low density periferal
populations have a much greater total garnet output, and I have suggested that it is recruitment from
these populations that is largely responsible for maintaining the high density populations.
Sutherlands (1970, 1972) analyses of high and low-shore populations of Collisella scabra reveal a
comparable situation. Low-shore populations are clearly at the centre of the species’ range and have high
densities because recruitment is greater and more predictable. These high densities reduce growth (and
thus size), and increase mortality, so that population density fluctuates annually. Food is more constant
low on the shore, so reproduction occurs over much of the year. Conversely, on the high-shore, reduced
tidal submergence lowers recruitment and density is lower but does not fluctuate during the year. Food
is seasonal and growth, although greater than on the low-shore, is also seasonal. Reproduction also
occurs when food is available. Figure 47 summarizes the contrasting situations of high- and low-shore
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
habitats and shows that the ‘edge’ of the range may support a higher biomass because competition is
less. Energy flow through the two populations is approximately equal (Sutherland, 1972, see above).
Territoriality occurs in Lottia gigantea (Stimson,
1970), Patella longicosta to, P. tabularis, probably P.
compressa, and in a mild form in P. cochlear (Branch,
1971, 1975c, 1976). Usually it is the larger, adult
individuals that possess a territory, which they
defend by thrusting against intruding limpets or
other herbivores, and even exclude anemone and
retard the encroachment of mussels. Lottia gigantea
maintains a generalized fine algal turf (see below. p.
347) but Patella longicosta and P. tabularis are even
more
specialized,
defending
patches
of
the
encrusting alga Ralfsia expansa (Fig. 48A), and Patella
cochlear has a fringing ‘garden’ of fine red algae (Fig.
49), mainly Herposiphonia heringii and Gelidiurn micropterum. The latter is only found in these gardens.
Although these gardens initially flourish if Patella cochlear is removed, they subsequently die back and are
replaced by other algae and clearly depend on the limpets for their maintenance. P. laticostata has very
similar gardens of red algae (including a Herposiphonia sp.) that fringe the limpets and are restricted to
solitary adult limpets (Branch, pers. obs.). A similar relationship may exist in this limpet. Both Lottia
gigantea and Patella longicosta exclude all juveniles of their own species from their territories (Branch, 1971,
1975c; Stimson, 1973) and if adults are removed, their territories are very quickly taken over by the
‘floating’ juveniles, and again only one becomes established in each territory. P. longicosta has a complex
life cycle. All juveniles are found on other shells, most often on the winkle Oxystele sinensis or on other
Patella longicosta. There they are always associated with an encrustation of Ralfsia on which they feed.
Once they are too large for this habitat they migrate onto the rock and for a period are associated with
an encrusting coralline, Lithophyllum , on which they feed (Fig. 48B). During this period body weights
fall, and the ash content of the body rises and none of the limpets matures sexually (Branch, unpubl.).
Adult Patella longicosta are all found on Ralfsia gardens, but the mechanism whereby gardens are
established is not known. Over 95% of the Ralfsia that is found intertidally occurs in Patella longicosta
gardens, and it is possible that the floating juveniles must locate one of the rare unoccupied patches or
await the death of a territorial individual.
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
Thus, territoriality denies ‘floaters’ access to choice feeding grounds and because they, therefore, grow
more slowly and suffer reproductively, ultimately this has a density-regulating effect.
P. granularis, P. vulgata, and Collisella scabra also act aggressively towards members of the same species, but
in most cases this is related to defence of the home scar, and involves forcing away intruders that have
occupied a scar (Stephenson, in Thorpe, 1962; Funke, 1965; Sutherland, 1970) and is not related to
defence of a food source.
Thus, intraspecific competition can have substantial effects, reducing growth, size, and survival,
modifying niche breadth, influencing recruitment, and resulting in the exclusion of individuals from
territorial areas.
Mechanisms reducing intraspecific competition
Migration: The correlation between body size and height on the shore may be the result of progressive
upward migration, as has been demonstrated in Patella vulgata (Lewis. 1954), P. granularis, P. granatina, and
probably P. concolor (Branch, 1975c.d), Acmaea dorsuosa (Abe. 1932), Collisella digitalis (Frank, 1965a), and
C. strigatella (Seapy & Hoppe, 1973). I have suggested that upward migration reduces intraspecific
competition, shifting larger animals above the range of the juveniles (Branch, 1975c). The case has been
explored for C. digitalis by Breen (1972) who recorded the incidence of upward migration in winter,
which greatly exceeded downwards movement in summer (see Fig. 1. p. 237) and thus resulted in a net
upward movement with ace. Breen also showed that emigration was greater from crowded populations
and that growth was inversely related to density. More important, he demonstrated that animals that
migrated upwards grew significantly faster than non-migrants, showing that migration probably does
relieve intraspecific competition.
We must, however, be cautious of deducing that migration occurs, simply from a size gradient. Neither
C. scabra nor Notoacmea petterdi migrate upwards (Sutherland, 1972; Creese, 1980c) yet they are larger at
the top of the shore due to decreased competition. Both species occupy physically demanding habitats,
and it may be more important for them to home to a scar and reduce desiccation than to be able to
migrate upwards.
Dispersion: Aitken (1972) revealed that Patella vulgata tends to emigrate more rapidly from areas of high
density and moves into areas of low-density. Several other species disperse in this way (Creese, 1978),
and the pattern is particularly marked when space or food is short. Lepeta concentrica (Yonge, 1960a) and
Patella miniata (Branch, 1975c) usually occur singly on stones and only single Patelloida nigrosulcata,
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
(Branch, unpubl.) P. miniata and P. insignis (Creese, 1978) occur on their respective host-shells. Patella
compressa adults are nearly always isolated on kelp stipes (Branch, 1975c). Creese (1978) has shown that
when Patelloida mimula was allowed a choice of oyster shells which had resident limpets already attached
or which lacked limpets, 89%,, chose the unoccupied shells. Similarly the survival rate was higher in
limpets that were placed on unoccupied than on occupied shells.
Breen (1971) tested the hypothesis that the incidence of homing in Collisella digitalis decreases when food
availability was low. He experimentally doubled or quadrupled the density of the limpets, but failed to
find any change in the proportion of limpets that homed. Unfortunately his experimental design was not
satisfactory, for the control was separated from the experimental populations by up to 5 months, so no
definite conclusion can come from this result. In a shorter-term experiment he found that reduction of
algal levels resulted in an increased incidence and distance of movement away from the site and that
limpets also responded almost immediately to an increased density by
emigrating at a higher rate.
This same question was addressed by MacKay & Underwood (1977), who
showed that in Cellana tramoserica a proportion of the population homes
while the rest of the limpets are non-homers. The proportion was not
related to tidal height, wave action, regularity of the substratum or the
amount of Hildenbrandia present. Desiccation stress was thus unrelated to
the incidence of homing. The incidence of non-homers rose, however,
with density, and when microalgal food was eliminated by burning, the
rate of emigration increased. This led MacKay and Underwood to
hypothesize that homing is a means of regulating density in relation to
food availability. Shortage of food seemed the key factor increasing the
incidence of non-homers. Thus density regulation can be added to the list of functions ascribed to
homing, resistance to desiccation and avoidance of predation already having been discussed. Perhaps it
is unrealistic to seek a universal purpose for homing.
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
Different species may need to home for different reasons, or may even simultaneously use homing for
more than one purpose.
S. B. Cook (pers. Comm.) has shown that in dense populations of Siphonaria, individuals that encounter
a neighbour will stop, “cluster” with the neighbour and then reverse direction and return home. This
does not happen in sparse populations. This is an interesting pattern, for it could reduce grazing in
crowded habitats. The value of this to the individual is, however, doubtful and it may really be to reduce
grazing over an area already occupied by another limpet. This suggestion is strengthened by Cook &
Cook’s (1981) observation that successive excursions from the scar are directed in different directions,
so when the limpet returns home after encountering a neighbour, it can then resume its foraging in a
different direction.
Thus in various forms, dispersion away from a neighbour, if it is linked with food shortage, can spread
the population and reduce competition, probably also leading to an increase of niche breadth (see Fig.
46).
Dispersal: Patella cochlear characteristically occurs at very high densities and occupies a narrow hand at the
bottom of the shore. In addition, it is territorial and depends on its fringing garden for food. Dispersion
away from sites of high density is not possible, but the limpets have a remarkably uniform pattern of
dispersal (Fig. 49A), which maximizes the distance between limpets. Adult limpets also feed by rotating
on their scars, grazing the garden, and this too reduces contact between the animals (Branch. 1975c). As
density rises, dispersal becomes more uniform. The same is true of the arrangement of P. longicosta
territories. Both species always maintain a minimum distance between animals. This is particularly
obvious in P. cochlear, for juveniles are largely confined to the shells of adults, and although they descend
to the rock face to graze, they will not establish their own territories on the rock face unless sufficient
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
space is available between the adults. Death of an adult limpet leads to an immediate occupation of the
vacant scar by one of the juveniles (Branch. 1975c).
