EIGHTEEN

ECOSY
Intertidal
CAROL A . B L ANCHE T TE , M AR K W. DENNY, JOHN M . ENG LE , BR IAN
HELM UTH, LU KE P. M I LLER , K AR INA J. N IELSEN, and JAYSON SM ITH

Introduction

Intertidal ecosystems exist at the interface between land and a surprising, incredibly high diversity of species. As John Stein-
ocean, occupying the thin strip of shoreline that is regularly beck famously noted in The Log from the Sea of Cortez, “The
covered and uncovered by tides. At the highest of tides these exposed rocks had looked rich with life under the lowering
ecosystems are covered or regularly splashed by water, and on tide, but they were more than that: they were ferocious with
the lowest of tides they are fully uncovered and exposed to air. life. . . . Mussels, sculpins, kelps, and urchins; anemones and
Because intertidal organisms endure regular periods of immer- sea stars of all sizes and colors; barnacles, worms, limpets, and
sion and emersion, they essentially live both underwater and abalone; algae that look like corals; others that look like tar—​
on land and are adapted to a large range of conditions. Since the diversity of rocky shores rivals that of tropical rainforests.”
most intertidal organisms are primarily marine in evolution- Intertidal habitats can have either soft-bottom or hard-bot-
ary origin, they benefit greatly from immersion in seawater tom substrates. Soft-sediment habitats include sandy beaches
during high tide, which moderates temperature, delivers food and intertidal wetlands such as mudflats and salt marshes.
and nutrients, and facilitates reproduction by mixing gametes Soft-bottom habitats are generally protected from large waves
and transporting larvae. During low-tide periods, when organ- but tend to have more variable salinity levels. They also offer
isms are uncovered, they can experience large changes in tem- a third habitable dimension—​depth; many soft-sediment
perature, ultraviolet and solar radiation, desiccation, and even inhabitants are adapted for burrowing. Hard-bottom inter-
salinity from freshwater inputs or evaporation. Intertidal eco- tidal habitat can consist of either human-made (e.g., jet-
systems also occur where wave forces and impacts are great- ties, pilings, and seawalls) or natural rock surfaces. Natural
est. The high hydrodynamic forces imposed by intense wave rocky shores are found along exposed headlands as well as
action can crush, break, and dislodge intertidal organisms. in more wave-protected habitats. They range from consoli-
Given the severity and challenges of this environment, the dated rocky benches to cobble beaches. Many of the organ-
intertidal ecosystems of rocky shores in California are home to isms found on rocky shores are sessile and live attached to

