Chapter 5

`````````````````````````````````````

Rocky Shores

R ocky intertidal habitats are home to many sessile and slow-moving in-
vertebrates, as well as algae capable of dealing with widely fluctuating
physical conditions. In contrast to soft-sediment shorelines, where organ-
isms are often buried in the substrate and thus buffered from exposure, ses-
sile and slow-moving organisms on rocky shores routinely face extreme
temperature and desiccation stresses during low tides. Rocky intertidal or-
ganisms can also be subjected to severe wave stresses that can dislodge them
from the substrate, limit their mobility, and greatly influence their size and
morphology.
Numerous advantages counter these disadvantages of rocky intertidal
habitats, however, and they typically harbor rich assemblages of algae and
sessile invertebrates. Rocky shores are bathed in plankton-rich water, and
water movement over littoral habitats typically enhances the delivery of
particulate food to filter-feeding invertebrates. Moreover, conditions for al-
gal growth are excellent, and rocky intertidal habitats usually have high al-
gal productivity, supporting large herbivore and carnivore populations.
Rocky intertidal habitats have been particularly valuable study systems
for ecologists because their strong zonation patterns and their relatively sim-
ple and easily observed communities make them especially suitable for ma-
nipulative experiments. A number of classic experiments performed in these
habitats have greatly influenced modern ecology. Work on rocky shores has
elucidated the roles of consumers (Paine 1966; Menge 1976; Lubchenco 1978),
competition (Connell 1961), disturbance (Dayton 1971; Sousa 1979a), and re-
cruitment (Gaines and Roughgarden 1985) in communities. As a consequence
of their accessibility, ecologists have paid a great deal of attention to these
habitats, and so we understand them better than most other communities.
On the east coast of North America, rocky intertidal habitats are primarily
found north of Cape Cod, where glaciers from the most recent Ice Age have
 ROCKY SHORES ` 173

scoured the shore clean of sediments. In comparison to the west coasts of

North America and Europe, rocky shores in New England and Canada have
a relatively depauperate fauna and flora. The low species diversity of these
rocky shorelines is a result of geologically recent large-scale disturbances.
Pleistocene glaciers covered the east coast of North America to southern New
England as recently as 10,000 to 20,000 years ago. Their scouring of sediments
from the shore led to the extinction of marine hard substrate-dependent or-
ganisms, since these species could not retreat to southern shorelines, which
lacked hard substrates (Vermeij 1978, 1987). Consequently, New England
shorelines have been recolonized and recovering from these local extinctions
only for the past 10,000 to 20,000 years, and are geologically very young. Se-
vere winter ice scouring has continued to occur frequently enough in Cana-
dian and New England intertidal habitats over the last few centuries to pre-
vent the reestablishment and persistence of most organisms other than the
fastest-growing, earliest-reproducing species (Wethey 1985).
In this chapter I examine the ecology of western Atlantic rocky shores. I
begin by introducing the organisms that occur on these shores, paying par-
ticular attention to the biology of the numerically dominant organisms. I
then discuss the unusually extreme physical stresses that influence the dis-
tributions of organisms in this habitat, and describe the striking zonation
of organisms on rocky shores that has long attracted the interest of marine
ecologists. I end by touching on some of the mounting conservation con-
cerns pertaining to rocky shore communities.

ROCKY INTERTIDAL ALGAE

Two sources of primary production form the base of rocky intertidal food
webs: planktonic diatoms and benthic algae. Planktonic diatoms are micro-
scopic and inconspicuous, but serve as the primary food source for the ses-
sile filter-feeding organisms, such as barnacles and mussels, that character-
ize most rocky shorelines. In contrast, the benthic algae common on rocky
shores range in size from microscopic diatoms to large seaweeds and kelps.
They are grazed by a variety of herbivores, including snails, urchins, and
fishes (Fig. 5.1).
Seaweeds are extremely productive along most rocky shoreline habitats.
The high levels of nutrients, light, and water movement that characterize
many intertidal habitats promote primary productivity. High nutrient sup-
plies in New England nearshore waters are the result of terrestrial runoff
and the nearshore oceanographic processes that bring nutrient-rich bottom
water to nearshore habitats (Mathieson et al. 1991; see chapter 2). In contrast,
the nutrient-poor, oligotrophic conditions in the nearshore waters off New-
foundland and Labrador are the result of low nutrient inputs (Chapman
and Craigie 1977). The high levels of light and water movement found in
rocky intertidal habitats also enhance seaweed productivity (Gerard and
Mann 1979; Gerard 1987; Leigh et al. 1987). The influence of light on seaweed
174 ` CHAPTER 5

Planktonic diatoms

Dytilum Stephanopyxis Navicula

Common seaweeds

Fucus Ulva Chondrus Ascophyllum

Fig. 5.1 Planktonic diatoms and benthic algae, consumed by filter feeders and
benthic grazers, respectively, are at the base of rocky shore food webs.

distribution and production is discussed in chapter 2. Water movement en-

hances gas exchange (CO2 absorption and O2 release), and by keeping algal
fronds in motion, ensures that light reaches more algal surfaces than if the
algae were stationary and constantly shading their neighbors. Seaweed mor-
phological responses to water movement, however, may also act to decrease
the surface area available for photosynthesis, and thus negate potential pro-
ductivity advantages for seaweeds in high flows.
The high productivity of seaweeds has made them a valuable resource
for human populations, which have harvested them for a variety of pur-
poses over many centuries (see Chapman 1970). In the seventeenth and
eighteenth centuries in Europe and North America, large brown seaweeds
or “kelps” were used for fertilizer and livestock fodder, or dried and burned
for potash (potassium salts), or used in pottery glazes and the manufactur-
ing of glass and soap. The word kelp, in fact, originally referred to brown
seaweeds that were ashed in large rock-lined pits near shorelines for their
potash, rather than live seaweeds. In the early nineteenth century, the
discovery of other potash sources and the high iodine content of some sea-
weeds shifted the focus of seaweed harvesting to iodine extraction. In Eu-
rope, harvesting of intertidal seaweeds was so intense that government
 ROCKY SHORES ` 175

regulation of harvesting and processing became necessary by the middle of

the seventeenth century.
The use of seaweeds for potash and iodine ended early in the twentieth
century when mining mineral deposits for these resources became more
cost-effective than processing seaweeds. Currently, seaweeds are harvested
globally for gel and emulsifier products. The common red seaweed Chondrus
crispus (Irish moss) is heavily harvested in New England and the Canadian
Maritime provinces. Irish moss is valued as a source of carrageenan, which
is widely used as a stabilizer and emulsifying agent in lotions, toothpastes,
ice creams, pie fillings, jellies, and more. Natural harvesting of Irish moss
has declined over the last few decades as mariculture techniques have been
developed to grow seaweeds under artificial conditions. Many seaweeds,
however, continue to be harvested and cultured for food, particularly in Asia.
In the Canadian Maritime provinces the abundant shallow-water brown
seaweed Ascophyllum nodosum (knotted wrack) continues to be harvested for
its alginate, a thickener used in everything from salad dressing to oil-drilling
lubricants.
In addition to serving as food sources for people and intertidal con-
sumers, some seaweeds play a vital role in intertidal communities by provid-
ing refuges from the physical stresses of heat and desiccation (Dayton 1975;
Menge 1978; Denny et al. 1985). In the Gulf of Maine, the knotted wrack (As-
cophyllum), in particular, often forms dense intertidal canopies on rocky
shores that are not exposed to direct wave shock. These canopies of long-
lived, often slowly recruiting algae buffer understory organisms from heat,
water loss, and wave forces, and they can support a rich assemblage that of-
ten would not exist in these habitats without the modifying effects of the
canopy (Bertness et al. 1999a). The overharvesting of Ascophyllum should be
conservation concern because of the large role it plays in these communities.
An important distinction to make among seaweeds, which is not always
taxonomic, is between ephemeral and leathery seaweeds. Ephemeral sea-
weeds, such as Ulva and Enteromorpha, are usually short-lived, rapidly re-
cruiting species that are easily eaten. In contrast, the leathery seaweeds,
such as Ascophyllum and Fucus, are heavier, less easily eaten, slowly recruit-
ing, and often serve as refuges for other intertidal organisms.

Major Seaweed Taxa

Seaweeds are primitive photosynthetic organisms that lack the internal water
transport systems of higher plants. They range in complexity from undiffer-
entiated sheets of cells to highly differentiated macroalgae with many of the
structural characteristics of higher plants. Seaweeds are phylogenetically
divided into three major taxa based on their photosynthetic pigments.
The green algae, or chlorophytes, utilize primarily green chlorophyll pig-
ments. Common intertidal green seaweeds include the sea lettuces (Ulva), the
filamentous Enteromorpha, and dead man’s fingers (Codium). The brown algae,
or phaeophytes, utilize special xanthophyll pigments such as fucoxanthin in
176 ` CHAPTER 5

Meiosis

Spores (1N)

External fertilization

Diploid sporophyte (2N) Haploid gametophytes (1N)

Mitosis
Young
sporophyte (2N)

Fig. 5.2 Generalized seaweed life cycle with alternation between similar
(isomorphic) diploid (2N) and haploid (1N) generations. Common examples
of seaweeds with this type of life cycle are Ulva and Enteromorpha.

addition to chlorophylls. Common brown algae include the rockweeds

(Fucus), knotted wrack (Ascophyllum), and the kelps (Laminaria). The red al-
gae, or rhodophytes, utilize phycobilin and carotenoid pigments in addi-
tion to chlorophylls, but not fucoxanthin. Common red algae include Irish
moss (Chondrus) as well as fleshy and calcareous algal crusts such as Hilden-
brandia and Lithothamnium, respectively.

Seaweed Life Histories

Seaweed life histories are highly variable, but often include an alternation
of haploid and diploid generations (in which there are one and two copies
of the genetic instructions, respectively). Typically, a diploid sporophyte
produces haploid spores through a reduction division (meiosis). These spores
develop directly into haploid gametophytes, which produce haploid gametes.
These gametes fuse to form a juvenile diploid sporophyte, which grows into a
mature adult form. Modifications of this basic scheme, however, are extensive
(Fig. 5.2).
Some common seaweeds, such as the sea lettuce Ulva and the filamentous
green alga Enteromorpha have sporophyte and gametophyte stages that are in-
distinguishable (isomorphic). Others have heteromorphic gametophyte and
sporophyte stages that are structurally and functionally different. Seaweeds
from a number of taxonomic groups alternate between fleshy erect forms (typ-
ically the sporophyte), which have high growth rates but high vulnerability to
herbivory, and encrusting forms, which are well defended against herbivores,
 ROCKY SHORES ` 177

• Rapid growth
• High reproductive output
• Vulnerable to consumers
and physical stress

• Slow growth
• Low reproductive output
• Well-defended from consumers
and physical stress

Encrusting stage

Fig. 5.3 Alternation of generations in Petalonia between a fleshy erect stage

and an encrusting stage on a snail shell.

but have low growth rates (Fig. 5.3). Examples of Atlantic coast algae with
this type of heteromorphic life cycle include Scytosiphon and Petalonia.
An interesting variation on this theme is found in the sea laver, Porphyra,
a common seaweed of New England that is a culinary delicacy used in
soups, salads, and sushi in Japan. It alternates between a fast-growing, sexu-
ally reproducing, fleshy erect blade form, found in the high intertidal zone
during the winter, and a subtidal conchocelis (shell-boring) stage that bores
into mollusc shells during the rest of the year. As was the case for many sea-
weeds with heteromorphic life histories, the conchocelis stage of Porphyra
was long thought to be a separate species (Fig. 5.4).
Encrusting or boring heteromorphic stages of seaweeds are thought to be
adaptations for avoiding herbivores and/or physical stresses (Lubchenco and
Cubit 1980; Dethier 1981). The fast-growing fleshy stages of these algae have a
high reproductive output, but are vulnerable to grazing and physical stresses,
whereas the encrusting or boring stages are slow-growing, but resistant to
grazing. On the coast of Oregon, where the fast-growing erect forms of these
algae are typically found only in the winter, experimental removal of herbi-
vores leads to erect fleshy forms persisting throughout the year (Lubchenco
and Cubit 1980). In New England, however, fast-growing fleshy forms of
many heteromorphic seaweeds can usually be found year-round.
Not all seaweeds have alternation of generations. Fucus and Codium,
two of the most common Atlantic coast seaweeds, have a more animal-like
life history. In these species, diploid adults give rise to gametes by meiosis,
and fertilized gametes develop directly into diploid adults (Fig. 5.5).
Settlement and recruitment are the least understood aspects of seaweed
178 ` CHAPTER 5

Spermatia (1N)

Fusion

Juvenile sporling (2N)

Mature form

Carpospores (2N)
Conchocelis stage Conchospores (2N)

Vegetative growth

Fig. 5.4 Alternation between the well-defended shell-boring conchocelis

and rapidly growing, upright fleshy forms of Porphyra.

life histories. Seaweeds do not have any resistant resting stages such as
hard-shelled seeds or spores for getting them through tough times (dehy-
dration, freezing, grazing), so they depend on alternating forms to escape
these problems. Algal propagules appear to be passive particles with little
control over their movement. Propagule dispersal distances, however, vary
widely (for examples see Dayton 1973; Burrows and Lodge 1950), suggest-
ing that dispersal mechanisms, propagule buoyancy, and the length of time
that propagules remain viable all influence dispersal. Intertidal fucoids have
been shown to release their gametes during low tide apparently as a mecha-
nism to enhance fertilization success (Brawley et al. 1999). It is likely that
algal settlement is strongly influenced by local hydrodynamic conditions,
with propagules accumulating in depositional microhabitats, such as pits
and grooves, but we know surprisingly little about actual algal settlement
and recruitment patterns under field conditions (see Chapman 1986 and
Vadas et al. 1992 for reviews of what is known). On New England rocky
shores grazing by periwinkle snails generally limits the success of most algal
recruits (Johnson and Brawley 1998; Bertness et al. 2002, 2004).

Seaweed Functional Groups

The sizes and morphologies of shallow-water seaweeds are influenced
by a variety of physical and biological factors. Coping with wave forces,
minimizing heat and desiccation stresses, and maximizing nutrient and gas
exchange are some of the physical challenges that affect algal design. Resisting
 ROCKY SHORES ` 179

Conceptacle magnified

Fucus adult

Sperm (1N)
Embryo

External fertilization Eggs (1N) Antheridia

(2N)
(male)

Oogonium
(female)

Fig. 5.5 Animal-like Fucus (rockweed) life cycle. Adults (2N) give rise to gametes
(1N) through meiosis. External fertilization results in young diploid plants that
grow to the adult form. The life cycle does not include an alternation of generations
as in the green algae.

consumers and competitors is also an important biological consideration.

Since dealing with any one of these problems can adversely affect the ability
to cope with others, compromises and trade-offs are apparent in algal design
(Littler and Littler 1980). The highest nutrient and gas exchange rates, for
example, are found in single-celled algae (diatoms), which have high surface-
to-volume ratios and little structural support, and in some undifferentiated
180 ` CHAPTER 5

sheets of cells like those of the sea lettuce Ulva, which is two cells thick. Maxi-
mizing gas exchange, however, leaves these seaweeds extremely vulnerable
to herbivory and physical disturbance. In contrast, seaweeds that invest heav-
ily in structural support to resist disturbance, such as kelps with long, flexible,
structurally complex stipes (or trunks) and blades, or seaweeds that invest in
antiherbivore defenses, such as algal crusts, may do so at the cost of reduced
gas exchange and slower growth. The ruffled shape of some kelp blades is
thought to increase gas and nutrient exchange (Gerard and Mann 1979).