Underwood (1976b) could find no difference in the dispersal pattern (distance to nearest neighbour) of
Cellana tramoserica in relation to density, but Sutherland (1970) describes how low-shore, high-density
Collisella scabra are uniformly to randomly distributed (presumably to reduce competition) while the
sparse high-shore animals are contagiously aggregated into clumps, possibly to reduce desiccation (the
suggested function of clustering in C. digitalis, see above). Patella granularis also forms clusters in the highshore and is dispersed in the low-shore, but if barnacles are present in the high-shore then the limpets
are randomly distributed (Branch. 1975c).
Adult-Juvenile differentiation: The change of habitat that P. longicosta undergoes, from juveniles occupying
shells to adults occupying Ralfsia gardens (see above), effectively separates adult and juvenile habitats. In
addition the transition involves a prolonged period when the limpets are confined to, and largely feed
on, encrusting corallines. This further separates the requirements ofdifferent sized animals and is one of
the few instances of a limpet changing its diet. In part the change is forced by a scarcity of the preferred
food plant. R. expansa, outside of territorially defended areas, but effectively it compels the limpets to eat
different food plants at different stages of development (Branch, 1975c). Six species of acmaeids can
occupy shells as juveniles and then become rock-dwelling as they grow larger (Brewer, 1975).
Patella cochlear may reduce competition by forming “stacks”: smaller animals living on the backs of larger
animals (Fig. 49A) and even forming fringing gardens there and beingable to feed on the host shell
(Branch, 1975c). Host shells that are detached from the rock are almost immediately abandoned by the
juveniles which have a well-defined response if the shell is inverted, loosening their grip and dropping
from the shell (Branch, 1971). P. miniata juveniles are found only under stones while adults occupy the
upper surface. P. compressa occupies only the folds between the kelp fronds when it is very small, moving
into the kelp hand at an age of about one year while older animals are confined to the kelp stipe
(Branch, 1975c). In all these cases differences between adults and juveniles may reduce competition, but
direct evidence for this is lacking and, as discussed earlier, there may be other explanations such as
increased tolerance to wave action or increased imiimunity to predation that allows adults to occupy
habitats where juveniles cannot occur. In the same way the polymorphism of Collisella digitalis (Giesel,
1970) may allow it to occupy two habitats whereas predation might limit it to one of these habitats of it
were monomorphic.
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
Population regulation: Stimson & Black (1975) have manipulated the densities of various acmaeids,
doubling the density or reducing it to almost zero, and then compared the fate of the acmaeids over two
years. They found that density rose in the low-density sites, and declined in the high-density site, relative
to the density in the untouched control in other words, population regulation occurred, the manipulated
populations tending to return to their original levels. The data did not allow the cause of regulation to be
determined. Possible causes were increased adult mortality at higher densities, altered rates of emigration
and immigration, reduced recruitment at high adult densities or greater mortality of juveniles due to
starvation or cannabalism by the higher adult densities. Stimson & Black concluded that recruitment was
reduced at high adult densities, but as Underwood (1979) has pointed out, this conclusion is suspect as it
was based on the proportion of juveniles and adults in random samples of 50 animals. Since this
proportion will depend on the initial numbers of adults in each population, actual densities of recruits
are needed before this conclusion can be accepted.
Black (1977) has repeated this experiment on Patelloida alticostata. The populations converged in density
but had not completed their return to original levels after two years. Although recruits were greater in
the experimental lots where adults were sparse, in unmodified areas recruitment was actually higher
where adults were more dense. Hence Black concluded that density regulation could not be due to a
change in recruitment rate. The situation is parallel to that of Patella cochlear (see p. 335) in which
recruitment is high where adults are dense, yet the adults may have an adverse effect on the survival of
recruits. Growth of Patelloida alticostata did decline in high-density populations, but mortality was not
affected. Thus, although population regulation began to occur, the response was sluggish and no clear
mechanism for regulation could be identified. Nevertheless, in both species a return to original (or near
original) levels did take place, and suggests that intraspecific competition can be reduced by regulation of
densities.
Migratory and non-migratory species: In a comparison of several Patella spp. I have made a distinction
between species that migrate upshore as they age and become more tolerant of physical stress, and those
that do not (Branch, 1975c). The former are all mid- to high-shore species which may reduce
intraspecific competition by their migration. Upshore movement is usually seasonal, occurring when
physical stress is reduced (Abe, 1932; Frank, 1965a; Breen, 1972; Seapy & Hoppe, 1973; Branch, 1975c)
and when food availability should be increasing. The standing stock of food in the high-shore is,
however, low (see Fig. 45) and macroalgae almost entirely absent (Black et at., 1979) so that a
generalized diet is forced on these higher-shore limpets. None of them is territorial, as there is no single
area with sufficient and reliable enough food to justify defence, and none is aggressive towards other
members of their species; in fact, they often aggregate in clusters, possibly reducing desiccation in the
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
process (Millard, 1968; Willoughby, 1973; Branch, 1975c). Most migrant species lack a home scar or
possess a temporary scar that is readily abandoned if conditions change. They also lack any obvious
differentiation between adults and juveniles in terms of microhabitat or food. In part this is because they
have generalized diets which do not allow for specialization, but it may also be because the migratory
habit spatially separates animals of different ages and reduces competition.
In contrast, the non-migratory species are mostly low-shore and subtidal species. In the low shore food
is more abundant, more constantly available and there are many macroalgae that are continually present
(Sutherland. 1970; Black et at. 1979). If a species is to be non-migratory and occupy practically the same
position throughout life, it cannot escape intraspecific competition by moving away. On the other hand,
the low shore provides opportunities for specialization and many of the species have specialized diets or
are epiphytic on large algae. More subtle means of reducing intraspecific competition have been
developed. Territorial defence of specific areas (Stimson, 1970, 1973) or particular algae (Branch, 1975c,
1976 becomes possible and yields a reliable food source. Most non-migratory species are aggressive
towards co-specifics so that if territoriality does not exist at least the limpets are widely dispersed (see
above). Dispersal pattern tends to be uniform, spacing the limpets out, and in some species there is clear
adult-juvenile differentiation in terms of microhabitat or diet. Most of the species home rigidly to a
home scar and this is particularly obvious in territorial species (Branch, 1975c).
Figure 50 summarizes and contrasts the migratory and nonmigrators characteristics of South African Patella spp. Clearly,
some species are intermediate, and interestingly the species
which are most distinctively migrators or non-migratory are
those known to suffer most from intraspecific competi tion
(Branch, 1975b,c, 1976). The terms “migratory” and “nonmigratory” are descriptive and adequately cover the South
African species, but need to be broadened to encompass other
species. Migratory species should include all species that move
in response to a shortage of food, as for example Cellana
tramoserica (MacKay & Underwpod, 1977), and not only those
that migrate up-shore. And while the description given of
non-migratory spccics is adequate for most low-shore and
subtidal specialists, there are at least two ultra-high-shore “non-migratory” species, Notoacmea petterdi
(Creese, 1980c) and Collisella scabra (Sutherland, 1970) that do not conform. I suggest that rigid homing
in these species is related to physical stresses and not to a specialized food source as it often is in the
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
low-shore, and that these species have more in common with the other high- to mid-shore species,
having generalized diets, being non-aggressive and non-territorial.
INTERSPECIFIC COMPETITION
Competition between grazers
Several authors have deduced that competition occurs between species because one species is reduced in
numbers where the other is common. This is true of Patella aspera and P. vulgata. The former occupies
areas of strong wave action, but reduces in number as wave action declines and is progressively confined
to the low-shore and replaced by P. vulgata (Thompson, 1979, 1980: see above p. 269). This replacement
may mean competitive displacement, but there is no proof of this. The case is more convincing when
one species intrudes into the centre of another’s range and excludes it from that part of its presumed
habitat. For instance, P. longicosta is found both above and below P. cochlear on the shore, but is excluded
from the P. cochlear zone (Branch, 1976). Similarly Collisella onychitis intrudes into the niche of Siphonaria
kurracheensis. In this case Black (1979) has experimentally removed Collisella onychitis and shown that
Siphonaria kurracheensis then fills this portion of its range (Fig. 51) demonstrating that this species is being
competitively excluded by Collisella onychitis. The two species
have very different radulae (see above), all Siphonaria spp.
rasping over the surface of the substratum or biting pieces
off macroalgae. Collisella onychitis has a stronger radula and
digs into the rock surface, thus removing more microalgal
growth. Thus C. onychitis is predictably a superior competitor
over Siphonaria kurracheensis.
Competition is also inferred from overlapping diets and spatial patterns. Connor (1975) has shown that
Collisella limatula and the chiton Cyanoplax hartwegii both feed on Pelvetia and Hildenbrandia, and that the
limpet is significantly smaller if it occurs within 20 cm of the chiton than if it is more than 50 cm away.
Black (1979) has also shown for Siphonaria kurracheensis and Collisella onychitis that the distance between
nearest neighbours increases with the size of neighbours; and this too may be indicative of competition.
In recent years there have been several experimental demonstrations of competition between grazers.