337
the rock, although a wealth of mobile predators and grazers elegantly described the seashore as “probably the most prolific
of these sessile organisms inhabit the shore as well. Because zone in the world, a belt so thickly populated that often not
other chapters in this book examine sandy beaches and wet- only is every square inch of the area utilized by some plant
lands, this chapter focuses on the intertidal ecosystems of or animal, but the competition for attachment sites is so keen
rocky shores. that animals settle upon each other—​plants grow upon ani-
Rocky intertidal habitats provide a range of ecosystem ser- mals, and animals upon plants” (quoted in Tamm 2004:86).
vices such as shoreline stabilization and protection of upland Until the early part of the twentieth century, much of
areas from the wave erosion and the impacts of storm surges marine biology and ecology was descriptive and followed in
and sea level rise. They provide haul-out areas for seals and the traditions of early plant ecologists (Benson 2002). Rick-
support the diets of foraging birds as well as other diverse etts was one of the key marine scientists of the 1930s to pio-
organisms vital to the base of the food web (UNEP 2006, neer the modern approach to community ecology of rocky
Arkema et al. 2013). Rocky intertidal ecosystems also support shores. Community ecologists investigate patterns, processes,
valuable recreational and commercial fisheries for inverte- and mechanisms that describe or explain the composition
brates such as mussels and limpets and for edible seaweeds. and dynamics of populations interacting and persisting in
They provide for subsistence, ceremonial, sport, and com- a particular habitat. Huge advances in intertidal community
mercial gathering and hunting of a diversity of intertidal ecology in the 1930s and 1940s were facilitated by marine
organisms. Finally, rocky shores are greatly valued for their laboratories, primarily on the California coast. The Hopkins
aesthetic qualities and offer easily accessible coastal areas for Marine Station (Stanford University), the Kerckhoff Labora-
recreation, education, and research. In an attempt to quan- tory (Caltech), and the Scripps Institution of Oceanography
tify these values, Hall et al. (2002) estimated a mean of $7 per (UC San Diego) operated year-round with full-time research
family per visit that users would be willing to pay to prevent staffs by 1930. George MacGintie, the founder of the Kerck-
reductions in the status of southern California’s rocky inter- hoff laboratory, known for his studies of Elkhorn Slough (Mac
tidal zone. Ginitie 1935), argued strongly for more long-term field stud-
Rocky intertidal shores occur along the entire length of ies. Willis G. Hewatt of Hopkins Marine Station adopted Mac
the California coastline. In some regions, long stretches of Ginitie’s recommendation for long-term study but also incor-
rocky habitat dominate the shoreline, while in others (south- porated field experiments to investigate community dynam-
ern California, in particular) small rocky outcroppings are ics (Hewatt 1937). Their work catalyzed a new approach to
separated by long expanses of sandy beaches. Approximately the study of the dynamics of intertidal communities. From
800 miles of rocky habitat occur along the California coast, these humble beginnings, scientists studying rocky intertidal
comprising about 35% of the entire shoreline of California’s ecosystems have steadily continued to expand the science of
outer coast. Rocky shores support an array of intertidal spe- ecology, developing new theories and insights about commu-
cies living on rock faces, crevices, undersides, and tide pools. nity and ecosystem dynamics both in the intertidal and more
Some coastal areas, particularly rocky headlands and exposed broadly.
outer coasts, experience tremendous wave action; here only
the most tenacious organisms survive. Sheltered embayments
and coastal areas protected by offshore rocks, reefs, or islands The California Coast
receive considerably less wave shock and support a variety of
more delicate forms. The ability to withstand desiccation and Coastal Geology and Topography
overheating while exposed to air by low tides is an impor-
tant factor in determining where marine organisms occur in California is one of the most biologically and geologically
the intertidal. Organisms living in tide pools of many rocky diverse regions in North America. The current geological
shores avoid some of the problems associated with desiccation configuration of the California shoreline arises from tectonic
but must still contend with elevated temperatures and rapidly activity over millions of years (Hayes and Michel 2010). The
changing salinities and oxygen levels. majority of California’s coast, from the southern border with
Baja north to Mendocino, sits on the Pacific plate. Many of
the rock formations that make up this coastline (those of the
Significance and History of Rocky Franciscan complex) were accreted onto the edge of the
Intertidal Research North American plate starting about 150 million to 130 mil-
lion years ago as the Farallon plate and later the Pacific plate
We cannot begin a discussion about California’s rocky inter- were subducted beneath the North American plate. Between
tidal ecosystems without reference to Ed Ricketts. Ricketts 10 million and 30 million years ago, the Pacific plate stopped
was a scientist and careful observer of nature who opened subducting and instead began to travel northwest relative
a biological supply company in Pacific Grove, California, in to the North American plate. This shift gave rise to the San
1923. He collected and observed organisms and became one Andreas fault, which turns offshore near Mendocino toward
of the first marine biologists to describe them in an ecologi- the north. Both the accreted marine sediments of the Fran-
cal context. His classic book Between Pacific Tides, coauthored ciscan complex and granite formations originally from the
with Jack Calvin and J. Hedgpeth and published in 1939, is southern Sierra Nevada mountains have been carried to their
widely regarded as the authoritative text on intertidal ecol- current locations by the northwest movement of the Pacific
ogy. It continues to be revised and expanded and remains as plate (Harden 2004).
an important point of reference for marine biologists. Ricketts In places where sedimentary rock (e.g., sandstone, mud-
stone, or shale) makes up the shore, erosion often forms
broad, intertidal benches (Figure 18.1). By contrast, erosion-
Photo on previous page: A diverse community of intertidal algae
and animals from the wave-swept shores of Monterey Bay. Photo: resistant igneous and metamorphic rocks (e.g., granite, basalt,
Luke P. Miller. schists) are typically cut into steep, topographically complex