A functional grouping of algae that reflects common morphological
solutions to these problems of design has been proposed by Steneck and
Dethier (1994). At the ephemeral end of the spectrum are the structurally sim-
ple, small, and fast-growing algal groups (microalgae such as diatoms; fila-
mentous and foliose algae such as Ulva and Enteromorpha). These are rapidly
colonizing, fast-growing algae that are typically found in recently disturbed,
early successional habitats. Other seaweeds invest more in structural features
that increase their persistence, competitive ability, and resistance to distur-
bance and herbivory; the trade-off for these species is reduced growth and
reproductive output. The structurally complex, leathery macroalgae (Irish
moss, Chondrus crispus; kelps, Laminaria; rockweeds, Fucus) provide examples
of this strategy. The calcified erect algae (Corallina) and coralline and fleshy
algal crusts (Lithothamnium and Ralfsia) represent extremes of investment in
structural defenses, resulting in extremely low growth rates (Fig. 5.6).
Steneck and Dethier (1994) suggest that the occurrence of these functional
groups can be predicted by two environmental features: the disturbance po-
tential and the productivity potential of the habitat (see Grime 1977 for a sim-
ilar model for terrestrial vascular plants). Disturbance potential is defined as
the rate of herbivore-induced or physically induced tissue loss or mortality.
Productivity potential is defined as the potential for primary productivity in a
habitat, given specific nutrient and abiotic conditions. This model thus pre-
dicts the spatial and temporal distributions of seaweeds. In habitats with low
disturbance potential and high productivity potential, long-lived, persistent,
competitively superior algal forms are dominant. Shallow, subtidal, wave-
exposed kelp bed habitats are a good example of this competitive strategy. If
disturbance potential (herbivory) is increased, but productivity potential re-
mains high, algal crusts capable of persisting under intense herbivory domi-
nate (the disturbance-tolerant strategy). Intensively grazed shallow subtidal
habitats are a good example of this situation. When disturbance potential is
high and productivity potential is low, such as in constantly disturbed cobble
fields on exposed coasts with low nutrient levels, no viable strategy is possi-
ble, and seaweeds do not occur. When both productivity potential and distur-
bance potential are low, stress-tolerant strategists, including algal crusts and
microalgae, prevail. Between these extremes, weedy seaweeds with interme-
diate solutions—typically involving rapid reproduction—are found (Fig. 5.7).

Seaweed Defenses
Seaweeds commonly have both structural and chemical defenses. The
only seaweeds that lack any real structural defenses are the rapidly growing
 ROCKY SHORES ` 181

Anatomy (cross- Grazing

Functional group Examples Morphology section) difficulty

Diatoms
Microalgae Blue-green algae

Increasing toughness
Cladophora
Filamentous algae Ectocarpus

Foliose algae Ulva

Porphyra

Macrophytes Chondrus
Mastocarpus

Laminaria
Leathery macrophytes
Fucus
Non-calcareous
crusts

Articulated calcareous Corallina

algae

Crustose coralline algae Lithothamnium

Clathomorphum

Fig. 5.6 Algal functional groups. (After Littler and Littler 1980; Steneck and Dethier
1994.)

ephemeral green algae such as Ulva and Enteromorpha, which are the pre-
ferred food of most intertidal herbivores. The tough, leathery cuticles of cor-
ticated seaweeds (e.g., Chondrus and Fucus) act as a structural barrier to limit
herbivory by small crustacean grazers such as amphipods (Gaines 1985). Al-
gal crusts are especially well defended. Fleshy crusts like Ralfsia are hard,
and snail grazers suffer conspicuous tooth damage when forced to eat them.
Calcified crusts, like Lithothamnium, are even harder, and are immune to
most herbivores except limpets, chitons, and urchins. Bob Steneck (1983) has
shown that the evolution of these coralline crusts parallels the evolution of
scraping herbivores in the fossil record.
As described in chapter 2, chemical defenses commonly complement
structural defenses in seaweeds and other sessile organisms (for review
see Hay and Fenical 1988; Hay 1996). Some seaweeds, such as Desmarestia,
produce sulfuric acid that dissolves the calcium carbonate teeth of potential
consumers. Other seaweeds utilize secondary metabolites (chemicals derived
from metabolic by-products), such as phenolic and halogenated compounds,
for defensive purposes. Like many terrestrial plants, seaweeds often respond
to grazing by increasing the production of defensive compounds. The
182 ` CHAPTER 5

Competitive
Disturbance
strategy
tolerance
Kelp
Crustose algae

Productivity potential
Corticated Weedy
macroalgae strategy
Microalgae,
filaments, thin
blades
No viable strategy
Stress tolerance
Crusts, microalgae

Disturbance potential

Fig. 5.7 A generalized model of the occurrence of algal functional groups across
disturbance and productivity gradients. (After Grime 1977 and Steneck and Dethier
1994.)

common rockweed (Fucus) increases phenolic concentrations when grazed,

limiting further grazing damage (Van Alsytne 1988). It also produces more
phenolic compounds when nitrogen is in limited supply (Yates and Peckol
1993). This occurs because the availability of carbon increases. Phenolics are
carbon-based compounds, and when nitrogen limits growth, algae have an
excess of carbon, leading to phenolic production. When nitrogen is not limit-
ing, most carbon is tied up in growth, leaving less for phenolic production.
Mark Hay and his colleagues (Hay et al. 1987; Duffy and Hay 1990; Duffy
1990) have suggested that the chemical defenses of most seaweeds evolved
primarily to limit the effectiveness of large herbivorous fishes and urchins
rather than smaller grazers such as amphipods and snails. They have shown
that small grazers often prefer to eat, and live in association with, seaweeds
that are heavily defended. Through this preference, the grazers are pro-
tected from their own consumers, either by sequestering ingested defensive
compounds or by living in habitats avoided by generalist consumers. Thus,
the small crustaceans that live on and consume chemically defended algae
have lifestyles similar to many specialist insect herbivores that live in close
association with chemically defended host plants while doing them minimal
damage and gaining protection from their own consumers (Fig. 5.8).

ROCKY INTERTIDAL HERBIVORES

The two sources of primary production that characterize rocky intertidal food
webs are harvested by different organisms using different means. Benthic di-
atoms and seaweeds are eaten primarily by slow-moving resident grazers
 ROCKY SHORES ` 183

(A) (B)

Reef fishes

Individuals building domiciles

Individuals with grazing scars

OH

Concentration of pachydictyol-A (%)

Built totally of
Pseudamphithoiaes this species
incurvaria
Individuals building domiciles

Built partially of
this species
Area eaten

Dilophus alterano

Dictyota cervicornis
Padina jamaicensis

Dictoteris delicatula
Lobophora variegata
Dyctyota dentata

Dictyota dichotoma
Dictyota bartaynesii

Dictyota bartayresii

Fig. 5.8 Relationships between chemically defended seaweeds and small grazers.
(A) In an experimental test of feeding preferences of herbivorous reef fishes and
amphipods, the fishes avoided the chemically defended algae that the amphipods
preferred. (After Hay and Duffy 1990.) (B) The amphipod Pseudamphithoiaes
preferentially builds its domiciles from seaweeds that either experimentally (top)
or naturally (bottom) contain high levels of defensive chemicals. (After Hay 1996.)

that have mouthparts modified for scraping hard surfaces or excavating tis-
sue from macroalgae. In New England and Canada, these grazers include
periwinkles, amphipod and isopod crustaceans, sea urchins, and limpets. Un-
like those in shallow-water tropical habitats (Randell 1967), fishes in most
cold temperate habitats are not typically important herbivores (Vermeij 1978).
184 ` CHAPTER 5

Green urchin
Strongylocentrotus Purple urchin
droebachiensis Arbacia puctulata

Fig. 5.9 Western Atlantic sea urchins of rocky shores.

A second trophic pathway links water column dynamics to benthic shore-

line populations. Pelagic microorganisms, including algae (phytoplankton),
cyanobacteria, and animals (zooplankton), are particularly abundant in
nutrient-rich coastal waters, and enter benthic food chains through sessile
filter feeders. On rocky intertidal shores of the Atlantic coast of North Amer-
ica, mussels and barnacles are the most conspicuous and abundant sessile
filter feeders.

GRAZERS

The green sea urchin Strongylocentrotus droebachiensis is the most voracious

scraping herbivore on New England shores, but its extreme vulnerability to
physical stresses and bird predation restrict it for the most part to subtidal
and deep tide pool habitats (Fig. 5.9). Sea urchins are also uncommon in bays
and estuaries, where salinity may vary widely. Like other echinoderms, they
have no physiological mechanism to deal with varying osmotic conditions.
Sea urchins feed with a movable jaw of five continually growing cal-
cium carbonate teeth, called an Aristotle’s lantern (see chapter 2). Urchins
consume seaweeds by ingesting them whole, taking bites out of them, or
scraping their surfaces. At high densities, they are capable of consuming
all but heavily calcified coralline crusts (Sebens 1985). In subtidal habitats,
 ROCKY SHORES ` 185

Fig. 5.10 The tongue-like radula of the periwinkle Littorina is used to rake the
surfaces of diatoms and soft algal tissue.

groups of hundreds of thousands of urchins (“fronts”) can move through an

area, consuming all erect algae and scouring the substrate down to algal
crusts and bare rock, creating “urchin barrens” (Witman 1985).
Both overharvesting and disease have taken a heavy toll on Atlantic
coast sea urchin populations over the past two decades. Sea urchins are har-
vested for their eggs, which are an expensive delicacy in Japan. Overhar-
vesting has become a serious problem in Canada and New England as well
as on the west coast of North America. In the north Atlantic, diseases have
also devastated urchin populations and led to catastrophic local extinctions.
Similar diseases have been responsible for the large-scale die-offs of Carib-
bean sea urchins that have contributed to changing Caribbean reef habitats
from coral-dominated to algae-dominated systems (Lessios et al. 1984). In
the northern Atlantic, outbreaks of a water-borne amoeboid pathogen have
been associated with unusually warm water temperatures, and have been
responsible for shifting entire subtidal habitats from urchin barrens domi-
nated by algal crusts to kelp beds (see Scheibling and Stephenson 1984;
Scheibling 1986).
Higher on New England rocky shores, three species of herbivorous gas-
tropods of the genus Littorina are the dominant grazers. Periwinkles feed
with a tongue-like radula, but modified for use as a rake or file (Steneck and
Watling 1982) (Fig. 5.10). They scrape diatoms, algal sporelings, and soft algal
tissue into their mouths, where the food is entangled in mucus and pulled
into the digestive system. Periwinkle radulae are incapable of digging deeply
186 ` CHAPTER 5

Veliger
Adult Juvenile larva

Fig. 5.11 The common European periwinkle, Littorina littorea.

into algal tissue and tend to grind down if the animals eat structurally de-
fended algae.
On both open-coast and estuarine shorelines of New England, the com-
mon periwinkle, Littorina littorea is often found at densities of 200–500 per
square meter, and can play an exceedingly important role in the structure
and organization of shoreline communities (Lubchenco 1978, 1983; Bertness
1984a) (Fig. 5.11). Until very recently (Wares et al. 2002), the common peri-
winkle was thought to have been introduced to North America in the mid-
nineteenth century from Europe. Molecular data, however, have revealed
that Littorina littorea has been in North America for at least the past ten thou-
sand years and that during the last Ice Age it found refuge somewhere
in Nova Scotia. Littorina littorea has planktonic development, and Carlton
(1982) has shown that prior to the 1840s adult snails were not found south of
Nova Scotia, until middle of the nineteenth century, when it began moving
south, reaching Cape Cod by the turn of the century and Chesapeake Bay by
the 1950s. What had been thought to be an exotic species invasion by a dom-
inant herbivore with large community impacts (Steneck and Carlton 2001),
however, turned out to be a range expansion by a snail that had its range
constricted during an earlier ice age (Fig. 5.12). Littorina littorea is a habitat
generalist found in all New England shoreline habitats that have at least
some hard substrate. It commonly reaches 2–3 centimeters in length. Mor-
phological variation in spire height and shape can be striking, and is largely
due to variation in growth rates. Fast-growing snails develop more globose,
higher-volume shells than slower-growing snails (Kemp and Bertness 1984)
(Fig. 5.13).
From salt marshes to wave-exposed rocky shores, the common periwin-
kle has become the most abundant intertidal herbivore throughout its biogeo-
graphic range, and has had a considerable effect on shoreline communities of
the Atlantic coast of North America. In salt marsh habitats it has displaced
the native mud snail Ilyanassa (Brenchley and Carlton 1983), and on open-
coast rocky beaches it is responsible for limiting the distribution and success
of palatable green algae and algal sporelings (Lubchenco 1978, 1983). It may
have had its greatest effect, however, on the estuarine cobble beaches of Nar-
ragansett Bay and Long Island Sound, where its numbers can exceed 1000 per
square meter (see the discussion of zonation on cobble beaches below).
 ROCKY SHORES ` 187

1840

1854
Halifax, Nova Scotia

1870

1872
Cape Cod, Massachusetts
1875
1879
1881

1888
Cape May, New Jersey
1890

1952
1964
1971
1978

Fig. 5.12 Invasion history of the common periwinkle, Littorina littorea, in North
America. (After Carlton 1982.)

Both the rough periwinkle, Littorina saxatilis, and the smooth periwin-
kle, Littorina obtusata, are smaller native species that, in contrast to the com-
mon periwinkle, have direct development and are never found at extremely
high densities. Littorina saxatilis is a small snail, rarely larger than 8 millime-
ters in length, found at high intertidal heights above where common peri-
winkles occur (Gosner 1978). It has received little experimental attention
in North America, and can be difficult to distinguish from juvenile common
periwinkles. In Europe, Littorina saxatilis grows faster and reaches larger
sizes on protected shores than on wave-exposed shores; these differences are
controlled by both environmental and genetic factors (Hughes and Roberts
1981; Janson 1983).
In New England, Littorina obtusata is almost always found associated
with algal canopies of the knotted wrack, Ascophyllum nodosum. Shell shape
188 ` CHAPTER 5

Fast growing
– 0.2

– 0.4
Log shell volume (cc)

– 0.6

– 0.8

–1
Slow growing
–1.2
1 1.1 1.2 1.3
Log shell length (mm)

Fig. 5.13 Growth rates influence shell morphology in the common periwinkle,
Littorina littorea. Fast-growing snails are more globose, or round, than slow-growing
snails. (After Kemp and Bertness 1984.)

and thickness in Littorina obtusata are highly variable. In wave-exposed habi-

tats it develops a larger foot for resistance to increased wave stresses
(Trussell et al. 1993). Shell thickness in this snail is also a plastic response
to the presence of its predators. Littorina obtusata from wave-protected habi-
tats have thicker shells than those from wave-exposed habitats because of
phenotypic shell thickening in response to exposure to predaceous crabs
(Trussell 1996). Thin-shelled individuals transplanted to low wave energy
habitats with high predator densities develop thick shells, as do snails reared
with predaceous crabs in the laboratory. Average shell thickness in New
England Littorina obtusata has also increased over the last century (Vermeij
1982b; Seeley 1986), apparently as a plastic response to the introduction of
green crabs.