Haven (1973) showed that if Collisella digitalis and C. scabra were removed from mixed populations, the
remaining species grew faster and there was an accompanying increase in algal biomass. Each species
thus has an adverse effect on the other but the design ofthe experiment does not allow us to gauge if
interspecific competition has a greater or lesser effect than intraspecific competition. Dixon (1978)
shows a similar effect between other pairs of acmaeids.
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
Underwood (1978b) compared the competitive interactions of three prosobranchs, including Cellana
tramoserica. Mortality of this limpet rose at higher
densities, and body weight declined. Increases in the
density of Nerita atramentosa had a similar effect on the
limpet, but Bembicium nanum had no effect on the body
weight or mortality of Cellana tramoserica (Fig. 52).
Underwood showed that C. tramoserica is a superior
competitor to Bembicium nanum, and that Nerita
atramentosa is superior to both. He related this to more
rapid movement and grazing by N. atramentosa, and the
greater depth to which the radula of Cellana tramoserica digs into the substratum.
Creese (1978) tested the interactions between several species of limpets, by caging them separately and
together at various densities. C. tramoserica suffered higher mortalities when its own numbers were
increased, but was unaffected by two Siphonaria spp. Mortality of the Siphonaria spp. rose as the density
of Cellana tramoserica increased, but as the latter could not be maintained at very high densities due to
adverse intraspecific effects, it is unlikely that it could ever become dense enough in the field to exclude
the Siphonaria app. Again, Cellana tramoserica digs deeply into the substratum while the siphonariids scrape
over the surface, so the outcome of competition is predictable. C. tramoserica also increases the mortality
of Patelloida alticostata and P. latistrigata adults, and of recruits of most other limpets.
Competition also occurs between Cellana tramoserica and the asteroid Patiriella exigua which is a microalgal
grazer (Branch & Branch, 1980). When caged with high densities of the limpet, P. exigua decreased in
body weight, but strangely Cellana tramoserica increased more in body weight in the presence of Patiriella
exiqua than in its absence. The reason for this is unknown. In addition to possible competition for food,
Cellana tramoserica also has an interference effect on the starfish. When they meet, the limpet extends its
mantle over the edge of the shell and expands its tentacles, and contact with these is clearly repellent to
the starfish, which pulls its arm away and retreats. Contact can even result in a temporary ‘wrinkling’ of
the starfish’s arm, giving the appearance of paralysis.
Competition between grazers can affect the distribution of one or both species, as described above,
where one species intrudes into the centre of the range of another, and excludes it from that area. Choat
(1977) has shown that when he removed Collisella digitalis from pilings, C. strigatella (= Acmaea
paradigitalis), which is normally confined to the zone below Collisella digitalis, then expanded its range and
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
moved upwards (Fig. 53). This is an important result,
for it shows that competitive interactions between
grazers can set upper limits on zonation.
Dixon (1978) has confirmed that if C. digitalis is
removed, C. strigatella moved upwards, and also shows
that its growth rate increases (Fig. 54). The decrease of
niche breadth in Patelloida alticostata in the presence of
competitive chitons (R. Black, pers. comm.) suggests the same effect. On the other hand, Dixon (1978)
has shown that the growth of a low-level species, Notoacmea fenestrata is actually faster in the presence ofa
higher-shore competitor. Collisella strigatella than if it is
kept at equivalent densities on its own; yet it does not
migrate up into the zone occupied by C. strigatella, in
contradiction to Wolcott’s (1973) hypothesis. Dixon
concludes that Notoacmea fenestrata is limited by physical
factors from migrating upwards, although his evidence
for this is not strong.
Connor (1975) has shown that if the numbers of Collisella pelta are doubled, density of the chiton
Cyanoplex hartwegii (with which it probably competes) is reduced; while removal of Collisella pelta results in
an increase in Cyanoplex hartwegii (Fig. 55A). As the changes are very rapid (almost from day to day) the
chiton may be responding directly to the limpet and not simply to a resulting change in food supply,
suggesting some interference effects. The chiton Mopalia muscosa reacts aggressively to Collisella pelta,
actively pushing it away. When C. pelta are placed within 1
cm of a Mopalia, they move further during the ensuing
hour than do controls placed more than 20 cm from
Mopalia (Fig. 55B). When Mopalia contacts a Collisella
limatula, it fails to be aggressive: this is significant, for C.
limatula does not eat the same food as Mopalia while
Collisella pelta is a direct threat to its food supply.
R. G. Creese (pers. comm.) is at present working on interactions between the chiton Katherina tunicata
and limpets. Collisella pelta may shove against the chiton, which retaliates and eventually pushes the
limpet away, often biting it on the edge of the shell for good measure. Notoacmea scutum, however, will
“mushroom” and move away from the chiton.
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
Territoriality introduces a new dimension to
competition between limpets. Stimson (1970) has
shown that Lottia gigantea excludes acmaeids from
its territorial algal patch. Removal of the territory
holder is followed by an invasion of other
acmaeids, while if a Lottia is re-installed into the
area these limpets are again excluded (Fig. 56).
Exclusion of other limpets is essential for the
maintenance of the algal patch, since the amount
of alga left behind after grazing is proportional to
the size of the grazing limpet (Stimson, 1973). The
smaller species thus eliminate most of the alga
while Lottia leaves more, allowing recurrent
grazing. Patella longicosta similarly excludes other
herbivores, particularly P. oculus, from its territorial
Ralfsia gardens (see Fig. 48A).
W. G. Wright (pers. comm.) has measured the force Lottia gigantea exerts on other limpets during
territorial contests and records a mean force of 2.1 kg. This greatly exceeds the resistance of moving
limpets to dislodgement (095 kg) so it is not surprising that L. gigantea can actually dislodge intruding
limpets. As dislodgement is likely to result in death, Wright’s (1977) observations are particularly
interesting; he found that Collisella digitalis can recognize and actively avoids Lottia territories. Specimens
placed on empty territories move away from them much faster than from control areas (Fig. 57B).
Collisella digitalis, in common with C. pelta, does not
home to a fixed point, and even when stationary has
a tenacity equivalent to only 19 kg; still inadequate to
resist dislodgement by Lottia gigantea. On the other
hand, homing species, including Collisella scabra and
other Lottia gigantea, can resist forces in excess of 5kg
when they are on their scars (Fig. 57A) and it is
significant that Collisella scabra does not avoid Lottia
territories (W. G. Wright, pers. comm.). All
introducing limpets have a well-developed escape response if they come into contact with a limpet
tentacle (of any species) while they are on a Lottia territory, but this response is absent if they are not on
a territory (Wright, 1977). The decision as to whether a Lottia should fight or flee when it contacts
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
another Lottia depends on how close it is to its own home scar: the closer it is, the more likely it is to be
aggressive (Wright, 1978).
Thus there are well defined territorial defences in several species of limpet, and a corresponding suite of
responses in intruding limpets that minimize the danger of dislodgement by the territorial animal.
Interactions with sessile species
Many authors have recorded the adverse effect barnacles have on limpets, depressing growth (Jones,
1948; Fischer-Piette, 1948; Lewis, 1954; Lewis & Bowman, 1975; Branch, 1976; Choat, 1977). The
influence of barnacles on recruitment of limpets varies from species to species. Hatton (1938) found
Patella vulgata settled more frequently in areas cleared of barnacles, and Dixon (1978) obtained the same
result for Collisella digitalis, Notoaemea fenestrata and Collisella stigatella, as did Creese (1980c) for Notoacmea
petterdi. Conversely, Choat (1977) found settling of Collisella scabra and C. digitalis was proportional to
barnacle cover, and Lewis & Bowman (1975) recorded highest survival of newly settled Patella vulgata
amongst barnacles and mussels where desiccation was less. Although these differing results may reflect
differences between the species, they also emphasize an unsolved problem: seldom is settlement actually
recorded. Usually limpets are a few months old before they are even detected, so that we are recording
those recruits that survive rather than the actual number that settle. Settling may well be reduced
amongst barnacles, but subsequent survival enhanced by barnacles.
As limpets grow, they may become too large to fit between barnacles, and Hatton tested this effect by
mounting plaster of paris dummy barnacles on the rock. He found that the numbers of P. vulgata
declined as a result. Choat (1977) also found that the irregular surface created by barnacles prevented
Collisella digitalis from ‘sealing’ effectively to the substratum, with consequently high mortality due to
desiccation in summer. Thus, while limpets are small they may shelter between barnacles and reduce
desiccation stress, but as they grow larger they may be at a disadvantage among barnacles. It is at this
stage that Lewis & Bowman (1975) recorded Patella vulgata emerging from “wet settlement” sites onto
the bare rock.
Mortality of adult P. granularis is unaffected by barnacle density, but growth is considerably reduced, and
mean size declines. This has a direct effect on the reproductive output. The relationship is, however, not
straight forward for high densities of barnacles are correlated with high numbers of P. granularis, and
both high limpet density and high barnacle density reduce the growth and size of the limpets (Fig. 58).