338  Ecosystems
 FIGURE 18.1 Examples of an easily eroded
sedimentary intertidal bench (above) and an
erosion-resistant granite shoreline with high
topographic relief (below). Photos: Jayson Smith
(above), Luke P. Miller (below).

shapes (Griggs and Trenhaile 1997). The resulting intersper- ing glacial maxima, and (3) subsequent tectonic uplift of the
sion of erosion-prone and erosion-resistant rocks determines shoreline out of reach of the waves when sea level rises again
the overall pattern of alternating headlands and beaches during glacial minima. Several periods of sea level change
along the southern and central California coasts. North of and continued tectonic uplift have created multiple, stepped
Mendocino, the shoreline is a product of recent subduction, marine terraces throughout San Diego, Orange, Los Angeles,
volcanic activity, and other orogenic processes. The verti- San Luis Obispo, Santa Cruz, San Mateo, Mendocino, Hum-
cal location of wave-induced erosion depends on sea level, boldt, and Del Norte Counties. These areas are often flanked
which has fluctuated through geological time in conjunction by present-day rocky intertidal benches (Griggs et al 2005).
with the coming and going of ice ages. Currently, sea level is
120 meters higher than at the peak of the last ice age, and it is
rising at a rate of at least 22 to 44 centimeters per century as Biogeographic Patterns
Earth warms (Harden 2004).
The large-scale pattern of California coastal topography is Biogeographic patterns of California’s rocky intertidal com-
modified by small-scale geological processes: folding, terres- munities have strong spatial structure and correlate closely
trial erosion, and local uplift or subsidence. The most obvious with both geography and sea surface temperature patterns
results of some of these processes are the marine terraces (Blanchette et al. 2008, 2009). Temperature is a useful proxy
found along much the coast. Marine terraces are formed by for tracking the movement of oceanic water masses. Tem-
(1) the erosive activity of waves, which sculpts wide benches perature can also directly affect critical biological functions
in the intertidal zone, followed by (2) sea level declines dur- including growth, survival, and reproduction. Biogeographic

In tertidal  339
 23.0 They experience variable mixing between the cold waters of

120 W

118 W
22.5
the California current and the warm, nearshore waters of the
southern California countercurrent (Huyer 1983, Hickey et
22.0
al. 2003). As on the mainland, temperature strongly deter-
21.5 mines the composition of Channel Island intertidal commu-
21.0 nities (Figure 18.3).
20.5
20.0
The Physical Environment
19.5