In contrast to periwinkles, whose radulae are designed for raking sur-
faces, limpets and chitons often have radulae with iron-capped teeth, de-
signed to excavate and shovel algal tissue into their mouths (Steneck and
Watling 1982). Neither limpets nor chitons, however, are very common or
important herbivores in the western Atlantic relative to other temperate ar-
eas. Whereas there are ten common species of shallow-water limpets in
Puget Sound, and eight on European shorelines, there are only two species
on New England shorelines, and neither is particularly abundant. The ab-
sence of a well-developed limpet and chiton fauna in the western Atlantic is
likely a consequence of Ice Age disturbances and more recent severe winter
ice scouring events that have driven most of these organisms to extinction
and prevented their reinvasion (Wethey 1985).
 ROCKY SHORES ` 189

Acmaea testudinalis Clathomorphum

circumsciptum
+

Receives a constant food source + Is cleaned of epiphytes,

and smooth foraging surface sediments, and dead
surface cells.

Fig. 5.14 The limpet/coralline crust mutualism. (After Steneck 1982.)

The most common limpet in New England, the tortoise shell limpet
Acmaea testudinalis, is a feeding specialist that preferentially settles and feeds
on the coralline crust alga Clathomorphum (Fig. 5.14). The relationship be-
tween Acmaea and Clathomorphum has been described as a coevolved mutu-
alism (Steneck 1982). From this association, Acmaea gets a constant food sup-
ply and a smooth surface on which to forage. In return, Clathomorphum gets
its surface cleaned of fouling epiphytes and sediments. Like most other crus-
tose algae, Clathomorphum depends on grazers for its persistence. Without
grazers, it is outcompeted for light by faster-growing algae or suffocates un-
der accumulated sediment.
Chitons are also uncommon in the western Atlantic, particularly in com-
parison to the west coast of North America and the temperate shores of New
Zealand and Australia. In the Puget Sound region of Washington State, five
shallow-water chitons are common. They play an important ecological role
in these communities, and reach sizes of up to 30 centimeters in length. In
New England, only three small (generally less than 30 millimeters) chitons
occur, none are common, and all are largely restricted to subtidal habitats.

Filter Feeders
The second major group of herbivores on New England rocky shores com-
prises the sessile filter feeders, of which acorn barnacles and blue mussels
are the most conspicuous. Acorn barnacles dominate middle to high rocky
intertidal habitats throughout New England, but become less dominant on
Canadian shores as a result of increased ice damage and possibly the lower
food supplies available in northern oligotrophic waters (A.R.O. Chapman,
personal communication). Acorn barnacles were described by Louis Agassiz
as shrimps glued to rocks by their heads, enclosed in a calcium carbonate
house, kicking food into their mouths with their feet. Acorn barnacles actu-
ally do less kicking and more passive straining to catch their food than
Agassiz suggested. Although they will beat their feet (cirri) in still water, ac-
tively straining particles from the water, in the field they are almost always
passive feeders, relying on ambient currents to deliver food to their feeding
appendages (Sanford et al. 1994; but see Trager et al. 1990).
190 ` CHAPTER 5

Fig. 5.15 The ubiquitous northern acorn barnacle, Semibalanus balanoides.

Since barnacles are important fouling organisms on ships and pilings,

they have received a great deal of attention, and as a result, we understand
their biology and ecology probably better than that of any other shoreline
organism. Both the American and British naval research offices have spon-
sored considerable basic research on the biology of barnacles.
Found throughout the northern Atlantic, the northern acorn barnacle,
Semibalanus balanoides (also known as the northern rock barnacle), is the most
common barnacle in New England (Fig. 5.15). Other common shoreline bar-
nacles include Chthamalus fragilis, found at high intertidal heights on hard
substrates south of Cape Cod, and Balanus crenatus and Balanus eburneus,
common in subtidal and estuarine habitats, respectively (Fig. 5.16).
Acorn barnacles are simultaneous hermaphrodites (functioning at the
same time as males and females). Internal fertilization is accomplished by a
penis up to five times the animal’s maximum body dimensions. This repro-
ductive strategy makes it necessary for barnacles to live close together, and
their larvae settle in response to specific chemical signals that indicate the
presence of conspecifics (Crisp and Meadows 1962). In the northern acorn
barnacle, fertilization occurs in the late summer, and the eggs are incubated
in the mantle cavity until late winter, when they are released as nauplius
 ROCKY SHORES ` 191

Semibalanus Chthamalus fragilis Balanus crenatus Balanus improvisus Balanus eburneus

balanoides Little gray Crenate barnacle Bay barnacle Ivory barnacle
Northern acorn barnacle Subtidal Estuarine Estuarine
barnacle High intertidal
North of Long South of Cape Cod
Island Sound
Coastal

Fig. 5.16 Common acorn barnacles of the Atlantic coast of North America.

larvae (Fig. 5.17). The larvae remain in the water column for 6–8 weeks, de-
pending on temperature and food concentrations, where they move at the
mercy of local oceanographic conditions, largely as passive particles. They
pass through four nauplius larval stages before metamorphosing into a ter-
minal cyprid larval form that selects a habitat and settles, committing irre-
versibly to a permanent adult habitat. Settlement involves attachment to
the substrate with adhesive antennal glands and the secretion of a calcare-
ous external skeleton. Life span is highly variable; many recruits survive
less than a day, while others can live up to 4–5 years.
Because acorn barnacles have a relatively long planktonic larval period
and larvae that behave like passive particles, their populations have long
been assumed to be genetically homogeneous. At small spatial scales, how-
ever, Paul Schmidt and David Rand have documented strong intertidal
height zonation of genotypes that is the product of intense selection and
mortality each settlement season (Schmidt and Rand 1999).
Blue mussels are the second most abundant and conspicuous rocky in-
tertidal filter feeder in New England. Until recently, all blue mussels in the
northern Atlantic were thought to belong to the same species. There are,
however, two species of Mytilus that occur in the northwestern Atlantic:
Mytilus edulis, which occurs from Cape Hatteras, North Carolina, to New-
foundland, Canada, and Iceland, and Mytilus trossulus, which occurs from
Newfoundland to Nova Scotia (Koehn et al. 1984; Koehn 1991; McDonald et
al. 1991). Hybrids between M. trossulus and M. edulis are found in Nova Sco-
tia and Newfoundland. Neither the ecology of M. trossulus or that of the hy-
brid zone between M. trossulus and M. edulis has been well studied. Earlier
reports of microgeographic variation among M. edulis populations in
Canada (Gartner-Kepkay et al. 1983) are almost certainly due to the interdig-
itation of these two species and their hybrids (Hilbish 1996). The two species
have different thermal limits, but are not visually distinguishable, and ap-
pear to play identical roles in the habitats they are found in. Like northern
acorn barnacles, blue mussels become increasingly patchy and less abun-
dant at higher latitudes as a result of ice disturbance (Stephenson and
192 ` CHAPTER 5

Late nauplius stage

Early nauplius stage

Final cyprid larval stage

Settlement and
Egg mass in ovisac attachment
in mantle cavity

Copulation

Fig. 5.17 Life cycle of an acorn barnacle.

Stephenson 1971) and, probably, the inability of oligotrophic waters to sup-

port large populations of filter feeders. The southern limit of the distribution
of Mytilus edulis at Cape Hatteras is known to be maintained by thermal
stress. Blue mussel recruits are regularly transported south of Cape Hat-
teras, but persist only until summer temperatures reach about 27°C, when
they die back (Gray 1960).
In contrast to barnacles, blue mussels are active filter feeders that pump a
current of water over their gills with cilia, and therefore their success is not as
tightly linked to flow as that of barnacles (Wildish and Kristmanson 1979).
Blue mussels also have external fertilization, with females releasing up to 25
million eggs per season. Fertilization is followed by a planktonic larval life of
up to 3 months. In the plankton, mussel larvae are passively transported by
ocean currents, leading to wide dispersal and gene flow (Scheltema 1971b,
1986).
Blue mussels initially settle as small (0.5–2.0 millimeters) plantigrade
 ROCKY SHORES ` 193

Plantigrade larva
Veliger larva

Trochophore larva Secretion of shell

Exhalant Settlement and Initital settlement in

siphon
External metamorphosis filamentous algae
fertilization
d
na
Go

Secondary
settlement with
other mussels

Fig. 5.18 Blue mussel life cycle.

larvae in association with filamentous algae near adult mussel populations.

After doubling in size, however, many juvenile mussels migrate into associ-
ation with adults (Bayne 1964). The initial settlement of plantigrade larvae
on algae probably minimizes competition with adult mussels while provid-
ing shelter from physical stresses and predators (Fig. 5.18).
Blue mussels attach to the substrate by means of proteinaceous byssal
threads, produced by a byssal gland at the base of the foot and applied to the
substrate by a groove in the foot (Fig. 5.19). Using their byssal threads like
climbing ropes, small mussels (less than 2 centimeters) are extremely mo-
bile. For all practical purposes, mussels become sessile when they get too
heavy for the strength of their byssal threads to move them, but they can
reattach by byssal threads if dislodged from the substrate. The strength of
mussel byssal attachment varies among habitats and seasonally. Mussels are
more firmly attached on wave-exposed shores than wave-protected shores
194 ` CHAPTER 5

Posterior
adductor
muscle
Byssal gland

Gill

Anterior
adductor
muscle

Byssal threads

Fig. 5.19 Byssal attachment in mussels.

(Witman and Suchanek 1984), are more firmly attached when they are soli-
tary or in small groups than when they are found in dense aggregations or
beds (Bell and Gosline 1997), and increase their attachment strength when
exposed to potential predators (Leonard et al. 1998b). Mussels are also more
firmly attached in the winter than in the summer (Carrington 2002). All
these patterns of attachment strength reflect that mussels increase the pro-
duction of byssal threads to increase attachment strength when wave stresses
and the risk of dislodgement are the greatest.
Blue mussels are typically found in dense beds in low intertidal and
shallow subtidal habitats. As is the case for barnacles, group living in mus-
sels has both costs and benefits. Dense mussel beds enhance external fertil-
ization success (Denny et al. 1985), provide protection to small, vulnerable
juveniles from crab and fish predators (Bertness and Grosholz 1985), protect
intertidal individuals from heat and desiccation stresses (Bertness and
Leonard 1997), and buffer individuals from wave stress (Denny et al. 1985).
By providing a rough topography on the bottom, dense mussel beds may
promote turbulent mixing of the water, which can limit the development of
a food-depleted near-bed boundary layer (Fréchette et al. 1989). Conversely,
competition among neighbors for food is intense in dense beds (Harger
1971; Bertness and Grosholz 1985; Okamura 1986).
Mussels are also important ecosystem engineers that modify shoreline
environments and provide habitat for other organisms (Suchanek 1986). By
slowing water flow, trapping and binding sediments, and depositing partic-
ulate wastes, mussel beds accelerate sedimentation rates, prevent erosion,
and limit the mobility of cobbles on rocky shores by binding them to the sur-
face (Stephens and Bertness 1991). Moreover, by increasing the hard-substrate
surface area, mussel beds serve as an important habitat for encrusting algae
and animals, small mobile organisms that live within the mussel matrix, and
soft-sediment tube-building organisms.
In spite of wide dispersal and high gene flow, adult mussels show
strong genetic differentiation on relatively small spatial scales (Hilbish and
 ROCKY SHORES ` 195

lap 94
Connecticut

Long Island

Atlantic Ocean

Fig. 5.20 The frequency of the lap94 allele (darkened area of pies) among blue
mussels, Mytilus, along a salinity gradient in Long Island Sound. In spite of the wide
dispersal of larvae, adult mussels in the sound show low lap94 frequencies due to
differential mortality of individuals with this allele. (After Koehn and Hilbish 1987.)

Koehn 1985). In particular, mussels in bays and estuaries are better at coping
with low salinities than mussels in nearby open-coast habitats, and this dif-
ference is due to genetic differentiation in their ability to regulate cell vol-
ume under changing osmotic conditions. Genetic differentiation in this trait
on relatively small spatial scales is maintained by strong selection on mussel
settlers every year. Wide dispersal annually leads to a random mixing of ju-
venile genotypes, but post-settlement differential mortality results in strong
spatial genetic differentiation in adult mussels (Fig. 5.20).
In addition to the barnacles and mussels that dominate most New
England rocky intertidal seascapes, low intertidal and shallow subtidal
habitats also support a variety of filter-feeding clonal invertebrates. These
include encrusting tunicates such as Botryllus and Botrylloides, solitary tuni-
cates such as Styela, bryozoans such as Bugula, hydroids such as Obelia and
Hydractinia, and shell-boring (Cliona) and encrusting (Microciona) sponges.
Most of these organisms are active filter feeders that propagate asexually,
which allows them to monopolize substrate rapidly and outcompete most
solitary space holders. As a rule, these clonal subtidal dominants are pre-
cluded by heat and desiccation stresses from living in intertidal habitats (Jack-
son 1977).

PREDATORS ON ROCKY SHORES

Predators on Atlantic rocky shorelines include shell-drilling snails, starfishes,

crabs, fishes, and birds (Fig. 5.21). Predaceous snails that use their tongue-like
 196 ` CHAPTER 5

Open coast Wave-sheltered bay

Gulls
Gulls

Urchins Nucella Asterias

Green crabs

Littorina Littorina

Fleshy algae Barnacles Mussels Fleshy algae Mussels Barnacles

Fig. 5.21 Food webs for open-coast and protected bay sites in the Gulf of Maine.

radulae to bore holes in mussel shells or the opercular plates of barnacles are
common predators, particularly in open-coast habitats. In New England and
elsewhere in the northern Atlantic, the dog whelk (Nucella lapillus) is the most
abundant intertidal predaceous snail in open-coast habitats. Nucella belongs
to the thaid family of snails, which are common predators in shallow, hard-
substrate habitats worldwide. In ancient times Nucella was a prized natural
resource because it was used by the Phoenicians to make royal purple dyes.
Dog whelks live at middle to low intertidal heights, feeding primarily on
mussels and barnacles. When common, they can sharply limit populations of
their prey (Menge 1976). In New England, dog whelks are rare and inefficient
predators in highly wave-exposed habitats, since they are easily dislodged by
waves and must hide in cracks and crevices during extreme weather (Menge
1978). They are abundant and important predators at open-coast locations not
exposed directly to waves, and are particularly effective under algal canopies
and on the undersides of boulders, which protect them from waves and keep
them cool and moist during low tides. Interestingly, in Nova Scotia, where
 ROCKY SHORES ` 197

Nucella

Eggs

Fig. 5.22 Nucella lapillus breeding aggregation with eggs.

seaweed canopies dominate wave-exposed shores, Nucella is abundant even

in the most exposed habitats. Tony Chapman of Dalhousie University has
suggested to me that the ability of the snails to live in these exposed habitats is
the result of the presence of the seaweed canopy, which is characteristic of the
nutrient-poor waters of the northern Atlantic. The canopy itself may dominate
these shores because water column food resources are not sufficient to sup-
port filter-feeder populations. In bays and estuaries, low salinities, crab preda-
tors, and winter ice generally limit the distribution of many drilling snails.