An analysis of covariance reveals that at a constant limpet density, body size is reduced by increasing
barnacle cover. The total reproductive output of P. granularis rises with density, to peak at about l00.m2
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
and then falls with further increases in limpet density. Again,
at a given limpet density, barnacle cover is inversely related
to limpet reproductive output (Fig. 59) (Branch, 1976).
The other side of the coin is that limpets have an adverse
effect on barnacles. P. cochlear completely excludes barnacles
from the P. cochlear zone, but on removal of the limpets
dense settlements of Balanus algicola appear (Branch. 1975b),
Hatton (1938), Lewis (1954), Southward (1956), Connell
(1961), and Dayton (1971) all record that limpets reduce
survival of post-settlement barnacles. Menge (1976)
produced evidence of this in experimental cages, but
doubted whether the effect was meaningful as he had to use
limpet densities 8 to 12 times the natural density to achieve
this result. Denley & Underwoods (1979) study shows, howcver, that while natural densities of Cellana
tramserica have no effect on the rate of settling, they reduce the subsequent survival of Tesseropora rosea to
about 41% in comparison with 65% in limpet-free areas.
Normal grazing by limpets seems incapable of preventing encroachment of mussels (Menge, 1976) but
Lottia gigantea (Stimson, 1970) excludes or slows the rate of encroachment by mussels onto its territorial
areas, and mussels never intrude onto the territories of Patella tabularis (Branch, 1976).
Mechanisms allowing co-existence of limpets with competitors
Differential zonation of limpet species may reduce overlap and hence competition. Zonation has
previously been regarded as a consequence of tolerance to physical stress, but work showing that species
may expand their ranges after removal of a competitor suggests competition as a mechanism controlling
zonation.
Differences in diet may also reduce competition as suggested for acmaeids (Craig, 1968; Eaton, 1968;
Connor, 1975) and patellids (Branch, 1971, 1976). Dietary differences or specialization do not prove that
competition exists, nor that it was the historical cause of such differences, although this inference is
often drawn. Moving around the South African coastline, the numbers of coexisting patellids reach a
peak at the Cape of Good Hope, and the numbers at any given point are related to the average dietary
and habitat specialization of those species. In other words, the more species coexisting, the more
spccialized they tend to be (Fig. 60) (Branch, 1976 and unpub.). This is circumstantial evidence that
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
competition may force specialization. As Choat & Black (1979), however, point out, competition is not a
likely explanation for the occurrence of specialized limpets on large host algae. While North American
and South African shores are rich in limpet species and
both have specialists algal-dwelling species, so too does
the British coast with its small number of limpets.
Choat & Black ask why in certain parts of the world
macroalgac that seem suitable are not colonized by
limpets. Occupation of a host plant may require certain
specializations such as a rapid turnover to keep up with
the rate of algal mortality. Some algae may produce
chemicals inhibiting settlement. In this context P.
compressa seems restricted to Ecklonia maxima despite the occurrence of Laminaria pallida in the same area:
the latter has very few epiphytes and is suspected of chemically preventing settlement C. L. Griffiths &
J. C. Allen, pers. comm.) Choat & Black also suggest that intense fish predation may prevent a limpet
specialist from cvcr becoming established on laminarians in certain areas. Thus, the relative number of
coexistent limpet species does not relate to the incidence of obligate limpet-algal associations, and we
have no ready alternative explanation why some areas support such associations while others do not.
Only Nicotri (1977) has tried to quantify dietary differences in relation to microalgae, and found that
certain diatoms were “preferred” over others because they are chain-forming and form an overstory
covering the other diatoms. Accessibility, therefore, determines which diatoms are eaten, and Nicotri
could find no differences between the diatoms eaten by three different acmaeids. Thus, at the microalgal
level there is no indication that limpets can apportion their food to reduce competition. This is perhaps
to be expected, as microalgal grazers tend to be generalized and opportunistic in their diets. Even in the
case of limpets having very different diets, competition can still occur. For example, Siphonaria spp. often
eat macroalgae, yet the microalgalgrazing Cellana tramoserica outcompetes them (Creese, 1978).
Murphy (1976) has suggested character displacement of enzymes may be important in reducing
competition. Recording the frequency of allozymes of the leucine aminopeptidase (LAP) locus, he found
that in generalist acmacids that may coexist, the frequencies werc displaced so that the species differed
considerably
(Fig. 61A). On the other hand, specialized species occupying unique habitats and, therefore, overlapping
with no
other acmaeids all had very similar LAP frequencies (Fig. 61B). Moreover, if Collisella digitalis and C.
scabra
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
were compared, their LAP frequencies were more
similar when the limpets were isolated that when
they
occurred
displacement
together
may
occur
(Fig.
in
61C).
Thus,
response
to
competition, although until more is known about
the significance of LAP frequencies we cannot
speculate on the ecological importance of this
phenomenon. Murphy (1978) has also described a
sibling species of Collisella digitalis, C. austrodigitalis,
recognizable largely on the basis of LAP
frequencies.
Segregation of mierohabitats has also been
suggested as a mechanism allowing coexistence of competitors. C. scabra and C. digitalis compete for
food, but C. scabra tends to occur on horizontal surfaces and homes rigidly while C. digitalis occupies
vertical surfaces, migrates up and down the shore seasonally and is more abundant where wave action is
strong (Haven, 1971; Collins, 1976, 1977). Cellana radians capensis and Patella concolor occupy the same
vertical zone and have the same generalized diets, but Cellana r. capensis predominates on bare dry rock
and Patella concolor in wetter often sand-covered situations. Consequently, their numbers tend to be
inversely correlated when small areas are sampled (Branch, 1975d, 1976).
Morton (1980) has recognized that Patelloida lampanicola and P. pygmea are separate species, although they
have often been put together. P. lampanicola occurs mainly on the shells of Batillaria spp. although it can
also be found on rocks; Patelloida pygmea is nearly always confined to rocks. Each species selects its
preferred substratum if given a choice. Both live in sheltered bays and lagoons, where hard substrata are
in short supply, being limited to shell and rocks on the surface of the soft sands. Morton suggests that
niche segregation has led to specialization of the two species, implying that competition has forced
segregation. At present there is no evidence that the two compete for substrata, or ever have. As only
0.24% of the Batillaria shells carry Patelloida lampanicola, competition for shells is unlikely.
The chiton Mopalia mucosa and Collisella pelta have similar diets and Mopalia reacts aggressively towards
the limpet (see above). Collisella pelta however, feeds at night while awash or exposed at low tide, while
Mopalia moves at night but only when submerged. Connor (1975) proposes that this difference
temporally separates the species. If competition between the two were based solely on exploitation of a
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
common food, this temporal difference would have little significance, but as there is an element of
interference, feeding at different phases of the tide may reduce contact and minimize this interference.
In all cases where segregation of microhabitat, dietary differences or temporal separation are known to
occur between species, competition needs to be proved before we can consider whether these
differences have any significance in reducing competition and allowing coexistence to continue.
Unfortunately it is too easy to argue from a historical standpoint: that because two species apportion a
resource, they must do so because they originally competed. Circularity then creeps into the argument,
for the apportionment is often held to eliminate the competition that caused it in the first place!
Although theoretically this is possible, I would contend that if apportionment is caused by competition,
it will not continue unless the compctition also continues (even at a reduced level). We should be able to
test for this before jumping to conclusions.
A different approach to competition has been to suggest that compctitivc exclusion will occur unless
there are continual disturbances preventing the dominant from monopolizing the habitat (Dayton,
1971). Paine (1974) regards predation as one of the key forms of disturbance and showed that if the
starfish Pisaster ochraceus is experimentally removed mussels take over the habitat, reducing diversity. In
one experiment Mytilus californianus expanded its range to displace 25 species of invertebrates and algae,
including three aemacids that occurred at densities of 37-57.m-2 in control areas.
On the other hand, competition is clearly demonstrable and important in natural populations, so
predation cannot be controlling community structure in all cases. Underwood (1978b, 1979) has drawn
attention to the fundamental difference between mobile herbivores and sessile organisms in terms of
competition. Herbivores usually compete for food which is renewable, and they are mobile, which
allows escape from predators, movement away from areas where food is short, and emigration to
replace populations that are eliminated. Sessile forms compete for space, which is an absolute and
nonrenewable resource in the sense that once it is occupied no other animal can use it unless the
occupant is eliminated. Thus, it is understandable that mussels may monopolize a habitat unless they are
preyed upon, while limpets are more often controlled by competitive interactions.
Given that competition between limpets is frequent, how is coexistence between competitors
maintained? One important factor is the spatial heterogeneity of rocky shores. For instance, Creese
(1978) has shown Patelloida latistrigata nearly always occurs among barnacles, and that in the absence of
barnacles, survival of P. latistrigata declines (Fig. 62) because Cellana tramoserica is able to move in, and
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
outcompetes the smaller Patelloida latistrigata. Thus, P. latistrigata is small enough to survive amongst
barnacles while the larger Cellana tramoserica cannot exist
there.