Temperature °C
19.0 The effects of the exceptionally severe intertidal environment
18.5 on population and community dynamics appear at many dif-
34 N 18.0 ferent scales, from regional-scale variation in the timing and
amplitude of tidal fluctuations to local topographic effects on
17.5
exposure of individuals to stressful hydrodynamic forces and
17.0
temperatures. The alternating exposure of intertidal organ-
16.5 isms to aerial and marine conditions is controlled largely by
16.0 the cycle of the tides. As the moon orbits Earth, and Earth
15.5 orbits the sun, gravity and celestial motion interact with the
15.0 ocean to create the a periodic fluctuation in sea level—​the
tides—​that determines how often and for how long shoreline
14.5
organisms are exposed to terrestrial conditions. The temporal
N0AA-14 NLSST SPLIT 1998/08/31 04:09:20 PDT 14.0 and spatial variation of the tides underlies all other aspects of
the intertidal physical environment.
FIGURE 18.2 Biogeographic patterns of rocky intertidal community
Two high tides and two low tides occur in the course of
structure at the California Channel Islands. Sites with dots of
the same color are most similar to one another in their species each tidal day (24 hours, 50 minutes). On the coast of Cali-
composition. Community similarity is strongly influenced by sea fornia the two high tides have different heights, as do the
surface temperature. Source: Blanchette et al. 2009. low tides—​a pattern know as mixed semidiurnal tides (Fig-
ure 18.4). The inequality of high tides and low tides means
that organisms low in the intertidal zone (below the higher
patterns of community similarity along the west coast of low tide) are emersed only once a day. Similarly, organisms
North America largely involve shifts in relative abundances high in the intertidal zone (above the lower high tide) are
of taxa rather than wholesale changes in species assemblages immersed only once a day. In contrast, organisms in the mid-
among regions. Many of the most abundant species charac- dle of the zone make the transition from air to water and
terizing particular biogeographic regions are not absent from back twice a day. These patterns of immersion and emersion
any region, but differ consistently and substantially in abun- strongly influence the stress to which the physiology of inter-
dance among regions. However, several exceptions to these tidal plants and animals must adapt.
general grouping patterns occur, suggesting that while similar The amplitude of the tides (the difference between higher
processes shape species distributions and abundances across high tide and lower low tide) is typically 1–​3 meters but
taxa and life histories, important local features such as topog- varies with the moon’s phase and the seasons. Tidal ampli-
raphy, geology, and wave exposure, as well as species interac- tude is greatest when the moon is new or full (spring tides)
tions, can also be important drivers of rocky intertidal com- and least at the first-quarter and third-quarter moons (neap
munity composition (Blanchette et al. 2008). tides). The disparity of the tides (the difference between
All major California rocky intertidal biogeographic regions higher and lower high tides and between higher and lower
are delimited by coastal features associated with transitions low tides) is typically greatest near the summer and winter
in oceanographic conditions, and/or changes in geomor- solstices and least near the spring and fall equinoxes. Spring
phology and substrate type (such as long stretches of sandy tides are most notable because they emerse organisms lower
beaches or changes in coastline orientation) (Blanchette et al. on the shore than other tides do in the remainder of the
2008). Point Conception is one of the most notable transition tidal cycle.
regions on the California coastline and the most important A variety of secondary factors modulates these general
biogeographic and oceanographic discontinuities on the west patterns. Because the moon’s orbit is elliptical, the distance
coast of North America (Figure 18.2; Valentine 1966, Doyle between Earth and the moon varies. The moon’s gravita-
1985, Burton 1998). Two major water masses meet here—​ tional effect on the ocean therefore fluctuates by almost 40%
the southward-flowing California current and the westward- over the 27.3 days of its orbital period. When the moon’s
flowing southern California countercurrent (Hickey 1993). closest approach to Earth coincides with new or full moon,
The northern region experiences consistent, strong, coastal tidal amplitude increases, exposing plants and animals that
upwelling that brings cold, nutrient-rich waters to the sur- otherwise would not be emersed. The reverse occurs when
face, resulting in both cold coastal sea surface temperatures the moon is farthest from Earth. Similarly, tidal amplitudes
and high nutrient concentrations. The Santa Barbara Chan- increase when Earth is nearest the sun (early January) and
nel, immediately southeast of Point Conception, experiences diminished when Earth is farthest away (early July). The angle
weak seasonal upwelling, which tends to occur in the winter between the plane of the moon’s orbit and Earth’s equato-
months (Blanchette et al. 2002, Winant et al. 2003). The Cali- rial plane varies with a period of 18.6 years, which can also
fornia Channel Islands, located just offshore from Point Con- affect the amplitude and disparity of the tides (Denny and
ception, lie within this highly diverse oceanographic region. Paine 1998).

340  Ecosystems
 FIGURE 18.3 Rocky intertidal community buried by sand in July. Photo: Carol
Blanchette.

Because the tidal day is slightly longer than the solar day
(24 hours), the timing of the tides shifts. For example, lower
2 Higher high
low tide tomorrow is (on average) 50 minutes later than it was

Disparity
Tidal elevation (m)

today, although the precise timing is affected by the ampli-

Amplitude
high
California coast also varies with latitude—​the farther north, 1
the later the tide. An 8:00 low tide in San Diego does not Higher low