Nucella has direct development and crawl-away young. These traits,
combined with its limited mobility, lead to low gene flow, population isola-
tion, and genetic adaptation to local conditions (Vermeij 1982a). Nucella is a
seasonal breeder and, like other thaid gastropods, aggregates in the late
summer or early fall in large breeding groups of tens to hundreds of individ-
uals (Etter 1989). Copulation occurs in these breeding aggregations, and fe-
males deposit eggs in semi-transparent proteinaceous egg capsules, which
they attach to the undersides of rocks. Crawl-away juveniles emerge from
these capsules the following spring, and most return to breed at the same lo-
cation throughout their 5- to 7-year life span (Fig. 5.22).
Like other thaid snails, Nucella are notoriously variable in morphology
and color. Individuals living in wave-exposed locations have a larger foot
and are more resistant to wave dislodgment than individuals from low wave
stress areas. Foot area, however, is a plastic trait that is environmentally de-
termined. Juvenile snails reared in the laboratory develop a small foot char-
acteristic of low wave energy populations, whereas juveniles from low wave
stress populations transplanted to high wave stress habitats develop a large
foot characteristic of high wave stress populations (Etter 1988a) (Fig. 5.23).
In contrast to the high plasticity of foot size, the color of thaids appears to
be under strong genetic control. In New England, Nucella is found in a wide
198 ` CHAPTER 5

300 Exposed
120
Protected

Dislodegment force (g)

Pedal surface area (mm2)

150
60

0
0
0 20 40
0 20 40
Shell length (mm)
Shell length (mm)

Fig. 5.23 The dog whelk, Nucella, develops a larger foot and shell aperture at
wave-exposed sites, resulting in the snails being able to withstand higher wave
forces. (After Etter 1988b.)

range of solid and striped color morphs (Fig. 5.24). White color morphs dom-
inate protected habitats, while darker color morphs dominate wave-exposed
habitats. Ron Etter (1988b) has shown that heat stress in protected habitats se-
lects for reflective light-colored morphs (and against heat-absorbing darker
morphs), and has suggested that cryptic coloration and protection from pre-
dation by birds may also play a role in maintaining these color morphs.
In bays and estuaries south of Cape Cod, the oyster drill, Urosalpinx cin-
era, replaces Nucella on hard substrates as a drilling predator. Urosalpinx is
best known as a pest of oyster beds, but it can also be an important predator
of barnacles and mussels on rocky shores (Katz 1985). Urosalpinx is native to
the Atlantic coast of North America, with a fossil record that goes back over
25 million years (Carriker 1955). Its original distribution appears to have
been from Chesapeake Bay to Narragansett Bay, but during the nineteenth
century it was spread as far north as Maine and as far south as Florida as a
by-product of oyster farming. Oyster transplantation in the twentieth cen-
tury has also introduced Urosalpinx to Europe and the west coast of North
America.
Like Nucella, Urosalpinx is found only on hard substrates. It has a small
foot, does not move well on soft substrates, and requires hard substrates on
which to deposit eggs. Unlike Nucella, however, Urosalpinx is tolerant of low
salinities (as low as 15 parts per thousand salt) and salinity fluctuations, al-
lowing it to live in estuarine habitats inaccessible to Nucella.
Oyster drills have strongly seasonal activity patterns. Like dog whelks,
they have direct development. They breed in the spring and summer and lay
egg capsules, which they usually attach to the sides or bottoms of hard cobble
or shell surfaces. The capsules hatch into crawl-away young in 30–45 days.
 ROCKY SHORES ` 199

Cape Ann

Massachusetts

Light morphs
To Dark morphs
Boston Marblehead

34
Tissue temperature ( C)

20
0 150
Time (minutes)

16
% water loss

Fig. 5.24 Dark-colored dog

whelks are common in
northern New England but
uncommon in southern New
England where they absorb
heat and lose water faster than
lighter snails. (After Etter
0 360
Time (minutes) 1988a.)
200 ` CHAPTER 5

Individuals can live for more than a dozen years. In the winter, Urosalpinx hi-
bernates by moving into deep water and burying itself in the sediment.
Starfishes are also important predators on New England rocky shores,
and often play a role in limiting the distributions of subtidal mussel beds.
Since starfishes are extremely vulnerable to desiccation and have no mecha-
nism to deal with varying salinities, they are usually found in low intertidal
or subtidal habitats, especially on coastal shores with full-strength seawater.
After open-coast storms, starfishes are commonly found thrown up onto the
beach, which suggests that storm disturbances can play an important role in
regulating their subtidal populations (Witman 1987). Starfishes move using
a hydraulic vascular system, which is a radial network of water-filled tubules
moved by both water pressure and muscles.
In low intertidal and shallow subtidal rocky habitats, starfishes are gen-
eralist predators of most sessile animals, but are particularly important mus-
sel and barnacle predators (Lubchenco and Menge 1978). Asterias forbesii and
Asterias vulgaris are the two most common shallow-water starfishes in the
western Atlantic. They feed by everting the stomach, excreting enzymes to
begin digesting their prey, and then sucking the resulting slurry into the di-
gestive system. When small, Asterias vulgaris feeds primarily on bryozoans,
hydroids, and small gastropods, but switches when larger to a diet of clams
and mussels (Hulbert 1979). When eating a mussel, a starfish inserts its stom-
ach between the mussel’s slightly gaping (less than 1 millimeter) valves, and
secretes digestive enzymes until the bivalve relaxes, opening the valves.
When eating barnacles, it simply smothers them with digestive enzymes be-
fore slurping them into the stomach, where digestion is completed. Jon Wit-
man and his colleagues recently found that starfish densities increased dra-
matically in response to a massive recruitment of blue mussels, one of their
favorite foods. They found that an unusually high mussel set in the Gulf of
Maine in 1995 led to elevated starfish densities, and that when the mussel
food supply was depleted, starfishes became less common and resorted to
cannibalism in the absence of alternative food sources (Witman et al. 2003).
Both Asterias forbesii and Asterias vulgaris have external fertilization, re-
leasing eggs and sperm into the water column. Both of these starfishes are
also good at regenerating lost body parts, and can regenerate an entire indi-
vidual from little more than a couple of arms and a third of the central disk
(Fig. 5.25).
Crabs are another common and important predators on New England
rocky shores, particularly in protected habitats. The two most common
shallow-water predaceous crabs in the northern Atlantic are the introduced
European green crab, Carcinus maenas, and the northern rock crab, Cancer
borealis (Fig. 5.26). Both are predators on mussels, barnacles, snails, and
other hard-bodied prey. In contrast to starfishes, crabs are most abundant
and have their greatest effects in protected bays and estuaries rather than in
open-coast habitats. Crabs can generally cope with salinity fluctuations, but
as relatively large mobile organisms, they have difficulty foraging in habi-
tats with strong water movement. Rock crabs are found in low intertidal
 ROCKY SHORES ` 201

Bipinnaria
larva

Fertilized egg
Brachiolaria
larva
External fertilization

Unfertilized egg

Sperm
Young starfish

Gonads expand

Fig. 5.25 Life cycle of a broadcast-spawning starfish such as Asterias forbesii.

habitats in Maine, but are more common subtidally (Gosner 1978). Green
crabs are the most abundant large intertidal crabs on rocky shores in New
England, but were not known north of Cape Cod before 1900, and were
probably introduced into Long Island Sound in colonial times (Glude 1955).
The reproductive behavior and growth of crabs are strongly affected by
their hard external skeletons, which must be shed or molted for growth to
occur. Both green crabs and rock crabs exhibit precopulatory courting be-
havior, in which males find premolt females and mount them in a copula-
tory embrace. Sometimes males carry around females for a number of days
before molting occurs. When the female molts, her genital pore is exposed,
and the crabs copulate. After copulation and fertilization, the female carries
the fertilized eggs under her abdomen, aerating them by gently flexing her
abdomen up and down under the carapace. The young are released as feed-
ing larvae. Larval release by shoreline crabs often occurs during spring
tides, which transport the larvae rapidly offshore, where they are exposed to
fewer consumers (Morgan and Christy 1995). After developing in the water
202 ` CHAPTER 5

Fig. 5.26 The green crab, Carcinus maenus (left), and the rock crab, Cancer irroratus
(right), are common scavengers and predators of hard-bodied prey on rocky shores.

column for a number of weeks, crab larvae move back to shore by regulating
their vertical position in the water column, moving to deeper water or into
surface slicks that move them shoreward (see Morgan 1995).
Juvenile rock and green crabs are translucent and tend to be cryptic to
their predators. Alvaro Palma has shown that juvenile rock crabs preferen-
tially settle on coarse sand substrates, where they are difficult for their pred-
ators to detect (Palma and Steneck 2001). As the crabs grow larger, fewer
predators are capable of consuming them, freeing them to live in other habi-
tats. Molting always makes crabs vulnerable to predators and physical
stresses, since immediately after shedding the old skeleton, they have soft
shells and little protection. Molting green and rock crabs move into shallow
water under rocks or seaweed canopies to minimize these risks.
Birds are more important predators on rocky shores than is often recog-
nized. Herring gulls (Larus argentatus), black-backed gulls (Larus marinus),
and purple sandpipers (Calidris maritima) commonly forage in rocky inter-
tidal habitats during low tides. Gulls drop hard-bodied prey items from the
air onto rocks to break them open (see chapter 3). Their populations have in-
creased over the last century due to human population growth and the pro-
liferation of garbage dumps, which has probably led to their playing a larger
role in coastal communities (Kadlec and Drury 1968). Herring gulls can be
important predators of blue mussels, urchins, starfishes, and rock and green
crabs (Dumas and Witman 1993; Marsh 1986), and may have important di-
rect effects on rocky intertidal communities. For example, while gull preda-
tion has been shown to limit rock crabs to subtidal habitats, green crabs are
less often eaten because they are cryptic and find refuge in algal canopies
(Dumas and Witman 1993). Gull predation can also have important indirect
effects on rocky shore communities by regulating population densities of
crabs and urchins, which otherwise regulate prey abundance patterns. Gull
predation on urchins in tide pools, for example, may enhance the persis-
tence of palatable algae by removing these herbivores (Lubchenco 1978).
 ROCKY SHORES ` 203

Shorebirds can have particularly dramatic effects on the shoreline communi-

ties of offshore islands that are used for nesting. Julie Ellis (2004) has re-
cently shown that on gull breeding islands in the Gulf of Maine gulls play
a major role in shaping the vascular plant communities both by trampling
vegetation and by increasing the nutrient supply. She found that removing
gull impacts on these islands with cages led to dramatic increases in plant
biomass and decreased plant species diversity.

STRESSES IN ROCKY INTERTIDAL HABITATS

Most of the intertidal zone of rocky shores is subjected each day to aerial ex-
posure, presenting problems of desiccation and extreme temperatures for
the organisms that live there. Most organisms from other habitats have a rel-
atively narrow window of about 10°C within which their biochemical sys-
tems will function. Any temperatures exceeding this range will result in
death. For organisms living in rocky intertidal habitats, 10–20°C daily swings
in temperature are routine. Rocky intertidal habitats on the east coast of
North America are stressful even in comparison to other temperate zone
rocky intertidal habitats, since they experience both relatively large tides
and strong seasonality. In southern New England, intertidal organisms can
be exposed to winter temperatures as low as −20°C (Kanwisher 1960a) and
summer temperatures as high as 40°C (Bertness 1989). Daily variations in
temperature are also impressive, with daily fluctuations of 20–30°C common
in both the summer and winter. In the early spring in New England, for ex-
ample, water temperatures may be 2–3°C, but intertidal rocks can heat up to
30–40°C within an hour during low tide exposures.

Desiccation
Desiccation, or water loss, during low tides is one of the most critical prob-
lems facing intertidal organisms. Mobile organisms that live in high inter-
tidal habitats, such as crabs, can move into crevices, under seaweeds, and
into tide pools at low tide to minimize dehydration problems (Kensler 1967)
(Fig. 5.27). Moving to safer habitats during low tide is not an option for ses-
sile or slow-moving organisms, and the species found at high intertidal
heights, such as barnacles and periwinkles, must be especially resistant to
desiccation. The high intertidal barnacle Chthamalus, for example, can sur-
vive 28 days out of water, and the ribbed periwinkle Littorina saxatilis, which
lives at extreme high intertidal heights, can survive over 42 days out of water
(see Newell 1979 for other examples). Organisms characteristic of lower ele-
vations on the shore are generally not capable of dealing with prolonged des-
iccation (Foster 1969).
The problem of dessication can be reduced by increasing body water
volume, limiting water loss, or simply tolerating large water losses. High in-
tertidal snails (Vermeij 1971) and barnacles (Barnes and Barnes 1957) carry
204 ` CHAPTER 5

Inner region Middle region Outer region

• Clay • Coarse sand
• Fine silt • Broken shells
• Gravel

Few inhabitants Greatest diversity and Mainly transient

abundance of mites, species (littorinid
clams, and isopods snails, insects, crabs)

Fig. 5.27 Crevice zonation. At high intertidal heights, cracks and crevices in rocks
offer thermal and desiccation refuges for transient and specialized species. (After
Carefoot 1977 and Kensler 1967.)

relatively large amounts of water in their shells. The globose shape of many
high intertidal snails maximizes the water-holding capacity of their shells
(Vermeij 1971). Water loss can also be limited by sealing off the outside envi-
ronment. Snails, barnacles, and mussels all close their shells tightly when ex-
posed to aerial conditions. Snails exposed to desiccating conditions can also
attach to the substrate with a mucus thread and close the operculum to limit
thermal contact with the rock surface and minimize water loss (Vermeij 1971).
Oxygen depletion can be a significant obstacle to limiting water loss.
Barnacles address this problem by having a small opening between their
valves (the pneumostome) that permits air movement while limiting water
loss (Barnes and Barnes 1957). Mussels periodically open their valves and
“airgape” during low tides to replenish their oxygen supply (Lent 1969).
Some high intertidal organisms rely heavily on anaerobic metabolism, while
many others are simply good at tolerating water loss. High intertidal sea-
weeds are particularly impressive in their ability to tolerate water loss. Fu-
cus, Ulva, and Enteromorpha can all lose as much as 75–90 percent of their
 ROCKY SHORES ` 205

100 1500

Percentage of initial water lost

Resubmerged

Oxygen consumption
(mm3O2/g/h)
50

0 0
0 1 2 0 50 100
Time (hours) Percentage of initial water lost

Fig. 5.28 Drying and respiration curves for the rockweed Fucus. (After Kanwisher
1957.)

water during low tide, but rehydrate rapidly and resume active photosyn-
thesis within an hour of being resubmerged (Kanwisher 1957; see Lobban
and Harrison 1994 for more recent work (Fig. 5.28).

High Temperatures
High summer temperatures are just as serious a problem as desiccation for
many intertidal organisms. During southern New England summers, wa-
ter temperatures are only about 20°C, but both air and rock temperatures
can reach 40°C during daytime low tides. As a result, intertidal residents
can be exposed to extreme high temperatures with large fluctuations. The
metabolic rate of most cold-blooded organisms, which is normally temper-
ature dependent, roughly doubles for every 10°C rise in temperature.
While most intertidal invertebrates do not maintain a constant body tem-
perature, as warm-blooded organisms do, many have relatively temperature-
independent metabolic rates over the range of temperatures at which
they usually live (Fig. 5.29). The mechanisms that permit this relatively
temperature-independent metabolism are largely unstudied, although they
are known to occur in cellular as well as whole-organism metabolism (Newell
1979).