A second factor is that some species have a refuge in time or
space, beyond the influence of the dominant competition. C.
tramoserica occurs subtidally as well as intertidally while its
superior competitor, Nerita atramentosa is only intertidal.
Thus, recruitment of intertidal Cellana tramoserica could always occur from the subtidal population
(Underwood, 1978b). Similarly Siphonaria could be excluded by competition with Cellana tramoserica, but
can coexist by using patches of macroalgae that cannot be eaten by this species, and even by eating the
microalgae growth on the shells of C. tramoserica (Creese, 1978). A further important point arising from
the experimental work of Creese and Underwood is that intraspecific competition may be more intense
than interspecific competition, so that although C. tramoserica is theoretically capable of excluding
Siphonaria spp., it never actually achieves the densities necessary to do so.
Finally, several authors have stressed the unpredictable nature of recruitment, particularly in species with
pelagic larvae. Dixon (1978), Underwood (1978b), and Creese (1981), give examples of year to year
variability in limpet recruitment, and Bowman & Lewis (1977) provide long-term evidence of this in
Patella vulgata. The result is that even if one species locally excludes its competitor, spatial and temporal
variability in recruitment make it most unlikely that this will occur throughout the competitor’s range, or
repeatedly ycar after year.
As a parting thought, we should not automatically conclude that all organisms sharing a resource are
necessarily competitive, or even if they are, that this does not mean that they also depend on one
another. Ayling (1981) has shown that the numbers of herbivorous gastropods (including Cellana
stellifera) are positively correlated with those of a herbivorous urchin; far from competing, they depend
on the urchin to clear surfaces that are suitable for the microalgal grazers. Similarly, although high
densities of C. tramoserica have an adverse effect on the herbivorous starfish Patiriella exigua, low densities
of this limpet may be necessary to stop macroalgae from covering the rock face (which P. exigua is
unable to prevent), and thus maintain a surface on which the starfish can graze most effectively (Branch
& Branch, 1980). Barnacles are normally adversely affected by limpets (see above), but in the absence of
limpets macroalgac develop and settlement of barnacles is prevented (e.g. Southward & Southward,
1978). Thus there may be a balance between competitive and cooperative interactions.
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
EPIZOIC LIMPETS
A surprising number of limpets live epizoically on the shells of other animals. These include species of
acmaeids and patellids that live there, possibly incidentally, as juveniles and then migrate onto the rock
face as they get larger (Branch, 1971, 1975b; Brewer, 1975). Other species spend their entire lives on
other animals or at the least their juveniles are obligate epizoics (see Table VIII).
In most cases only a single limpet
occurs on each host (Branch, 1971;
Creese, 1978), one exception being
Collisella asmi in which there is a greater
frequency of two limpets per host than
expected
(Brewer,
1975).
C.
asmi
frequently changes host shells, only
40% remaining on one host for more
than 13h (Eikenberry & Wickizer,
1964). Patelloida insignis also exchanges hosts regularly, moving directly from one shell to another, and
showing no preference for ‘new’ hosts as opposed to those that have recently been vacated by another
P. insignis (Creese, 1978). P. lampanicola is more faithful to its host but, during winter, the hosts are
abandoned as they burrow into the mud (Morton, 1980). Patella longicosta juveniles remain on a single
host, their shells conforming accurately to the host and a home scar being established. Patelloida
nigrosulcata occupies one host, again forming a scar on the shell. It shows a strong preference for certain
sectors of the shell, 97%, occupying a lateral position, just posterior to the shell apex. This coincides
with the minimum curvature of the host shell (Branch, unpubl.).
Where tests have been made, epizoic limpets show a strong preference for their own host species.
Collisella asmi selects live Tegula funebralis in preference to animals with alcohol treated shells or to
uninhabited shells. Fresh shells that contain hermit crabs are, however, equally acceptable. It seems that
there is some substance on the fresh shells that is detected on contact by a process of trial and error
(Alleman, 1968). Patelloida insignis also selects live hosts in preference to dead shells, and live control
shells rather than those that have been scrubbed with sulphuric acid, and prefers shells that have been
kept in the light to those kept in the dark (presumably because algal growth is greater in the light)
(Creese, 1978). P. lampanicola prefers its host Batillaria to rocks, while the non-epizoic Patelloida pygmaea
reverses this preference (Morton, 1980).
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
For a grazing limpet the advantage of an epizoic life is that the food supply is largely untouched by other
grazers. On the other hand, it may be very limited, necessitating regular changes of shell. As described
above (p. 283) estimates of the production rate of algae on Tegula and of consumption rates by Collisella
asmi lead to the conclusion that up to 7 % of the alga is eaten each hour, so that the regular changes of
shell are not surprising. On the other hand, the production rate of Ralfsia expansa on the shells of Oxystele
sinensis almost exactly balances the energy requirements of juvenile Patella longicosta so that it can remain
faithful to one host (Branch, unpubl., and see below). Creese (1978) suggests that Patelloida insignis is
protected from desiccation by its position on the ventral surface of Austrocochlea. Specimens placed on
bare rock rapidly died while those in pools, or control animals on Austrocochlea, survived. Finally the
rapid escape rcsponses of some of the hosts from predators may also be an advantage to the epizoic
limpets. For instance, Oxystele sinensis has a marked reaction to starfish predators and moves about 17
times faster than its epizoite Patella longicosta (Branch, 1971 and unpubl.).
There are, of course, limpet-like forms that are epizoic for more obvious reasons. Hipponix spp. feed on
scraps of food left by their hosts, and possibly on host faeces, and move their scar on the shell to retain
position near the edge of the shell (Hartley, 1958). Capulus spp, are semi-parasitic, drilling through the
host’s shell and inserting the proboscis to suck away the bivalve host’s filtered food (Orr, 1962;
Thorson, 1965).
ALGAL-LIMPET INTERACTIONS
Restriction of algae by limpets
The ability of limpets to prevent macroalgae from developing is well known, and was spectacularly
demonstrated by the stripping of Patella vulgata froni a l0 x 110 m stretch of shore on the Isle of Man
(Jones, 1946, 1948; Lodge. 1948). Green algae bloomed initially and were then followed by Fucus spp
which formed dense stands. Others have shown similar results although the problem of excluding
limpets and other grazers was not completely overcome and the outcome less spectacular (May, Bennett
& Thompson, 1970; Luckens. 1974). Boney (1965) and Hay (1979) showed that Fucus and Durvillei can
develop higher on the shore than normal, if limpets are removed.
Following dense algal growth, Patella vulgata settles in large numbers under the canopy, where desiccation
is no threat and there is an abundance of food. These limpets then prevent further recruitment of
macroalgac bx eating sporelings, and may also eat the holdfasts of the Fucus so that the original
condition is eventually restored. During this cycle barnacles sufler being unable to settle under the algal
canopy (Southward, 1956, 1964a,b) After oil spills, and particularly if toxic emulsifiers are used to clean
the shore an identical sequence occurs; the elimination of limpets allows first the greci and then the
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
brown algae to establish themselves. Southward & Southward (1978) have summarized this effect and
the literature relating to it, and proposed that there is a local cyclic relationship between limpets and
Fucus dense stands of Fucus promote limpet settling and growth, with consequence reduction of the
Fucus stand so that limpet recruitment declines, allowing further settlement of Fucus. In wave-washed
areas the cycle favours limpet, in calm areas Fucus is favoured (Fig. 63A). As Thompson (1980) describes
in areas of intermediate wave action the cycle is more obvious and local patches of Fucus escape grazers,
to develop and be eliminated. The effect of oil pollution is to exaggerate this cycle both in space and
time (Fig. 63B), an as Southward & Southward (1978) describe, the annual nature of recruitment and the
high longevity of the participants may cause the imbalance to last for many years.
Goss-Custard, Jones, Kitching & Norton (1979) have shown a similar effect in tide pools, removal of
Patella vulgata allowing Ulva to flourish McQuaid (1980) documents the dramatic influence Patella cochlear
has on algae. As on most shores, algal biomass and diversity increase from the high-shore downwards,
but in the P. cochlear zone at the low-water spring tide level, both algal biomass and diversity plummet.
Removal of P. cochlear allows establishment of a rich algal community (Branch. 1975b and unpubl.).
The dense algal growth that often develops on limpet shells when the surrounding rocks are devoid of
algae also testifies to the importance of limpet grazing: their shells are often the only ungrazed area
(Bouxin, 1964; Branch, 1975e). Experimental work on Cellana tramoserica (Branch & Branch. 1980)
incidentally revealed a further development of this pattern; animals in high-shore pools that were kept in
roofed cages developed dense growths of Ulva on their shells, while on those that were not shaded Ulva
failed to develop, or formed only stunted growths. This confirms Underwood’s (1980) contention that
while limpet-grazing may prevent growth of Ulva and Enteromorpha in the mid- and high-shore, physical
factors (in this case light intensity, since the algae were in pools and desiccation was of no consequence)
stunt growth.