Disparity
reach Point Reyes until 9:30 and Humboldt Bay until 10:15. Mean lower low
Summertime spring low tides in California typically occur Water
0
in the morning, so this latitudinal shift in the time of the
tide means that the farther north a site, the more time it is Lower low
exposed to potentially stressful midday terrestrial conditions.
Both the timing and amplitude of tides can be affected by –1
0 8 16 24 32 40 48
seafloor topography. Tides inside the San Francisco Bay have
much lower amplitude and occur nearly an hour later than Hours
tides just outside, for instance. For an accurate prediction of FIGURE 18.4 Example of mixed semidiurnal tides, in which there are
the tides at any particular location, it is best to consult the two high tides and two low tides differing in amplitude every lunar
site-specific predictions provided by the National Oceano- day. Source: Denny 1988.
graphic and Atmospheric Administration (http://www.tide
sandcurrents.noaa.gov/). Even then, one can expect some
deviation of actual tides from those predicted—​as much as warmer than the annual minimum. By contrast, the low spe-
10–​2 0 centimeters—​due to weather-driven changes in baro- cific heat of air allows for rapid changes in temperature; air
metric pressure. For more detailed explanation of the tides, temperature can vary by more than 20 oC in a single day.
consult Brown et al. (1999) or Cartwright (1999). Air and water temperature variations contribute to varia-
tion in the body temperatures of intertidal organisms. Dur-
ing submersion at high tide, the water’s high thermal con-
THE CONTR AST BET WEEN TERRE STRIAL ductivity ensures that the temperature of an organism is the
AND AQUATIC ENVIRONMENTS same as the water around it. Thus submerged body tempera-
ture can vary by at most a few degrees Celsius in a day as the
The physical differences between seawater and air have pro- sun heats surface waters or upwelling delivers cold subsurface
found effects on individual physiology and community struc- water. During aerial exposure at low tide, body temperatures
ture (Denny 1994). Many of these effects are tied to tempera- of intertidal organisms are affected by air temperature but
ture and therefore to the specific heat capacities of these two also by the multiple, interacting environmental factors (e.g.,
media. Specific heat capacity is the amount of heat energy solar heating, conduction of heat to or from the rock, evapo-
required to raise the temperature of 1 kilogram of a substance rative cooling). As a result, on sunny days, the body tempera-
1oC. Water has an unusually high specific heat capacity, more ture of intertidal organisms can be considerably warmer (10–​
than four times that of air. As a result, water temperature var- 15°C) than the surrounding air and can vary over very fine
ies much less than air temperature. In Monterey, for instance, spatial scales; animals on south-facing sides of rocks can be
annual maximum sea surface temperature is 16oC, only 6oC many degrees hotter than nearby animals on shaded surfaces