Intertidal organisms avoid high summer temperatures and fluctuations
with some of the same mechanisms they use to minimize water loss. Many
live in thermal refuges such as crevices, tide pools, or algal canopies, thereby
minimizing exposure to high temperatures. On protected shores in the Gulf
of Maine, the algal canopy of Ascophyllum nodosum plays a major role in pro-
viding refuge for intertidal organisms from heat and desiccation (Menge
1978). Other sessile organisms, including many barnacles, mussels, and sea-
weeds, live in dense groups that buffer group members from water loss and
high temperatures (Bertness 1989; Bertness and Leonard 1997). Nonetheless,
the thermal limits of intertidal organisms are reflected in where they occur
206 ` CHAPTER 5

Temperature-dependent
metabolism of deep-water
invertebrates

Metabolic rate

Temperature-independent
metabolism of many sessile or
slow-moving intertidal
invertebrates

Temperature

Fig. 5.29 In contrast to most cold-blooded organisms, many intertidal invertebrates

have metabolisms that are independent of temperature over the ranges they
normally encounter. This allows them to remain active during normal intertidal
temperature fluctuations. (After Newell 1969; Hochachka and Somero 1973.)

on the shore, with the most and least thermally tolerant species found at the
highest and lowest levels of the shore, respectively (Figs. 5.30–5.32).
The effects of summer heating on rocky shore organisms are conspicu-
ously influenced by rock color, composition, and size. Dark-colored rocks ab-
sorb rather than reflect heat, and thus get hotter than lighter-colored rocks.
Sessile organisms such as barnacles may be unable to deal with the tempera-
tures reached by dark-colored substrates (Raimondi 1988a). Rock size effects
on heating can be particularly strong (Bertness 1989). Large boulders or rock
benches have a large mass that buffers them from heating, while small, loose
cobbles not embedded in sediment are not thermally buffered and heat up
rapidly when exposed during summer daytime low tides. In Narragansett
Bay, the differential heating of rocks of different sizes influences barnacle
populations. Few barnacles survive to reproduce on small cobbles, while
larger, thermally buffered boulders support large, age-structured barnacle
populations (Bertness 1989). The rock benches common in open-coast habi-
tats are probably important thermal refugia for many sessile invertebrates.
Seaweed canopy cover can also buffer temperature fluctuations on rock
surfaces (Fig. 5.33). Rock heating effects on the distributions of rocky inter-
tidal organisms, however, are probably not as important on northern New
England or Canadian shores, where summer temperatures are not as high.
The importance of heat stress in determining both the local and bio-
geographic distributions of intertidal organisms was illustrated by David
Wethey’s (1983a, 1984b) work with New England barnacles. In Long Island
 ROCKY SHORES ` 207

40

Chthamalus
Upper lethal temperature (˚C)

35

Semibalanus balanoides

Balanus crenatus

30

1 2 5 10 20 50
Median lethal time (hours)

Fig. 5.30 The thermal limits of Atlantic coast barnacles in Europe reflect their typical
habitats on the shoreline. Chthamalus is the most tolerant of high temperatures and
lives at the highest elevations. Balanus crenatus is the least tolerant and is found in
subtidal habitats. (After Foster 1969.)

Sound, two acorn barnacles are common on rocky shorelines. Chthamalus

fragilis occupies the high intertidal zone, while Semibalanus balanoides domi-
nates the middle intertidal zone. As described in the last chapter, both of
these barnacles are commonly found at high densities and settle widely in
the intertidal zone, so that their distributions are often set by post-
recruitment rather than recruitment processes. Chthamalus can tolerate higher
temperatures, but Semibalanus is competitively dominant to Chthamalus,
since it has shell walls filled with air passageways that allow it to grow
faster and larger (Stanley and Newman 1980). Wethey (1984b) demon-
strated that experimental shading reduced thermal stress and allowed
Semibalanus to displace Chthamalus from high intertidal habitats. He also
found that Chthamalus was restricted to high intertidal habitats by the com-
petitive dominance of Semibalanus. He further suggested that the effect
of thermal stress on the relationship between Chthamalus and Semibalanus
has dramatic biogeographic consequences. North of Cape Cod, summer
temperatures are not hot enough to exclude Semibalanus from high inter-
tidal elevations. As a result, Semibalanus may displace Chthamalus from high
208 ` CHAPTER 5

46

Ilyanasa
Upper lethal temperature (°C)

40

Uca

Arbacia

36 Ophioderma

Asterias
32

50 100
Median lethal time (minutes)

Fig. 5.31 Thermal tolerances of some common western Atlantic shoreline

invertebrates. (After Orr 1955.)

Solitary on cobbles
Crowded on cobbles
Solitary on boulders
High intertidal zone Crowded on boulders Low intertidal zone
36 36
Temperature (˚C)

Temperature (˚C)

26 26
0 100 200 0 100 200
Exposure time (minutes) Exposure time (minutes)

Fig. 5.32 Acorn barnacle tissue temperatures during a summer low tide in
Narragansett Bay as a function of rock size and crowding. (After Bertness 1989.)
 ROCKY SHORES ` 209

Rock temperature under canopy

40
Temperature (˚C)

10

Rock temperature with canopy removed

40

Maximum under-canopy temperature

Temperature (˚C)

Minimum under-canopy temperature

Fig. 5.33 Seaweed (Ascophyllum)

10 canopy effects on mid-intertidal rock
temperatures at Little Compton,
June 21 June 25 June 29 Rhode Island, in 2003.

intertidal habitats, setting the northern biogeographic limit of Chthamalus

(Fig. 5.34). Recent work by Eric Sanford (personal communication), how-
ever, has shown that water temperatures north of Cape Cod may be too
cold for marine organisms with warm water distributions to complete de-
velopment in the water column. If this is generally the case, Chthamalus
may not live north of Cape Cod due to cold water effects on larval develop-
ment rather than competitive displacement by Semibalanus. This hypothesis
should be tested.

Low Temperatures
Extreme low winter temperatures are also a problem for organisms on
New England and particularly Canadian rocky shorelines. On wind- and
210 ` CHAPTER 5

Experimental shading and

northern New England

Southern New England

larval settlement Mean high water

W ul
ith ts
ad
N ove

sh o
or s u
m
Upper limit of Chthamalus

ad ve
th
Ch adu

m
set by physical factors

e S up
of p, d
tha lts

Ca isp

em , ta
ma
Lower limit of Chthamalus

iba ki
pe lac
lus
set by competition

lan ng
Co ing
Se

us ov
Ch

d, C
mi
Upper limit of Semibalanus

tha

Se hth
ba

mi am
ma
set by physical factors

lan
Se

er
ba
mi
lu

us

lan alus
s

bal
Lower limit of Semibalanus

ad
Mean low water

us
an

ul
set by biological factors

ts
s

Semibalanus Chthamalus

Fig. 5.34 Zonation of the acorn barnacles Chthamalus and Semibalanus. In southern
New England, Chthamalus is competitively displaced to high intertidal heights by
Semibalanus. With experimental shading, Semibalanus moves to the high intertidal,
displacing Chthamalus. This process occurs naturally at cooler northern latitudes,
where Chthamalus is driven to regional extinction. (After Connell 1961; Wethey
1983a,b.)

wave-swept shorelines in January and February, ice sheets can cover high
intertidal surfaces, leaving barnacles, mussels, and algae encased in ice for
weeks at a time. Many mobile rocky shore organisms, such as snails (Litto-
rina, Nucella) and crabs (Carcinus and Pagurus), migrate into subtidal habi-
tats to avoid winter stresses. For most sessile organisms, however, extreme
winter conditions are one of the costs of living in intertidal habitats in the
northern Atlantic. Many barnacles and algae can tolerate extreme low tem-
peratures remarkably well, although the mechanisms responsible are not al-
ways clear. Under typical New England winter conditions, as much as 50–70
percent of the water content of invertebrates and algae freezes (Kanwisher
1960a,b). Organisms survive freezing by limiting ice formation to regions be-
tween rather than within their cells (so that cells do not rupture) and by tol-
erating the intercellular hypersaline conditions that develop once ice forms
(Kanwisher 1957). Additionally, some intertidal invertebrates probably uti-
lize organic “antifreezes” analogous to those known to occur in arctic fishes
(Devries 1971). Acorn barnacles, for example, have increased concentrations
of glycerol (a possible organic antifreeze) in the winter, corresponding to
increased resistance to cold (Newell 1979).
Differential freezing tolerances can play a leading role in the zonation of
northern New England seaweeds. The rockweed Fucus is often encased in ice
during the winter in high intertidal habitats in New England, but suffers little
 ROCKY SHORES ` 211

Chondrus Mastocarpus
.75 .75

Change in biomass after 1 month

Change in biomass after 1 month

–.75 0
20 C 5C Frozen Frozen 20 C 5C Frozen Frozen
1 h/d 3 h/d 1 h/d 3 h/d
Acclimation regime Acclimation regime

Fig. 5.35 Freezing effects on the intertidal red seaweeds Chondrus and Mastocarpus
result in Mastocarpus dominating the higher intertidal zone in colder habitats. When
exposed to simulated low tide freezing, Mastocarpus grew, while Chondrus died.
(After Dudgeon et al. 1989.)

mortality (Kanwisher 1957). Similarly, Mastocarpus stellatus, a mid-intertidal

red seaweed, shows no adverse effects when frozen daily for over a month.
In contrast, Irish moss (Chondrus crispus), which dominates many subtidal
New England habitats, dies when exposed to freezing conditions (Dudgeon
et al. 1989). Cold winter exposure commonly kills intertidal Chondrus, and in
northern New England, freezing appears to limit Chondrus to subtidal habi-
tats (Dudgeon et al. 1989; Mathieson and Burns 1975) (Fig. 5.35).
Cold winter conditions are also important in determining the biogeo-
graphic distributions of species on New England rocky shores. Cape Cod is
a major biogeographic boundary for many marine taxa, forming the south-
ern range limit of many boreal species and the northern limit of many south-
ern species (Vermeij 1978). The importance of cold winters in maintaining
the northern limit of southern species was demonstrated by W. C. Allee
(1923). Allee documented that severe winters north of Cape Cod kill few bo-
real species, but southern species that successfully recruit north of Cape Cod
suffer heavy mortality in severe winters.
As described in the first chapter, ice damage is an extremely important
consequence of the cold winter conditions on Canadian rocky shores, partic-
ularly north of Nova Scotia (Stephenson and Stephenson 1971). Ice can en-
case intertidal organisms and rip them from the shoreline (Mathieson et al.
1982), leaving many northern rocky shores in a constant state of recovery
from chronic disturbance. Ice scour from floating ice is also a major problem
for organisms on many Canadian rocky shores. In the Gulf of Saint Lawrence,
for example, heavy annual ice scouring restricts northern acorn barnacles to
living in cracks and crevices. Bourget and Holm (1994) have suggested that
212 ` CHAPTER 5

Fig. 5.36 A simple wave force dynamometer consists of a spring mounted in a

plastic tube, attached on a swivel mount to the substrate. The instrument measures
the force exerted on a drogue attached to the spring.

this chronic ice scouring has led to selection for increased settlement in cryp-
tic crevice habitats in barnacles in the Gulf of Saint Lawrence.

Wave Stresses
Wave stress in exposed open-coast habitats can play a major role in the design,
abundance, and distribution of rocky intertidal organisms and acts as an im-
portant modifier of shoreline zonation patterns. Wave velocities can be mea-
sured with a simple, inexpensive device called a wave force dynamometer
(Bell and Denny 1994) (Fig. 5.36). Such measurements show that wave veloci-
ties on exposed shorelines can reach 25 meters per second (Denny et al. 1985;
Denny 1987).
One of the most conspicuous effects of wave forces on intertidal organ-
isms is the limitation of organism sizes (Denny et al. 1985). Small, squat
organisms, such as barnacles and limpets, live with much of their bodies
within surface boundary layer conditions, which minimizes their exposure to
wave forces, and have streamlined shapes that further minimize lift and
drag. As organisms increase in size, their vulnerability to wave forces in-
creases, and unless they compensate with increased attachment and/or
structural strength, they become more vulnerable to being ripped off the sub-
strate. Wave forces may thus often set the upper size limit and optimal size of
intertidal organisms in wave-exposed habitats (Denny et al. 1985; Gaylord
1998) (Fig. 5.37).
A number of mechanisms limit the effects of wave stress in coastal habi-
tats. Dense groups of organisms buffer individuals from wave stresses. Mus-
sels in mussel beds, for example, are less exposed to wave forces than soli-
tary individuals, allowing individuals in beds to exceed the calculated
maximum solitary size (Denny et al. 1985). Algal canopies also reduce wave
forces and permit organisms to live in habitats that they could not otherwise
occupy (Holbrook et al. 1991). In particular, many of the mobile organisms
associated with mussel beds and algal canopies (including carnivorous and
herbivorous snails) are clearly dependent on canopy wave buffering in wave-
exposed habitats.
The macroalgae on wave-exposed shorelines often are much larger than
the sessile invertebrates. In contrast to invertebrates, which rely on small
size, firm attachment, and rigid bodies to cope with wave stress, seaweeds
 ROCKY SHORES ` 213

Tortoise shell limpet Cup and saucer limpet Red chiton Acorn barnacles
Acmaea testudinalis Crucibulum striatum Ischnochiton ruber Semibalanus and Chthamalus

Fig. 5.37 Sessile and slow-moving invertebrates on wave-exposed rocky shorelines

are small and have streamlined profiles to minimize the effects of wave stress.

often rely on flexibility. By bending, algae reduce their exposed surface area
and move closer to the low-wave-energy boundary layer (Koehl and Wain-
wright 1977). Flexibility allows many seaweeds (such as the shallow subti-
dal kelp) to attain relatively large sizes while minimizing their exposure to
waves (Fig. 5.38). Other soft-bodied organisms, such as anemones, sea

Low flow High flow

Fig. 5.38 Many seaweeds cope with high wave energy by bending into the flow,
by which they reduce their profile and drag, and also move closer to the substrate,
where they experience lower wave forces. This strategy allows them to achieve
larger body sizes than if they had rigid bodies.
214 ` CHAPTER 5

squirts, and hydrozoans, also depend on flexibility to deal with wave forces
(Koehl 1984a,b).
Spatial variation in wave stresses can be important in generating distri-
bution patterns both within and between seaweed species. A good example
of wave stress effects on the morphology of an algal species can be found in
the knotted wrack Ascophyllum nodosum. In wave protected bays Ascophyl-
lum can be 1–2 meters in height and have very low stipe densities. In con-
trast, in wave-exposed habitats Ascophyllum is typically shorter than 25 cm
tall and has extremely high stipe densities as a consequence of stipes being
ripped off by waves followed by stipe regrowth. In Nova Scotia, Ascophyl-
lum lives unattached on salt marshes as a short, stunted plant resembling a
tumbleweed (A. Chapman, personal communication).
Morphological variation in seaweeds across wave stress gradients, how-
ever, must be interpreted with caution, since conspicuous morphological
differences in flexible organisms do not necessarily influence their responses
to hydrodynamic stresses (Carrington 1990). Morphological variation in
soft-bodied sessile invertebrates in response to wave stress gradients is also
probably common, but is not well studied. Steve Palumbi (1984, 1986) has
shown that individual sponges can increase their investment in structural
support and take on a more compact, rigid structure in response to wave
stress exposure.