Different species of limpet have different effects on algal growth. While Cellana tramoserica completely
suppresses development of macroalgae (Creese. 1978; Branch & Branch, 1980), Siphonaria spp are often
unable to do so (Creese. 1978). In part this is due to their different methods of feeding (see above), but
a more important general principle also emerges. Low on the shore algal growth is fastest (see Fig. 45, p.
334). Thus high on the shore limpets have no difficulty in preventing algal development; lower down a
point is reached where algal growth outstrips the grazing of most limpets.Creese demonstrated this for
Patelloida latistrigata, which keeps the rock clear of algae in the mid-shore region, but is incapable of doing
so in the algal turf zone further down the shore, even when it has the advantage of being transplanted
into a cleared patch. Some species are more effective in the low shore, as for example Patella cochlear,
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
which by virtue of its remarkably high densities
can exclude virtually all algae from the low water
level (McQuaid, 1980, and see above). In this
instance, however, the algal stands that develop
after removal of P. cochlear are much more
long-lived than in the cycles of Fucus-Patella
vulgata, and P. cochlear can be excluded from
these areas for more than 10 years (Branch,
1975b and unpubi.). Some limpets depend on
other grazing organisms to prevent macroalgae from developing, and the reliance of Cellana stellifera on
the herbivorous urchin. Evechinus chloroticus (Ayling, 1981) has been discussed above (p. 355).
Limpets also have a major effect on the abundance of microalgae. Castenholz (1961) caged Collisella
digitalis at various densities and showed that it kept the upper shore free of diatoms, even at densities
well below those normally present in the high-shore. Interestingly, limpets caged lower on the shore
(below their natural level) migrated to the top of their cages and only grazed this section; diatoms
developed thick mats over the lower parts of the cage, as they did in limpet exclusion-cages at all levels
of the shore. This behavioural response is interesting, for C. digitalis is migratory, and in this instance
gives the appearance of trying to migrate back up to its original zone, in spite of there being abundant
diatoms for them to feed on in the lower zone where they were caged. Nicotri (1977) also showed that
three acmaeids reduce diatom standing stocks, although they are not able to over-ride the seasonal
pattern of growth in thediatoms. Blue-green algae were scarcely influenced by the limpets, but diatom
diversity decreased as the readily available chain-forming species were removed.
Co-evolution
While limpets graze algae, some species of algae seem to
depend on the limpets. This is most obvious in the
territorial limpets (see below) but there are other cases.
Steneck (1977, 1981) has unravelled the relationship
between Collisella testudinalis and the encrusting coralline
Clathromorphum. Collisella testudinalis preferentially grazes on
Clathromorphum, although in its absence will eat other
crustose corallines. Unless Clathromorphum is grazed by this
limpet it is overgrown by epiphytic algae and diatoms and
dies (Adey. 1973) (Fig. 64). It seems likely that Lithophyllum
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
similarly depends on Patelloida corticata (Raffaeli, 1979) and Patella cochlear (Branch, 1975b) to prevent
overgrowth or smothering. Lithothamnion is the exclusive food plant of Patelloida virginea (Clokie &
Norton, 1974) and may also depend on it in this way. Clathromorphum is morphologically modified to
tolerate limpet grazing. It has a unique multi-layered photosynthetic epithallus that lies over the
meristem (Fig. 64) preventing limpets damaging the vital growth point, and its reproductive conceptaces
are sunken to avoid grazing. The rate of epithallus growth is approximately equal to the grazing rate of
Collisella testudinalis at normal densities. In turn, C. testudinalis has a specially modified radula with a
reduced number of teeth that are mounted at right angles to the radular ribbon and can thus exert a
maximum force onto each of the two cusps. The tough nature of the coralline presumably demands this
adaptation. Thus both species are co-evolved and interdependent.
Farrow & Clokie (1979) and Clokie & Boney (l980) describe how grazing organisms such as Patelloida
virginia may graze away the surface layers of shells and other ealeareous substrata, in the process
removing the Conchocelis phase of algae such as Porphyra which bores into shells. At the same time the
boring habit of the Conchocelis protects it against superficial grazers, and indeed grazing may be necessary
to prevent incrustations from reducing light penetration to the algal filaments.
Slocum (1980) has suggested that the heteromorphic alternation of generation displayed by many algae is
an adaptation to different degrees of grazing. She eliminated herbivorous gastropods, (of which Collisella
digitalis was the most important), from experimental strips on the shore, and found that the upright
frondose form of Gigartina papillata increased while the crustose form declined. Slocum proposes that
the heteromorphic life cycle is a form of “bet-hedging”: the frondose form grows faster and is not
overgrown, but is vulnerable to grazing; while the crustose form depends on a certain level of grazing to
prevent overgrowth by epiphytes. Thus the two forms are adapted to different intensities of grazing.
The limitation of limpets by algae
As stated above, in the lower shore algal growth may be too rapid for limpets and other grazers to
prevent the establishment of algae. Intuitively it might be expected that a greater algal growth will
support a higher biomass of herbivores, but in fact herbivore biomass usually declines sharply in the
algal turf zone (see Fig. 45, p. 334) (Black et al., 1979). Underwood (1980) and Underwood & Jernakoff
(1981) have tried transplanting Cellana tramoserica into cleared patches in the middle of Ulva stands and
find that in the midst of a seeming abundance of food, Cellana tramoserica declines in body weight and
suffers high mortality. Evidently it depends on a bare rock surface to obtain its microalgal food. Creese
(1978) found that if Patelloida latistrigata is placed in cleared patches in the algal turf zone it is soon
smothered by Ulva, and he suggests algal growth may set the lower limit of zonation on this species.
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
This is an important point, for while it has been readily accepted that limpets may set upper limits on
algal zonation, the reverse case also seems to be true. Goss-Custard et al. (1979) showed that removal of
Corallina from low-shore pools allowed Patella vulgata to invade these pools. Bastida, Cappezzini & Torti
(1971) record Siphonaria lessoni forming a “front” at the upper edge of the algal zone, and despite intense
grazing, algal growth and re-population were high enough to keep the limpets at bay. Using floating
rafts, Bastida et al. lowered the position of the algal zone and showed that S. lessoni then migrated down
to this new deeper zone. Thus, the lower limit of this species is also set by macroalgal growth. Patella
cochlear can also be excluded from its normal habitat if algae are allowed to develop there (see above).
Algae may also have more indirect effects on
linipets. Underwood (1975b. 1976a,b) analysed the
spatial distribution of a number of gastropods by
recording the frequency with which they occurred
on particular substrata, relative to the abundance of
each substratum. He showed that Cellana tramoserica
has a preference for water but occurs less often on
Hildenbrandia
(identified
as
Peyssonella)
than
expected (Fig. 65). He placed 50 Collisella tramoserica
on bare rock and another 50 on Hildenbrandia and
recorded, respectively, 84% and 52% survival after
one high tide, leading to the suggestion that the
Hildenbrandia is a less suitable substratum for attachment of the limpet in the face of wave action.
Simpson (1976) recorded lower numbers of Nacella (Patinigera) macquariensis in the Durvillea zone and
showed that removal of this kelp was followed by a rapid increase in numbers of the limpet. As
Durvillea forms a canopy, under which surfaces suitable for limpet grazing are present, Simpson
suggested that the whip-lash action of wave-driven Durvillea fronds is what normally excludes limpets:
either by dislodgement, or, more likely, by interfering with feeding excursions.
Limpets living on macrophyte hosts
Obligate relationships between limpets and particular species of large plants are well known and include
a number of acmaeids such as Notoacmea insessa on Egregia laevigata (Black, 1976), Scurria scurra on kelps
(Vermeij, 1978), Notoacmea paleacea on Phyllospadix, Collisella instabilis on various brown algae, and N.
depicta and C. alveus on Zostera (Bishop & Bishop, 1973; Carlton, 1976). Of the patellids, Helcion pellucidus
occurs on Laminaria spp. (Graham & Fretter, 1947; Kain & Svendsen, 1969; Vahl, 1971, 1972), and
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
Patella compressa on Ecklonia maxima (Stephenson, 1936; Branch, 1975c). Among the siphonariids, only
Siphonaria compressa, which occurs on Zostera capensis, is restricted to a macrophyte (Branch, unpubl.). Shell
shape is often modified in these limpets to allow a close fit to the plant. The shell of Patella compressa is
long and narrow and compressed laterally so that in adults the shell wraps around the stipe of the kelp
(Branch, 1975c). Notoacmea depicta has a very narrow shell when it lives on Zostera, but has a broader fiat
form that probably lives on large brown algae. This latter form was originally described as Acmaea
(Notoacmea) gabatella and is common in Pleistocene deposits but is now very rare (Lindberg, 1980).
Notoacmea palaeacea has a similarly narrowed shell for life on Phyllospadix, and bears a notch in the shell
allowing exhalant respiratory and cleansing currents to leave the mantle (Yonge, 1962). The shell shape
and number of notches vary depending on the species of Phyllospadix that is inhabited and the locality
(Fishlyn. 1976). Shells of plant-dwelling limpets are often more streamlined than those of rock-dwellers,
as the plant sways away from the current and the direction of water movement is thus predictable
(Warburton, 1976).