Species differences in morphology or resistance to wave damage com-
monly lead to species replacements across wave stress gradients. An exam-
ple can be found in coastal habitats in the Gulf of Maine, where Mastocarpus
stellatus replaces Chondrus crispus in wave-exposed habitats. Though these
two seaweeds have similar breaking strengths, Chondrus fronds have a higher
surface area, which increases drag and biomass loss (Dudgeon and Johnson
1992).
Vulnerability to wave dislodgement is often enhanced by epiphytic or-
ganisms that increase drag forces on their hosts. The horse mussel, Modiolus
modiolus, for instance, commonly forms dense subtidal beds off rocky shores
in the Gulf of Maine. It is much more vulnerable to wave dislodgement
when kelps are attached to its shells (Witman and Suchanek 1984). Similarly,
the introduced green alga Codium fragilis spp. tomentosoides has had a major
effect on cobble shorelines because it increases drag on cobbles. This makes
the cobbles more vulnerable to dislodgment, which kills associated organ-
isms (Carlton and Scanlon 1985) (Fig. 5.39).
Wave forces can also shift the distributions of organisms by reducing
desiccation stress at high intertidal heights (Stephenson and Stephenson
1971). On exposed shorelines, waves crashing onto the shore splash higher
than on more protected shores, permitting organisms whose upper inter-
tidal limit is set by heat and desiccation to live at higher intertidal heights.
Typically, this effect shifts the entire zonation sequence to higher intertidal
heights (Fig. 5.40).
Wave forces also influence the distributions of intertidal organisms by
abrading surfaces of settlers. Algal abrasion—the thrashing of seaweeds
 ROCKY SHORES ` 215

Fig. 5.39 Examples of seaweeds growing epiphytically on other organisms,

increasing the probability that those organisms will be dislodged by waves, include
kelps on horse mussels (left) and Codium on slipper limpets (right).

against the substrate, resulting in the death of recent settlers—can be an im-

portant source of mortality, particularly for sessile organisms associated
with algal canopies in high wave energy environments (Menge 1976). On
wave-exposed rocky shorelines in Maine, for example, surfaces adjacent to
algal canopies often have a band of bare space, or whiplash halo. This band
is caused by the physical removal of organisms by whiplash abrasion and
the grazing of snails that are dependent on the algal canopy for protection
from heat and wave stresses (Fig. 5.41).

ZONATION

The zonation of rocky shores has long interested ecologists and has been well
studied on the Atlantic coast of North America. Rocky intertidal shores have
served as a model system for studying the zonation of shoreline organisms
introduced in the last chapter. This pronounced vertical or elevational zona-
tion is the product of strong gradients in physical and biological stresses.
At high intertidal heights, only organisms capable of tolerating long periods
out of water and extreme temperature fluctuations persist. At low intertidal
216 ` CHAPTER 5

Exposed Sheltered
Upper limit of
barnacles

Upper limit of
mussels

Upper limit of
fucoids
Extreme high
water

Upper limit of
kelps

Extreme low
water

Fig. 5.40 Relationship between the intertidal heights of distribution zones on rocky
shores and wave exposure. (Modified for New England after Lewis 1964.)

Fig. 5.41 Abrasion halos around rockweeds prevent most larval recruitment.
 ROCKY SHORES ` 217

heights, where habitats are not exposed to such intense disturbance, organ-
isms face less stressful physical conditions, but more severe biological stresses.
Consequently, only organisms capable of successfully dealing with consumers
and competitors persist at low intertidal heights.

Wave-exposed Shores
The vertical zonation of organisms on rocky shores on the east coast of North
America has been studied most intensively on wave-exposed shorelines in
the Gulf of Maine (Menge 1976; Grant 1977). Wave-exposed headlands are
characterized by discrete zones of densely packed organisms and little (usu-
ally less than 10 percent) unoccupied (free) space (Fig. 5.42). The acorn barna-
cle Semibalanus balanoides typically occupies a distinct high intertidal band,
but is replaced at middle intertidal elevations by the blue mussel Mytilis edulis.
The mussel zone usually extends into the shallow subtidal zone, where kelp
beds occur.
The simplicity of these habitats is largely due to wave stress and shock.
Few organisms can tolerate these stresses, and those that can (barnacles,
mussels, and kelps) dominate these habitats because waves limit the abun-
dance of their predators. Where algal canopies are absent, predatory crabs,
fishes, and snails and herbivorous snails and urchins are rare and ineffective
consumers (Menge 1978), leading to the dominance of only a few wave-
tolerant species. As already mentioned, this scenario appears to break down
in the oligotrophic waters of the Canadian Maritimes, where even extremely
wave-exposed rocky shores support robust seaweed canopies that harbor
dense snail populations.
In the absence of consumers, competition for space is usually an impor-
tant determinant of the zonation of wave-exposed shores in New England.
Semibalanus dominates the high intertidal zone because it is the only com-
mon primary space holder able to live at high intertidal heights. Mytilus typ-
ically replaces Semibalanus at intermediate elevations due to its competitive
dominance. Recruitment densities, however, also influence zonation pat-
terns on wave-exposed shores. Without sufficient recruitment to saturate the
available substrate space, competition for space does not become a major
force in determining organism distribution patterns (Fig. 5.43).
Variation in recruitment conspicuously affects barnacle population dy-
namics and morphology. At low densities, acorn barnacles grow into short,
squat individuals wider than they are tall. In contrast, at high recruit densi-
ties, crowding causes barnacles to grow up rather than out, since they are con-
strained by neighbors. Crowding has interesting consequences for barnacle
growth and reproduction, as well as population dynamics. Crowded barna-
cles invest less in structural support (shell material), since they are supported
by neighbors (Wu et al. 1977; Wu 1980). Moreover, since crowded individuals
are elevated higher above the surface, they experience higher food fluxes and
grow faster than solitary individuals (Pullen and LaBarbara 1991; Bertness et
al. 1998). Crowded, columnar barnacles have larger mantle spaces, permitting
218 ` CHAPTER 5

Wave-exposed open coast zonation

Barnacle zone

Mussel zone

Irish moss

Kelp zone

Protected coast zonation

Barnacle zone

Fucoid canopy
understory with
mussels,
barnacles,
snail grazers,
and predators

Irish moss

Algal crusts
Urchin barrens

Fig. 5.42 Some of the effects of wave exposure on rocky intertidal zonation are the
result of low consumer densities. The relative lack of predatory snails, starfishes,
and sea urchins on wave-exposed shores typically leads to conspicuous mussel and
kelp beds.

them to produce larger clutches of eggs (Wethey 1984a). Crowded barnacles

can also buffer one another from thermal stress and increase survivorship at
high intertidal heights (Bertness 1989). Balanced against these advantages of
crowding, however, are serious disadvantages. Overcrowding leads to intense
competition for space and structurally weak individuals that are easily crushed
 ROCKY SHORES ` 219

High recruitment Low recruitment

Group benefits lead to Lower, more ambiguous
organisms living at upper borders without
higher elevations group benefits

Diffuse zonation with

Intense less competition for
competition for space and consumer
space leads to pressure
strong zonal
boundaries Consumers have
less impact
controlling lower
Abundant borders
consumers control
lower borders

Fig. 5.43 Recruitment effects on rocky intertidal shoreline zonation patterns.

by neighbors or external forces (Barnes and Powell 1950; Bertness 1989).

The balance between these costs and benefits of crowding in barnacles is de-
termined by environmental conditions. In habitats where barnacle growth
rates are high (low intertidal and high-flow habitats), the disadvantages of
crowding typically lead to massive mortality of crowded individuals. In habi-
tats with low growth rates or harsh physical stresses, the advantages of
crowding can outweigh the disadvantages (Bertness 1989; Sanford et al. 1994)
(Fig. 5.44).
Mussel recruitment on wave-exposed shores is tightly linked to both
the supply of recruits and the presence of barnacles. Barnacles enhance
mussel recruitment, since mussels preferentially settle on and have higher

• Decreased skeletal support costs per individual

• Increased reproductive output per individual
• Increased buffering from thermal and
desiccation stress and mortality
• Increased food supply for individuals
elevated above the surface
• Reduced competition
for space and food

Fig. 5.44 Costs and benefits of crowding in acorn barnacles.

220 ` CHAPTER 5

Barnacle recruits increase surface

roughness

Enhanced
mussel
recruitment

Growth

Mussels overtake
barnacles

Fig. 5.45 By increasing surface roughness, the presence of barnacles can facilitate
the recruitment and competitive dominance of mussels. (After Menge 1976.)

survivorship on rough-textured surfaces (Menge 1976; Petraitis 1987). High

rates of mussel settlement on barnacles and rapid mussel growth and mo-
bility lead to mussels overgrowing and suffocating the barnacles. Thus, bar-
nacles facilitate mussel settlement, which paves the way for their ultimate
demise (Fig. 5.45).
Physical disturbances, common in all rocky intertidal systems, play a
large role in creating spatial patterns on rocky shores exposed to heavy
waves (Dayton 1971; Osman 1977; Sousa 1979a, 1985). Wave shock can rip
 ROCKY SHORES ` 221

organisms from the substrate (Menge 1976; Witman 1987), and waterborne
objects such as driftwood and stones (Dayton 1971; Shanks and Wright 1986)
can crash onto shorelines and destroy organisms. These physical distur-
bances kill sessile space holders, reduce competition for space, and stimulate
the invasion of competitively subordinate rapid colonizers. On wave-exposed
headlands in Maine, for example, winter wave exposure is often responsible
for scouring rocky shores of mussel recruits in all but refuge habitats.

Protected Shores
Zonation on protected shores in New England is strikingly different from
that on wave-exposed shores. The major similarity is the barnacle zone de-
marcating the upper intertidal border in both habitats. On protected shores,
there is often considerable free space (often more than 50 percent) at lower
elevations, few mussels, a profusion of seaweeds, and abundant mobile
consumers. Farther north, in the Canadian Maritimes, protected habitats
are strongly affected by ice, which is more common and heavier in bays
and estuaries than in coastal habitats. Bays and estuaries experience more
ice damage, since they are not as thermally buffered by the open ocean as
coastal habitats are, and because their lower-salinity waters freeze more
readily.
The intertidal community on protected rocky shores in New England
differs markedly from that on shores exposed to heavy waves, since con-
sumers become more important and a seaweed canopy of relatively unpalat-
able larger seaweeds, like Ascophyllum and Fucus, buffers understory organ-
isms from physical stresses. The algal canopy at middle elevations generally
supports a rich assemblage of organisms, many of which could not persist
at these intertidal heights without the cool, shaded, moist habitat provided
by the canopy. The herbivorous snails Littorina littorea and Littorina obtusata
limit the abundance of ephemeral algae and even the success beneath the
canopy of the algal sporelings of canopy-forming seaweeds. The carnivo-
rous snail Nucella, the starfish Asterias, and crabs limit the abundance of both
mussels and barnacles (Ebling et al. 1964; Menge 1976) (Fig. 5.46).
Northern acorn barnacles, while sparse, are often the most common ses-
sile understory animals. They live at much lower elevations on wave-
protected shores than on exposed shorelines, since mussels (their major spa-
tial competitors) are kept in check by predators under the canopy (Fig. 5.47).
Epiphytic algae (algae that grow on other algae), including ephemeral, op-
portunistic species like the sea lettuce Ulva and specialists like Polysiphonia,
grow attached to canopy seaweeds. They escape their herbivores by living
on unpalatable algae that are not heavily grazed (Harlin 1975, 1980). On ex-
tremely sheltered shores, sediment accumulation under the canopy pre-
cludes the successful recruitment and survival of most sessile organisms
characteristic of hard substrates, including barnacles and other seaweeds.
In New England, the smooth periwinkle Littorina obtusata is almost al-
ways found associated with algal canopies of the knotted wrack Ascophyllum
222 ` CHAPTER 5

All predators are strongly inhibited Mobile crab predators are Mobile crab predators limit
in the absence of algal canopies inhibited the abundance of slow-
Slow-moving starfish, sea moving predators and
Heavy competition for space
urchin and snail predators sessile space holders
limit sessile space holders

Wave-exposed Protected Bays and

open coast open coast estuaries

Fig. 5.46 The general influence of wave exposure on the predators and sessile space
holders of rocky shores.

nodosum. This snail resembles Ascophyllum air bladders, and may be camou-
flaged from predators in association with Ascophyllum. In Europe, green crabs
are important predators of this snail, and restrict smaller snails to high inter-
tidal heights and algal cover (Williams 1992) (Fig. 5.48). The relationship
between Littorina obtusata and Ascophyllum, however, has not been carefully
examined in North America. Periwinkles appear to rely on Ascophyllum for
cover and camouflage, but how much adult Ascophyllum they consume is
unclear. Their grazing on diatoms and epiphytes that grow on the canopy
could benefit Ascophyllum by limiting algal fouling, but this hypothesis has
not been critically examined.
The presence of an Ascophyllum canopy on New England rocky shores
is strongly correlated with wave stress. Ascophyllum canopies are absent from
heavily wave-exposed shores. They are present in protected open-coast sites,
but reach their most extensive development on the shores of protected em-
bayments (Leonard et al. 1998a). Ascophyllum recruits attach very weakly to
the substrate, limiting recruitment in wave-swept habitats (Vadas et al. 1990).
Even if recruits were able to settle in wave-exposed habitats, adult Ascophyl-
lum would probably be ripped from the substrate because of their large size.
Ascophyllum in open-coast areas is relatively short in comparison to individu-
als in protected bays, further suggesting that wave stresses can limit Asco-
phyllum success. Once a canopy is established, grazers limit the recruitment
of most algal sporelings, including those of species that are immune to herbi-
vores as adults (Lubchenco 1983; Bertness et al. 2002a). Adult Ascophyllum is
eaten infrequently due to a tough outer cuticle and chemical defenses.
Direct positive associations among sessile organisms that result from
neighbor amelioration of heat and desiccation stresses are important in
protected rocky intertidal communities (see chapter 4 for a general discus-
sion of direct positive interactions). Dense groups of barnacles, mussels, and
 ROCKY SHORES ` 223

Control
100

Semibalanus

Mytilus
0

Nucella excluded
100
Mytilus
Percentage cover

0 Semibalanus

100 Nucella excluded and Mytilus removed

Semibalanus
Fucus

1972 1973 1974

Fig. 5.47 An experiment demonstrating the effects of dog whelk (Nucella lapillus)
predation on protected New England rocky shores. (After Menge 1976.)

algae can all buffer group members from heat and desiccation stresses at high
intertidal levels and permit them to live at higher intertidal heights than
would be possible without neighbors (Hay 1981; Lively and Raimondi 1987;
Bertness 1989; Bertness and Leonard 1997). The presence of dense aggrega-
tions of seaweeds, barnacles, and mussels also ameliorates stressful physical
conditions for many associated organisms, such as snail and crustacean
consumers, allowing them to live at higher intertidal heights than they could
without these neighbors. Thus, positive associations among dense aggrega-
tions of mussels, barnacles, and seaweeds, in general, can set the upper inter-
tidal limits of intertidal organisms (Fig. 5.49).
At the upper border of the Ascophyllum canopy, a strip of bare space may
separate the canopy from the barnacle zone. This bare zone is the result of
224 ` CHAPTER 5

High intertidal
100
Adult snails

50

Juvenile snails
Percentage survival

Low intertidal
100

50

Adult snails

Juvenile snails
0
0 40 80
Time (days)

Fig. 5.48 Survival of tethered Littorina obtusata. Juveniles are heavily preyed upon
by green crabs at both high and low intertidal heights. Adult snails are preyed upon
only at low tidal heights, where larger crabs occur. (After Williams 1992.)