Few of these stenotopic plant-dwelling limpets have been studied in detail, but striking adaptations of
the life cycle have been revealed in two species. Helcion pellucidus may settle randomly on rocks and algae,
but only those settling on laminarians survive. Growth is extremely rapid and the limpets become
reproductive at a size of only 5 mm.
Laminaria fruits in spring and autumn, and the distal part of the frond disintegrates after this. As the
limpets settle mainly after spring, it is the autumn disintegration that is critical. Graham & Fretter (1947)
suggest that they migrate down the frond to its base (to avoid being cast off), possibly relying on some
chemical change in the frond to trigger this migration. A small proportion migrate down to the holdfast,
where they can be encapsulated right inside the hold-fast, with resulting distortion of the shell. These
limpets are referred to as form laevis.
On the Isle of Man, Helcion pellucidus behaves in a similar way on Saccorhiza polyschides, but in Norway
although the limpets may move towards the base of the frond after spawning, and hence reduce their
losses as the old blade is sloughed off, none of them migrates down the stipe to the holdfast (Kain &
Svendsen, 1969; Vahl, 1971, 1972). The rapid growth and early sexual maturity of this species, and of
Notoacmea insessa, are surely adaptations to the relatively short life of their host plants (Choat & Black,
1979, see above).
Black (1974, 1976) has uncovered a more intricate relationship between N. insessa and its host, Egregia.
Egregia is essentially annual, and the main settlement of Notoacmea insessa is slightly after that of Egregia,
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
allowing it to live as long as possible before loss of the Egregia occurs. Notoacmea insessa forms deep
depressed scars on the main rachis of the alga, which weaken the plant and make it more likely to break
during storms. This may, however, be an advantage to the plant, for the existence of this weak point
prevents the whole plant from being ripped off the rock. Furthermore, the loss of a main rachis can be
compensated by development of branch rachises. Damaged plants eventually develop sporophyllbearing rachises that are just as long as in plants that are not grazed. Thus, the reproductive potential of
the plant is unaffected by loss of the main rachis. Small limpets are more common on stipes carrying the
scars of older limpets. This would seem to be a poor choice for the chances of the plant being lost must
be high, but Black (1976) has shown survival and growth are greater injuveniles occupying old scars.
This pattern of settling in old scars concentrates the limpets on older (post-reproductive) plants.
Furthermore, the limpets avoid the growing meristem of the alga. Thus the potential damage that could
be done by limpet grazing is minimized, partly because of the behaviour of the limpets, and partly
because of the response of the alga to grazing or loss of the main rachis. Scurria scurra affects Lessonia
similarly (Santelices et al., 1980).
An analysis of the energy budget of Patella compressa reveals that its energetic requirements are vastly
exceeded by the production rate of its host plant, Ecklonia maxima (Branch. 1980 and unpubl.). The
question thus arises why the adults should be territorial and spaced out, one per stipe. (Branch, 1975c).
It may be that spacing the adults reduces grazing damage to the stipe and thus increases the survival of
kelp plants. The kelps are, however, often torn free in strong storms, and Patella compressa almost
immediately abandons plants that break free and rise to the surface (Branch, 1971). Unlike Egregia,
Ecklonia cannot grow again from broken stipes so there is no advantage in having a weak point that
breaks before the whole plant is torn off the substratum. Ecklonia is also a much longer lived plant, so
that Patella compressa is not as dependent on continual recruitment and rapid growth to sexual maturity.
Thus in various ways the behaviour and life cycles of plant-dwelling limpets are modified in relation to
their specialized habitats, and in two cases they also act as “prudent” predators, reducing the damage
they could otherwise do to their hosts.
Territoriality and algal-limpet interactions
Stimson’s (1970, 1973) work on Lottia gigantea shows quite clearly that territorial defence by this limpet
maintains an algal film that would otherwise be invaded and eliminated by other limpets. Patella longicosta
and P. tabularis are perhaps even more specialized, defending a particular species of alga. Ralfsia expansa.
Patella cochlear also has specialized fringing gardens of red algae (see Fig. 49B, p. 339). The life cycles of
these Patella spp. have already been discussed. One other candidate that may be territorial is Patella
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
laticostata, although definite proof is lacking. P. laticostata has fringing algal patches that resemble those of
P. cochlear, although they are not nearly as clearly defined. One of the common algae associated with P.
laticostata is Herposiphonia, which also occurs in Patella cochlear gardens. P. laticostata nearly always occurs
singly on these algal patches, and many of the algae in the patch are not found elsewhere on the shore.
On the single occasion when two animals were found on the same patch they were locked together,
suggesting a territorial contest (Branch, unpubl.). These conditions are suggestive, but more work is
required on this species. Interestingly, a second species, Patelloida nigrosulcata, occurs on the shells of
Patella laticostata, also singly, and also associated with a specific filamentous green alga which is largely
confined to the area grazed by this limpet (Branch, unpubl.). Recalling that Stimson (1970) showed the
amount of alga left behind by grazing limpets was directly related to the size of the limpet (see above), I
speculatively suggest that the size of the limpet and the manner in which it grazes are key elements in
determining what types and quantities of algae are allowed to develop in the vicinity of a limpet. Some
algae may tolerate closer or more frequent cropping, or may even depend on this cropping to exclude
other species that are superior competitors.
An analysis has been made of the energy budget of Patella longicosta (see Fig. 35, p. 316) in relation to the
production rate of Ralfsia (Branch. 1980, and unpubl.). This reveals that the two coincide closely. Thus
territorial defence is necessary to conserve this limited but dependable food supply. If Patella longicosta is
removed from its garden, one of three things may happen, depending on local conditions. If young P.
longicosta which lack gardens of their own (“floaters”) are nearby, one will almost immediately take over
the garden, even occupying the vacated scar. The garden is then maintained by the new occupant.
Failing this, other grazers may move in and slowly eliminate the garden, or adjacent frondose algae may
overgrow the Ralfsia (Branch, 1971, 1976). Crustose algae never overgrow Ralfsia which may have
antibiotic properties that inhibit the growth of other algae (Fletcher, 1975). The grazing pattern of Patella
longicosta is also unique among patellids and
essential to the maintenance of the Ralfsia
garden. Whereas most limpets swing the head
from side to side, thus grazing on all algae in
their path. Patella longicosta cuts regular paths
through the Ralfsia, and these are spaced out so
that the alga is never eliminated (see Fig. 48B. p.
338). Two important consequences arise from
this. First, the rate of algal consumption is
somehow linked to the number of paths that are
cut across the garden. If animals are introduced
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
into a Ralfsia patch that has no paths, the rate of grazing is fast until paths are established, and the limpet
tends to avoid grazing over areas that have had paths cut. Thus overgrazing and elimination of the alga
does not occur. Secondly, Ralfsia grows more rapidly around the edges of the encrusting growth, so by
cutting paths, Patella longicosta effectively creates more ‘edges’ and increases the productivity of the alga.
This effect can be experimentally demonstrated by cutting paths through an ungrazed Ralfsia (Fig. 66);
the subsequent productivity is about 30% greater than in untouched controls (G. M. Branch & B. Broll,
unpubl.). Thus in this case limpet and food plant are interdependent and the behaviour of the limpet
tuned to maintaining its food-plant.
An important issue has arisen from this study: that
the zonation of a limpet may be regulated by the
productivity of its food plant. In most cases this is
not easy to quantify, but measurements on Ralfsia
show that its biomass and its growth rate decline
upshore (Fig. 67). As the energy requirements of
Patella longicosta are finely balanced against the
production of Ralfsia, the latter will be too low in the
high-shore. So although Ralfsia occurs as high as the level of high-water neaps, Patella longicosta fails to
penetrate as far up the shore. This may also be the reason why P. tabularis, which also defends gardens of
Ralfsia, is limited to the subtidal zone, for it has much greater energy requirements than Patella longicosta
(G. M. Branch, unpubl.). P. cochlear is remarkable in that it lives at very high densities, and I have
suggested that these densities are necessary to exclude other limpets and, more important, to prevent
macroalgal growth (Branch, 1975b). This does not explain how they manage to survive at such high
densities. Their gut contents contain practically only calcareous material, leading me to suggest initially
that they feed mainly on Lithophyllum. A more recent analysis of the energy budget of the limpet (Branch,
1980 and unpubl.) shows, however, that the requirements of Patella cochlear could never be met by the
production rate of Lithophyllum (Fig. 68). Each limpet is
surrounded by a fringe of red algae (Stephenson, 1936)
and this is territorially defended (Branch, 1975b,c,
1976). Removal of Patella cochlear results in an initial
dramatic growth of the garden (Bokenham, 1938;
Branch, 1971) which can be used as a measure of the
production rate of the alga, assuming that P. cochlear
normally grazes the garden away at this same rate to
maintain it at a constant level. This reveals that the
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
production of Herposiphonia in these gardens closely matches the energy requirements of Patella cochlear
(Fig. 68) (Branch, 1980, and unpubl.).
Thus the very high densities maintained by P. cochlear are dependent on the relationship they have with
highly productive gardens of red algae. Estimates of the potential productivity of these algae range from
48000 to 86000 kJ.m-2.yr-1, putting them on a par with kelp forests: an astonishing production
considering their small size (Branch, unpubl.). Of course, the realization of this production is due largely
to the continual cropping by P. cochlear. In addition, the gardens depend on P. cochlear for their
maintenance, being grazed away or overgrown within 4 to 9 weeks if the limpets are removed. Both P.
cochlear and P. longicosta have slow growth rates and low reproductive outputs (see above) and I suggest
that these patterns have been evolved in response to the limited but reliable food source available in the
territorial gardens.
COMMUNITY STRUCTURE, CONTROL OF LIMPET POPULATIONS, AND ENERGY FLOW:
A SUMMARY
From the preceding sections it is clear that limpet populations may be regulated by a variety of factors,
and in turn may have a strong influence on the nature of the community.
Intraspecific competition may limit population density by density-dependent mortality, by modifying the
success of recruitment or by influencing the rate of emigration in relation to food availability. This third
process seems most important in mobile migratory species such as Collisella digitalis, Cellana tramoserica,
and Patella granularis, while mortality has only been known to be related to density in species that occupy
a fixed site for most of their lives, such as P. cochlear and Notoacrnea petterdi.
Interspecific competition may also regulate limpet populations. Exploitation of a food source may
reduce growth rate or restrict the zonation or distribution of a species. One species may hamper the
recruitment of another by grazing newly settled juveniles. In some cases interference competition is
important, territorial defence locally excluding some species from defended areas or specific algal
patches. The more generalized interference between Cellana tramoserica and Patiriella exigua is associated
with a spatial segregation of the two species and probably contributes to a reduced growth of the latter
species. Territoriality has even resulted in the evolution of avoidance behaviour in intruding limpets,
reducing the chance of dislodgement by the territorial limpet.
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
Limpets may influence the success of barnacle settling, reducing survival of recruits; but at the same
time are often necessary agents preventing macroalgal growth which can totally preclude barnacle
settling. Conversely, barnacles may decrease limpet settling; increase survival of small limpets and
adversely affect growth and survival of larger limpets.
Mussels seem largely immune to limpets and only the larger territorial limpets are capable of slowing or
halting the encroachment of mussels. Small limpets may live on mussels or oysters; very large limpets
may exclude them; but as Choat (1977) points out, intermediate sized limpets seem to suffer most from
sessile organisms. Regulation of mussels by predators has been shown to be important in maintaining
limpet populations.
The most dramatic effect limpets have on community structure is their influence on algal species
composition and growth. Almost total exclusion of algae from the mid to upper shore is frequent, and
even at the low-tide level species such as Patella cochlear can radically reduce algal diversity and biomass.
On the other hand, in most cases algal growth in the low-shore is great enough to exclude limpets that
feed on microalgae. On a smaller scale, territorial limpets may maintain particular algae that are
otherwise rare or even absent from the shore, and in some cases co-evolution of alga and limpet has
resulted in an intimate interdependence.
The question of whether competition is important in regulating communities, or whether predation or
some other form of disturbance is necessary to prevent competitive monopolization of a habitat, is
largely resolvable by distinguishing the nature of the species and the nature of the limiting resource
(Underwood, 1978b). Sessile, space-occupying species may need to be controlled by a predator; mobile
herbivores such as limpets are more likely to compete for food, and for them, competition is known to
regulate population density and distribution. Despite this, coexistence between competing herbivores
continues, permitted by a number of factors including spatial heterogeneity, spatial and temporal
refuges, behavioural responses, specialization of diet or microhabitat, unpredictability of recruitment,
and the possibility that competing species may also depend on one another.
Predators are clearly important to limpets, well-defined escape responses having evolved, and the
rhythmicity of feeding excursions and possession of home scars in part being devices for reducing
predation. Morphological features such as defensive glands and colour patterns are clearly adaptations to
predators. Despite this, no case is known where predators have anything but a small-scale effect on the
distribution of limpets. For instance, Collisella limatula lives under stones to reduce predation, and both
this species and Notoacmea scutum may move upshore in the presence of predatory starfish; but these
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
effects are local and unlikely to explain the distribution or zonation of limpets. On the other hand,
elimination of a predatory starfish has been shown to result in competitive exclusion of limpets by
invading mussels.
There is also an impressive array of morphological, physiological, and behavioural adaptations to
physical stresses in limpets. Of these physical factors, salinity is not known to limit the zonation of
limpets except where freshwater seepage is substantial. In estuaries, low salinity may restrict limpets
although its effect has not been separated from that of siltation. Wave action can be correlated with the
distribution ofseveral species although its precise effect is not known nor is it easily separable from
other contributing factors like the availability of food. The physical problem of dislodgement seems less
important than the decreased efficiency of feeding and the increased energetic costs of living in areas of
high wave action.
Both temperature extremes and desiccation are known to kill limpets and to set upper limits on their
zonation, but almost always this involves high-shore species or high-level individuals of a species. This
means that most species are living well within their physiological limits and their zonation and
abundance cannot be controlled by physical factors.
It was this that led Wolcott (1973) to propose that high-shore species may be flanked above by an
unexploited food source which justifies their upward movement to the limits of physiological tolerance,
even although the risk of death during deteriorating physical conditions may rise. Low-shore species
would benefit less by moving upwards, since they would encroach on the range of higher-shore species
and have to compete with them in addition to risking death from increased physical stress. Thus,
Wolcott suggests lower-shore species behaviourally regulate their zonation, well within their physical
tolerances. This behavioural regulation may relate to predation, to physical cues or perhaps to the levels
of food. Underwood (1979) has pointed out that many gastropods crawl upwards until they encounter
food, when they move randomly, or may thus set their zonation by availability of food. It is not clear,
however, how an animal that moves above its optimal zone will then return down the shore.
Two studies (Choat. l977; Dixon, 1978) have produced data supporting Wolcott’s hypothesis, showing
that a lower-shore species, Collisella strigatella will move up the shore in response to removal of a highershore competitor, C. digitalis. Despite the attractiveness of Wolcott’s hypothesis, some limpets do not,
however, conform to his proposals. Notoacmea petterdi is a high-shore limpet which would seemingly
benefit by migrating upwards (for the low density high-level individuals grow fastest) yet it does not
migrate. As it occurs very high on the shore, perhaps the advantages of movement are overridden by the
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
need to home to a fixed scar. Similarly it is puzzling why N. fenestrata does not migrate upwards, seeing
that it grows faster in the presence of a higher-shore competitor, Collisella strigatella, than it does when
kept at equivalent densities on its own. Thus despite its appeal, Wolcott’s hypothesis needs further
testing before it can be accepted.
At least four patterns of life-style are recognizable in limpets. Mid-to high-shore species are often
migratory, moving upshore or away from areas of food shortage, and are characterized by generalized
diets, competition by exploitation, and having high rates of growth and reproductive output. In the high
to extreme high-shore this pattern breaks down and species like Notoacmea petterdi are non-migratory and
occupy fixed sites, and are often slow-growing and long-lived. In the low-shore there are more species
of limpets and biological factors seem more important in regulating the species than physical factors.
Predation seems more intense (Parry, 1977), and more of the linipets have specialized diets and are
associated with particular organisms. Species with short-lived hosts or which suffer from a space
shortage are often short-lived and have high growth coefficients and high reproductive output. Others
are associated with algae that produce at a low rate and are themselves slow-growing and have a low
reproductive output.
There is a strong correlation between the production : biomass ratio and longevity, and between the
growth coefficient and longevity, although as discussed above, we cannot state which is the cause and
which the effect.
The amount of food (and the variability in that amount) may be a key issue in determining the pattern
and flexibility of growth displayed by each species. Those with abundant food may exploit this with a
rapid but inefficient turnover, associated with high losses of energy in the form of faeces, mucus, and
metabolic heat. Those with a predictably low food supply are of necessity “conservers”, minimizing
energy losses and having a low but efficient turnover of energy (Newell & Branch, 1980).
ACKNOWLEDGEMENTS
My research assistant, Mrs M. A. P. Joska, must be singled out for special thanks, for many hours of
help with the preparation of this review. Mrs Leonora Freeland accurately and very speedily typed the
manuscript, and many thanks are due to her. Many research workers generously gave of their time to
correspond with me and often to share their unpublished findings, some of which are included in this
review. In particular, I am thankful to Drs Howard Choat, Bob Black, Bob Creese, Susan Cook, John
Dixon, Dave Lindberg, Sally Levings, Stephen Garrity, Bob Steneck, Bill Wright. Peter Jernikofi. Tony
Underwood, and Ray Wells. Pierre de Baissac and Monique Delafonteine helped with French
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
translations. Finally, and most important, my wife, Margo, completed all of the illustrations, and her
patience and support were perhaps the most important ingredients bringing this review to fruition: and I
dedicate this paper to her in appreciation for many things.
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380
Reference: Branch G. M. (1981) Oceangr. Mar. Biol. Ann. Rev. 19 p235 - 380