the whiplashing of algal fronds and the foraging of snail consumers that live
under the canopy (Menge 1978) (see Fig. 41). At its lower border, the Asco-
phyllum canopy is usually replaced by a zone of free space, rockweeds (Fu-
cus), and Irish moss (Chondrus). Occasional foraging by starfishes and urchins
in this zone leaves bare space, which is colonized by these algae (Lubchenco
1983). Predation by crabs and snails prevents mussels from displacing Chon-
drus, so that grazer-resistant adult Chondrus is the functional dominant in
this zone. Once established, Chondrus benefits from snail grazing, which
cleans it of epiphytes, and even bounces back from moderate urchin grazing
because its holdfast regrows new fronds when clipped back. Recent work by
Jay Stackowicz (2005) in Long Island Sound has shown that without grazing
by a guild of very small and inconspicuous snails, Chondrus is overgrown
and killed by a variety of fouling organisms.
 ROCKY SHORES ` 225

Mytilus Geukensia
100% 100%
Survival

Survival
0 0
Shaded Control Shaded Control Shaded Control Shaded Control
High zone Low zone High zone Low zone

With neighbors
Without neighbors
Ascophyllum
Fucus
100% 100%
Survival

Survival

0 0
Shaded Control Shaded Control Shaded Control Shaded Control
High zone Low zone High zone Low zone

Fig. 5.49 Group benefits for high rocky intertidal space holders. At their upper
intertidal borders, most common sessile organisms are dependent on their
neighbors for habitat amelioration and survival. Unless shaded, blue mussels,
ribbed mussels, and common rockweeds and barnacles suffer heavy mortality
without neighbors. (After Bertness and Leonard 1997.)

Tide Pools
The tide pools characteristic of New England shorelines have their own
zonation. Pools at high intertidal heights heat up rapidly and become hyper-
saline in the summer, and may become hypotonic due to rains and freeze in
the winter. These physical stresses limit the types of organisms that can live
in these pools. Pools at lower elevations are frequently flooded by tides,
which decreases these physical fluctuations. Large pools at lower elevations
may even be thermally and osmotically stable enough to support sea urchins,
which can limit fleshy algae, leading to a community of crustose algae and
animals (limpets, urchins, and chitons) similar to that found in subtidal habi-
tats (Fig. 5.50).
Algal abundance in tide pools is strongly influenced by herbivores. At
226 ` CHAPTER 5

Physically stressful conditions with few

organisms.

Increasing thermal and osmotic stress

Pools with intermediate stress levels,

Increasing tidal height

moderate grazing and diverse

seaweeds.

Physically benign pools with

heavy grazing and grazer-
resistant algae.

Increasing pool size (volume)

Decreasing thermal and osmotic stress

Fig. 5.50 Effects of the size and intertidal height of tide pools on their occupants.

intermediate intertidal heights, tide pools containing few periwinkle grazers

(Littorina) are dominated by rapidly colonizing ephemeral green algae, such
as Ulva and Enteromorpha, while pools with high periwinkle densities
are dominated by grazer-resistant algae such as Chondrus and Ralfsia. Jane
Lubchenco (1978) showed that these relationships are causal with manipula-
tive field experiments at Nahant, Massachusetts. Removing periwinkles led
to the invasion of Ulva, which ultimately dominated grazer-free tide pools,
competitively excluding other algae. Conversely, adding adult periwinkles
to pools dominated by ephemeral green algae led to only the most grazer-
resistant algal forms persisting. Pools that initially lacked snail grazers were
found to resist snail recruitment, since the algal canopy harbored crabs that
ate all snail recruits (Lubchenco 1978) (Fig. 5.51). Geoff Trussell and his col-
leagues (2004) have recently shown that green crabs do not have to actually
prey upon periwinkles to trigger algal-dominated tide pools. The simple
presence of green crabs in tide pools cause periwinkles to leave pools, lead-
ing to algal dominance. Trussell and colleagues found that adding crabs to
tide pools and crabs in vented plastic containers both led to periwinkles ex-
iting pools and the development of a green algal canopy. Since periwinkles
are relatively mobile, differences in tide pool algal composition driven by
snail densities also occur at larger, between-habitat spatial scales, as well as
within sites (Ron Etter, personal communication). At wave-exposed sites,
periwinkles are often rare, leading to tide pools with algal assemblages not
controlled by grazing. In contrast, at protected sites, periwinkles are often
common, and their grazing appears to control algal abundance and species
distribution patterns.
 ROCKY SHORES ` 227

High-diversity pools with snails Low-diversity pools without snails

Dominated by a mixture of palatable green Dominated by fast-growing, competitively
seaweeds (Ulva, Enteromorpha) and slower- dominant green seaweeds such as Ulva and
growing and well-defended species such as Enteromorpha. Green crabs colonize these pools
algal crusts (Lithothamnium) and Irish moss and can limit the recruitment of herbivorous
(Chondrus). snails.

Fig. 5.51 Jane Lubchenco’s (1978) demonstration of the relationship between grazers
and seaweed diversity in New England tide pools.

Maximum algal diversity in New England tide pools occurs at intermedi-

ate herbivore densities. This relationship between herbivore density and algal
diversity is a consequence of herbivore feeding preferences. Periwinkles pre-
fer ephemeral green algae (the competitively dominant algae in tide pools),
and intermediate snail densities increase diversity by preventing them from
competitively excluding grazer-resistant algae. In contrast, on nearby emer-
gent rock surfaces that dry during low tide exposure, the grazer-resistant
rockweed (Fucus) is competitively dominant, since it is resistant to both graz-
ing and desiccation, whereas Ulva and Enteromorpha are vulnerable to desic-
cation. As a result, high snail densities decrease algal diversity in these habi-
tats, because increased herbivory hastens the dominance of Fucus (Fig. 5.52).

Subtidal Zonation
The vertical zonation of New England rocky shorelines extends well into
subtidal habitats. Shallow subtidal habitats off sheltered rocky shores are
usually characterized by heavy urchin and starfish grazing that eliminates
most erect fleshy seaweeds. As a result, this zone is typically covered by pink
and red coralline crusts (Lithothamnium and Phymatolithon), the only algae ca-
pable of withstanding heavy urchin grazing. Dominance by coralline algae
is clearly grazer-dependent, since without constant grazing, algal crusts are
covered with sediment or overgrown and replaced by more palatable but
competitively superior erect algae (Dethier 1981; Slocum 1980). Removal of
urchins from shallow subtidal habitats leads to the establishment of a diverse
algal assemblage dominated by kelps, and the successful recruitment of ses-
sile invertebrates (Himmelman 1983; Witman 1985).
On wave-exposed shores in New England, kelps dominate shallow sub-
tidal hard substrates, but are usually replaced by horse mussel (Modiolus
228 ` CHAPTER 5

Species richness
Snail density

Tide pools
Snails eat ephemeral green algae, the competitive
dominant, increasing algal diversity at
intermediate grazer densities
Species richness

Snail density

Emergent rock
Snails eat ephemeral green algae, the competitive
subordinate, decreasing algal diversity;
Fucus dominates

Fig. 5.52 The differential effect of herbivore grazing pressure on algal diversity
in and out of tide pools. (After Lubchenco 1978.)

modulus) beds at depths greater than 10 meters (Fig. 5.53). The lower limit of
kelps is set by urchin grazing (Witman 1985, 1987). In the shallow subtidal
kelp zone, strong currents and storm surges limit the abundance of urchins.
Below the kelp zone, reduced wave disturbance allows the persistence of
urchins, which leads to the elimination of kelps, enabling horse mussel beds
to persist without kelp-induced dislodgment (Fig. 5.54). Removing urchins
 ROCKY SHORES ` 229

Wave dislodgment limits urchins;

kelps dominate

Reduced wave stress at intermediate

depths leads to urchins limiting kelps, so
horse mussel beds can persist

Shallow subtidal kelp zone

At lower depths, heavy urchin
grazing leads to the dominance
of algal crusts
Horse mussel and urchin zone

Algal crusts

Fig. 5.53 Shallow subtidal zonation of wave-exposed rocky shores in New England.
(After Witman 1987.)

from the horse mussel zone leads to kelps growing on horse mussel shells
and the subsequent dislodgment of the mussels during storms due to the in-
creased drag. Consequently, while mussels benefit from urchins grazing on
epiphytes, the urchins are hidden from their predators and protected from
wave dislodgment by the horse mussel beds. This association between horse
mussels and urchins is a good example of a facultative mutualism, in which
both participants benefit from the association, but neither is totally depend-
ent on it. Since horse mussel beds are pockets of high species diversity (Wit-
man 1985), this mutualism indirectly maintains diversity.
One of the most marked features of subtidal habitats in general is the
dominance of clonal organisms such as bryozoans, tunicates, and sponges. Je-
remy Jackson (1977) has argued that organisms with solitary body plans, such
as barnacles and mussels, dominate intertidal habitats due to their ability to
colonize highly physically stressful and disturbed habitats. In contrast, clonal
organisms dominate subtidal habitats due to their competitive dominance
over solitary organisms and their ability to rapidly cover primary space with
vegetative growth.

Protected Bays
In the Gulf of Maine, rocky shorelines in protected bays and estuaries differ
markedly from coastal habitats. These shorelines are characterized by less
230 ` CHAPTER 5

Kelps
Urchins
–

+
– +
–

Mussels

Urchins keep mussels

clean of kelp recruits

Mussels provide
spatial refuge
to urchins from
predators and
wave dislodgment

Without urchins, kelp

recruit to mussels,
increasing drag and
dislodgment

Fig. 5.54 Jon Witman’s

(1987) demonstration of
Without urchins,
the positive relationship
kelp beds ultimately
between horse mussel dominate
beds and sea urchins in
shallow subtidal rocky
habitats.
 ROCKY SHORES ` 231

wave energy, higher thermal stress, and increased crab predation relative to
coastal habitats. Tidal currents influence communities in these habitats much
as wave shock influences communities in coastal habitats. At the mouths of
bays or constrictions in estuaries, tidal currents are strong, and intertidal com-
munities resemble wave-exposed coastal habitats (Fig. 5.55). A high intertidal
barnacle zone gives way at intermediate intertidal heights to dense mussel
beds dominated by small individuals, with shallow subtidal habitats often
containing kelp beds. At nearby low-flow sites, a high intertidal barnacle zone
gives way in the middle intertidal to an Ascophyllum canopy, which is replaced
at low intertidal heights by a zone with considerable free space and patchy
mussel beds made up mostly of large individuals (Bertness et al. 2002a).
One of the most striking effects of increased flow on the structure of estu-
arine communities is that the zonation of sessile invertebrates and seaweeds
can be shifted higher by as much as a meter. High-flow sites are exposed to
increased fluxes of planktonic larval recruits and the particulate food of filter
feeders, leading to high barnacle, mussel, and herbivorous snail densities.
These high densities buffer sessile organisms from high intertidal physical
stresses, allowing these organisms to live at higher elevations than are possi-
ble at the low densities found in nearby low-flow habitats. At low-flow sites,
recruit and particulate food delivery is low, and the effect of predators is
much stronger than at high-flow sites. Intense snail grazing in low-flow habi-
tats can lead to a lack of seaweeds other than grazer-resistant canopy species,
and intense crab predation can restrict mussels to refuge habitats and large
size classes that are immune to predators (Leonard et al. 1998a).
South of Cape Cod, the open coast is generally dominated by soft-
substrate habitats, untouched by recent Ice Age scouring events. However,
the shorelines of Narragansett Bay and Long Island Sound have characteris-
tic cobble shores left by receding glaciers. Intertidal communities on cobbles
are simple for a number of reasons. First, they exist south of Cape Cod, a
major biogeographic boundary excluding many species of the rich boreal
Atlantic fauna. Second, these protected cobble beach habitats are thermally
stressful. They are isolated from the thermal buffering of coastal habitats,
and the smaller cobble substrate is thermally labile in comparison to large
rocks. Finally, these inland estuarine habitats have been exposed to large-
scale environmental insults for at least three centuries, and the effects of eu-
trophication, increased sedimentation, overfishing, and pollution on these
communities are difficult to estimate with certainty.
Cobble beaches in Narragansett Bay and Long Island Sound have a high
intertidal zone dominated by the cordgrass Spartina alterniflora or by bare
cobbles. At high intertidal heights, summer thermal effects are strongest,
and cobbles can be dislodged and abraded in winter, leaving them devoid of
cover. Cobbles that are embedded in the root mat of cordgrass are shaded
from heating, stabilized from rolling, and as a result are usually encrusted
with barnacles, rockweeds, and mussels. Cobble beach cordgrass stands
also buffer wave shock and facilitate the recruitment of other halophytic
(“salt-loving”) vascular plants. Atriplex, Suaeda, Salicornia, and Limonium, all
232 ` CHAPTER 5

High flow

• High delivery of recruits

• High growth rates of filter feeders and algae
• Low predator efficiency
• High competition for space
• Strong zonation

Mussel beds

Chondrus

Kelp
Low flow
• Low delivery of recruits
• Low growth rates of filter feeders and algae
• High consumer pressure
• Low competition for space
• More diffuse zonation

Barnacle zone

Fucoid canopy

Mussels restricted to
cracks and crevices

Mud crabs
in sediment

Fig. 5.55 High- and low-flow rocky intertidal habitats in tidal Maine estuaries.
(After Leonard et al. 1998a.)

plants found in salt marshes, are common on estuarine cobble beaches, but
are restricted to the zone immediately behind cordgrass stands (Fig. 5.56).
This pattern is the result of the cordgrass trapping the waterborne seeds of
these plants as well as limiting the direct effects of waves on the plants dur-
ing storms (Bruno 2000). John Bruno has found that on Narragansett Bay
 ROCKY SHORES ` 233

High intertidal with

cordgrass or loose
cobbles

Middle intertidal cobbles

with periwinkles, barnacles,
and algal crusts

Shallow subtidal with

sediment-covered cobbles,
heavy algal cover (Chondrus
and Codium), and large
whelks (Busycon)

Fig. 5.56 Southern New England cobble beach vascular plant communities are
composed of salt-tolerant plants characteristic of salt marshes. These communities
appear to be strongly influenced by both seed supply and physical disturbance.

cobble beaches more than twelve vascular plant species are dependent of cord-
grass beds to persist on cobble beaches, with some of them being dependent
on only the largest cordgrass beds, which maximize habitat modification by
cordgrass (Bruno 2002). Over longer periods of time, probably measured in
decades, the establishment of cordgrass on cobble beaches also appears to fa-
cilitate the successful establishment of other high marsh species (particularly
the marsh hay, Spartina patens). This enhances sedimentation and ultimately
leads to the development of typical high marsh plant communities. John
Bruno (2002) has suggested that cordgrass should be considered a foundation
species or ecosystem engineer, since it fundamentally changes the cobble
beach habitats that it colonizes through habitat modification.
The middle intertidal zone of cobble beaches in Narragansett Bay and
Long Island Sound typically consists of cobbles covered with barnacles,
fleshy algal crusts, and extremely high (600 to 1000 individuals per square
meter) densities of the herbivorous snail Littorina littorea (Bertness et al.
1983; Bertness 1984a; Petraitis 1987). These extremely high herbivore
234 ` CHAPTER 5

Snail removal

• Sediment accumulation
• Suffocation of algae
• Suffocation of barnacles

Without Littorina
With Littorina Community dominated by
Community dominated by
• Tube-building worms
• Barnacles
• Crustaceans
• Algal crusts
• Mud crabs
• Marsh grasses

Fig. 5.57 In southern New England, periwinkle grazing can maintain cobble beach
habitats by preventing sediment accumulation and the establishment of a soft-
sediment community. (After Bertness 1984a.)

densities, which are probably due to the lack of predators and competitors in
these habitats, exclude all algae other than herbivore-resistant leathery algal
crusts (Ralfsia and Hildenbrandia). Experimental removal of the common peri-
winkle from these cobble beaches has dramatic consequences, suggesting
that its reinvasion of the Atlantic coast after the last Ice Age has played a ma-
jor role in changing these shoreline landscapes. Snail removal leads rapidly
to the development of a dense algal canopy, the accumulation of sediment,
and the establishment of organisms typical of soft-sediment habitats (Bert-
ness 1984a). Without the snails, the barnacles and algal crusts typically found
in these habitats are covered with algae and suffocate under sediment. Thus,
the presence of the snail may have been responsible for shifting communities
in wave-sheltered habitats from soft-sediment assemblages dominated by
tubiculous worms, crustaceans, mud crabs, and marsh grasses to assem-
blages more typical of hard-substrate habitats. The mechanism of these ef-
fects is simple. High periwinkle densities continually clear hard surfaces of
diatoms, inadvertently preventing sediment accumulation and the develop-
ment of an algal canopy. In the absence of snails, algal canopies become es-
tablished, enhancing sedimentation and stabilizing sediments, and leading to
the recruitment of tube-building organisms, which further stabilize the sedi-
ment (Fig. 5.57).
Why Littorina is restricted to the intertidal zone of cobble beaches is un-
clear. The predatory whelk, Busycon, or predatory crabs may play a role in
limiting periwinkles to intertidal habitats, but this has not been experimen-
tally tested. As a consequence of Littorina staying in the intertidal zone year-
round, however, the shallow subtidal habitat has an algal canopy of Irish
moss, dead man’s fingers (Codium), and sea lettuce (Ulva). Without constant
 ROCKY SHORES ` 235

grazing, the subtidal habitat is covered with sediment and sediment-

dwelling organisms (Bertness 1984a).

CONSERVATION ISSUES

Rocky shores have historically been thought to be relatively immune to se-

vere environmental problems. Shorelines have been used for centuries for
the disposal of sewage and industrial wastes under the assumption that the
dilution of wastes in the vast ocean waters would render them harmless.
The open populations of most shoreline organisms have also long been as-
sumed to buffer them from overharvesting and local environmental contam-
ination. Most shallow-water marine organisms have pelagic dispersal, which
decouples adult benthic populations and opens them to heavy movement of
recruits between populations. This metapopulation structure has been sug-
gested to give local populations considerable resilience, or the ability to
bounce back from perturbations.
In spite of this rationale and the historical lack of concern, shorelines are
one of the most threatened environments on the planet. When Europeans
began colonizing the east coast of North America 300 years ago, western At-
lantic waters were teeming with cod, and lobsters were so common that they
were dug into the ground as fertilizer. The shores of Narragansett Bay, Long
Island Sound, and Chesapeake Bay were paved with dense oyster beds.
Now all of these major shoreline features are gone, and their loss has dra-
matically changed the dynamics and structure of shoreline communities.
The loss of cod and other nearshore fish predators to overharvesting has
probably had major effects on benthic prey populations (Witman and Sebens
1992). Similarly, the loss of oyster populations and their ability to increase
water clarity now prevents seagrass and seaweed beds from thriving in Nar-
ragansett Bay, Long Island Sound, and Chesapeake Bay (Ulanowicz and Tut-
tle 1992).
Jim Carlton (1993) has argued that changes in our coastal waters over
the past few centuries have led to numerous local and global extinctions.
Few of these have been documented, since the extinction of many rare or-
ganisms probably occurred before biologists had the opportunity to describe
them. The extinctions we are most aware of have occurred when the habitats
that specialist organisms depended on were destroyed. For example, the eel-
grass limpet, Lottia alreus, went extinct on the Atlantic coast of North Amer-
ica with the demise of shallow-water eelgrass beds in the 1930s (Carlton et
al. 1991; see chapter 6). Organisms dependent on bay and estuarine habitats
(such as oysters and scallops) are more at risk than those found in coastal
habitats because they are more heavily harvested and affected by human ac-
tivities. However, the vulnerability of even open ocean populations to hu-
man activities has recently been demonstrated with the unprecedented col-
lapse of the Atlantic cod and flounder fisheries of Newfoundland and
George’s Bank and the Pacific coast salmon fisheries and the near eradica-
236 ` CHAPTER 5

tion of large predatory fish from the world’s oceans (Baum et al. 2003; Myers
and Worm 2003).
Overharvesting, pollution, and species introductions are the most press-
ing conservation issues confronting contemporary nearshore communities.
These are all old problems that have affected shorelines for centuries, but
have become particularly important over the last few decades with increas-
ing population pressure and coastal development. Overexploitation of ma-
rine resources can have substantial direct and indirect effects on marine
communities. On rocky shores, harvesting of organisms by humans can de-
plete populations and change the size distributions of those organisms, with
the potential for cascading effects on shoreline communities (Castilla and
Duran 1985; Kingsford et al. 1991). Probably the best-known example of
human overexploitation triggering shoreline community changes was the
hunting of sea otters for fur. The decimation of Pacific coast sea otter popula-
tions early in the twentieth century led to a sea urchin population explosion
and the destruction of kelp beds from California to Alaska (Estes and
Palmisano 1974; Estes et al. 1978). Since kelp beds are important nursery
grounds for commercially important fish populations, there were serious
economic repercussions. East coast examples of community shifts due to
overharvesting include exploitation of sea urchins and oysters, as well as
commercial fishing.
One problem with the depletion of marine organisms with external fer-
tilization and pelagic larval dispersal is that populations can be reduced to
levels so low that fertilization and successful recruitment may be limited.
The potential importance of these Allee effects (see chapter 3) is just begin-
ning to be realized. For sea urchins, seaweeds, clams, and other organisms
that release their gametes into the water column, fertilization may not occur
at low densities due to gamete dilution. In addition, for sessile and slow-
moving organisms that need to settle with members of their own species,
densities below some threshold level may simply be too low for successful
recruitment to occur (Quinn et al. 1993). Understanding the importance of
these population success thresholds is vital in determining harvesting prac-
tices and designing refuge habitats. Reed (1990) has shown that with kelp,
high densities of sexually reproducing spores (one spore per square millime-
ter or more) are necessary to trigger pheromone-induced sperm release. This
entirely precludes kelp reproduction at low densities. Jim Quinn and his col-
leagues (1993) have shown that refuges from harvesting where Allee effects
do not limit populations are needed for the persistence of heavily harvested
shoreline organisms such as sea urchins. They also suggest that similar con-
siderations are needed in designing marine preserves (Fig. 5.58).
Pollution is an equally important threat to shoreline communities, espe-
cially in shallow coastal bays and estuaries. Sewage runoff, which is often
dumped directly into nearshore habitats, can influence these environments
by causing eutrophication and blooms of nuisance seaweeds, which displace
native plants and animals (Littler and Murray 1975; Valiela et al. 1992). Toxic
paints applied to boat bottoms to prevent fouling by marine organisms are
 ROCKY SHORES ` 237

Harvest
Survival

Subadults Survival

Fertilization Allee effect

Higher fertilization
Post-dispersal Allee effects success at high densities
Juveniles settle or survive better due to concentrated
with adults present gametes

Zygotes
Juveniles

Larval survival

Larval transport
OUT

Larval transport
IN

Fig. 5.58 Sea urchin population model, illustrating Allee effects. (After Quinn et al.
1993.)

another pervasive problem in nearshore waters. They can leach into the wa-
ter, killing many organisms. In Europe, fouling paint use has been linked to
the decline of predatory snail populations in port cities (Gibbs et al. 1988).
Oil pollution, however, may be the most widespread threat to our shore-
lines (Suchanek 1993). It has been estimated that at least 4 billion liters of oil
enter the oceans each year as a result of human activities. Surprisingly, only
12 percent of this occurs due to tanker spills, and only 8 percent of this oil is
released in normal tanker operations. The majority of oil pollution (over 36
percent) comes from the runoff of municipal and industrial wastes. Oil can
clearly cause both chronic problems associated with its consistent presence
in marine systems and acute problems associated with spills and natural
disasters.
On rocky shores, not all organisms respond in the same way to oil. Mo-
bile organisms such as crabs, echinoderms, gastropods, amphipods, and
some long-lived seaweeds are extremely vulnerable to oil, and their loss can
lead to dramatic changes in shoreline populations, which may take many
years or decades to return to their original state (Suchanek 1993). To date,
238 ` CHAPTER 5

however, the response of shoreline systems to chronic and/or acute oil pol-
lution is not well understood.
Introduced species are another major concern on western Atlantic rocky
shores. Introduced species have become so common on temperate zone
shorelines that it is difficult to reconstruct what native communities were re-
ally like before the invasions occurred. In the western Atlantic, the major
shell-crushing predator Carcinus maenus and some of the most dominant sub-
tidal spatial competitors (Codium fragilis spp. tomentosoides, the lacy bryozoan
Membranipora membranacea, and the encrusting sea squirt Botryloides schleseri)
are all recent rocky shore introductions. In shallow water New England kelp
bed communities the introduced bryozoan Membranipora has been shown to
overgrow and kill native kelps, which are then replaced by a second invasive,
the dead man’s fingers Codium. Thus, in New England kelp beds one intro-
duced species is facilitating the success of a second introduced species lead-
ing to the collapse of the native community (Levin et al. 2002). Since intro-
ductions are continuing at a rapid rate, temperate zones around the globe are
becoming a homogeneous mix of world-traveling hitchhikers that are dis-
placing many indigenous organisms and entire native communities. Nearly
half a century ago, Charles Elton called this homogenization of the world’s
biota the most dramatic biological change that the earth has ever experi-
enced. Nowhere is this happening at a more rapid rate, or with greater conse-
quence, than in nearshore marine environments.

SUMMARY

Rocky intertidal communities are one of the best-studied natural assemblages

because of their conspicuous spatial patterns, aesthetic appeal, and relative
ease of experimental examination. On the Atlantic coast of North America,
rocky shores are restricted to New England and Canada, where recent Ice Age
glaciers have scoured the shores of the sediments that cover the southern
coastline.
The food chains of rocky intertidal habitats are dependent on two food
sources. First, filter-feeding barnacles and mussels tap the plankton food
supply in the water column, linking shoreline communities with water col-
umn processes. Second, herbivorous snails and urchins consume benthic al-
gae ranging from diatomaceous films on hard surfaces to large seaweeds.
Rocky shorelines are characterized by striking elevational zonation, par-
ticularly where recruitment does not limit population densities and space
for sessile organisms is limited. New England rocky shores are remarkably
harsh physical habitats in terms of temperature fluctuations and desiccation,
even in comparison with other temperate rocky shores around the world. As
a general rule of thumb, the upper intertidal limits of rocky shore organisms
are set by physical stresses and the mortality of recruits at higher elevations,
whereas the lower intertidal limits are set by biological factors, such as con-
sumer pressure and competition. In New England, drilling snails and
 ROCKY SHORES ` 239

starfishes are dominant predators in open-coast habitats. In bays and estuar-

ies, rock and green crabs are dominant predators. Northern acorn barnacles,
blue mussels, and seaweed canopies are dominant spatial competitors at
middle to high intertidal heights on many New England shorelines, but are
displaced by clonal invertebrates at lower elevations.
Most research on process and pattern on New England rocky shores
has focused on the role of consumers and competition in generating dis-
tribution patterns. Positive associations among organisms and habitat-
modifying bioengineers, however, are also clearly important organizing
forces in these habitats. The upper intertidal limits of barnacles, mussels,
and algal canopies are all strongly affected by habitat-ameliorating group
benefits. Without neighbors, solitary individuals of all these organisms
have lower survivorship due to heat and desiccation stresses. The algal
canopies and mussel beds common on New England rocky shores are also
important autogenic bioengineers that influence their habitats and the or-
ganisms that live there. Algal canopies and mussel beds both typically sup-
port a rich assemblage of organisms that are largely dependent on them for
their persistence.
Whereas rocky shores have long been thought to be relatively immune
to environmental problems due to the open populations of many shoreline
organisms and the vastness of the sea, they are currently being seriously
threatened. Pollution, overexploitation of commercially harvested species,
and species introductions are dramatically changing our shorelines. It is a
formidable challenge for us to understand them before they are irreversibly
changed.

FURTHER READING

Little, C. and J. A. Kitching. 1996. The Biology of Rocky Shores. Oxford University
Press, New York.
Lobban, C. S. and P. J. Harrison. 1994. Seaweed Ecology and Physiology. Cambridge
University Press, Cambridge, UK.
Menge, B.A. and G. Branch. 2001. Rocky Intertidal Communities. In: Marine
Community Ecology, M. D. Bertness, S. D. Gaines, and M. Hay (eds.). Sinauer,
Sunderland, MA.
Moore, P. G. and R. Seed (eds). 1995. The Ecology of Rocky Coasts. Hodder &
Stoughton, London.
Newell, R. C. 1979. The Biology of Intertidal Animals. Marine Ecological Surveys,
Faversham, UK.
Paine, R. T. 1994. Marine Rocky Shore and Community Ecology: An Experimentalist’s
Perspective. Ecology Institute, Oldendorf/Lohe, Germany.
Raffaelli, D. and S. Hawkins. 1996. Intertidal Ecology. Chapman & Hall, New York.

Key References for Atlantic Coast Rocky Intertidal Communities

Bertness, M. D. and G. H. Leonard. 1997. The role of positive interactions in
communities: Lessons from intertidal habitats. Ecology 78: 1976–1989.
240 ` CHAPTER 5

Etter, R. J. 1988. Physiological stress and color polymorphisms in the intertidal snail
Nucella lapillus. Evolution 42: 660–680.
Leonard, G., J. M. Levine, P. Schmidt, and M. D. Bertness. 1998. Flow-generated
bottom-up forcing of intertidal community structure in a Maine estuary. Ecology
79: 1395–1411.
Lubchenco, J. 1978. Plant species diversity in a marine intertidal community:
Importance of herbivore food preference and algal competitive abilities. American
Naturalist 112(983): 23–39.
Lubchenco, J. 1980. Algal zonation in the New England rocky intertidal community:
An experimental analysis. Ecology 61(2): 333–344.
Menge, B. A. 1976. Organization of the New England rocky intertidal community:
Role of predation, competition, and environmental heterogeneity. Ecological
Monographs 46: 355–393.
Steneck, R. S. and M. N. Dethier. 1994. A functional group approach to the structure
of algal-dominated communities. Oikos 69: 476–498.
Steneck, R. S. and L. Watling. 1982. Feeding capabilities and limitation of
herbivorous molluscs: A functional group approach. Marine Biology 68: 299–319.
Wethey, D. S. 1985. Catastrophe, extinction and species diversity: A rocky intertidal
example. Ecology 66: 445–456.