In tertidal  341
(Helmuth and Hofmann 2001, Denny et al. 2011). Emersed the upper portion of the water column to a shoreward-seaward
body temperature can also be colder than the surrounding oscillation extending all the way to the seafloor. An increase in
air, especially at night, as organisms lose heat by infrared velocity accompanies this shift in flow pattern. In deep water a
radiation to the sky. wave with a period of 10 seconds and a trough-to-crest height
The temperature of an organism’s body affects most phys- of 1 meter causes a maximum water velocity of 0.3 meter per
iological processes, such as metabolic rate (Jansen et al. second. When the same wave has shoaled to a depth of 2
2007) and efficiency of enzyme functioning (Somero 2011). meters, velocity increases tenfold. As waves shoal even fur-
Increases in metabolic demand, and thus oxygen demand, in ther—​to a depth approximately equal to their height—​they
turn can lead to oxygen deficiency at the cellular level (Pört- break. Breaking sets the maximum velocity waves can pro-
ner and Farrell 2008). While the relative importance of inter- duce before reaching shore. Velocity at the crest of a break-
tidal body temperatures in water and in air remains unclear, ing wave is approximately 4.4 times the square root of wave
and varies between species, both can have significant effects height, more than 4 meters per second for a 1 meter high wave
on rates of mortality, growth, and reproduction (Blanchette et and more than 6 meters per second for a 2 meter high wave.
al. 2007, Somero 2011). Experiments show that these impacts Whether these high velocities are imposed on benthic
can be due to both rare but extreme events (Harley and Paine organisms depends in large part on the slope of the seafloor. If
2009, Denny et al. 2009) and chronic exposure to suboptimal the slope is gradual, waves break seaward of the intertidal zone
temperatures (Petes et al. 2008, Sará et al. 2011 and 2012). and lose energy (and velocity) to viscous turbulent processes
For example, Harley (2008) reported mortality of mussels and as they move up the shore. In this case the intertidal com-
limpets in March and April 2004 in Bodega Bay, California, munity is relatively protected. By contrast, if the shore slopes
following exposures to a series of sunny, warm days when low steeply, waves break directly on the intertidal zone, where
tide exposed animals to the air during the mid-day. crest velocity can be amplified by the water’s interaction with
Evaporative cooling allows organisms to avoid (or at least the rock’s small-scale topography. When this occurs, veloci-
postpone) high temperature stress. Each gram of water evapo- ties of 10 meters per second are common, and storm waves
rated removes 2,500 joules of heat energy from the organism. can cause speeds in excess of 30 meters per second (approx-
Excessive water loss can be lethal, however. Thus a trade-off imately 67 miles per hour). Where shoreline topography is
exists between desiccation and thermal stress. Many mobile complex, water velocity can vary substantially over short dis-
organisms seek refuge from potentially desiccating condi- tances. While the seaward faces of rocks might see extremely
tions underneath algal canopies or in crevices and tide pools. high water velocities, the leeward sides of the same rocks can
Some intertidal animals (e.g., littorine snails [Littorina spp.]) be relatively sheltered, allowing a different suite of animals
retreat into their shells at low tide, sealing in water and rely- and plants to survive. The exposure of a site also depends on
ing instead on their ability to cope with subsequent high tem- the direction from which waves arrive. Waves that approach
peratures. Lacking shells or waxy cuticles, seaweeds readily on a path perpendicular to shore lose the least energy before
lose water, allowing them to stay cool for a time. Seaweeds reaching the intertidal zone and therefore have the greatest
have also evolved physiological mechanisms to cope with the impact. Those approaching on a path more parallel to shore
resulting desiccation. have a smaller effect.
In addition to temperature and desiccation stress, inter- Wave-induced water velocities have both detrimental and
tidal organisms must contend with broad variation in salin- beneficial effects. Hydrodynamic forces (drag and lift) are pro-
ity, sand burial, and other conditions. Variability in salinity portional to the square of velocity (Vogel 1994), and—​g iven
is typically low during high-tide submersion but can increase the extreme velocities associated with waves—​can pose chal-
dramatically at low tide during rain events or from exposure lenges for intertidal organisms. Many organisms found on
to freshwater runoff from streams or storm drains. Movement wave-swept shores, such as limpets (e.g., Lottia spp.) and chi-
of sand along the coast can bury intertidal organisms in sea- tons (e.g., Leptochiton spp.), have evolved unique, low-profile
sons of limited wave scouring, typically in summer (see Fig- shapes to reduce the forces imposed on them by waves and
ure 18.3). Sand movement and tolerance of sandy conditions to reduce their likelihood of becoming dislodged by wave
is especially important for rocky intertidal communities in action. Wave-induced disturbance (when organisms are torn
southern California, where rocky benches are typically inter- from the rock by wave action) has important ecological con-
spersed with long stretches of sandy beach. sequences for the diversity and function of rocky shore com-
munities. For example, the California mussel Mytilus cali-
fornianus is the competitive dominant for space on exposed
WAVE E XPOSURE shores in California, but forces imposed by breaking waves
can rip them from the rock. Although this disturbance harms
As winds blow, they transfer energy to the ocean surface, pro- mussels, the dislodged animals are food for sea anemones,
ducing waves (Denny 1988). In the area directly affected by and the open space they leave behind makes room for fugitive
wind, waves—​k nown as seas—​a re steep and disorganized, species such as the sea palm, Postelsia palmaeformis (Dayton
with periods of 4 to 6 seconds. But waves can travel great dis- 1973, Paine 1988, Blanchette 1996). Hydrodynamic forces can
tances; as they move away from the winds that generated also constrain movement by predators and herbivores, which
them, their character gradually changes. Waves that arrive is bad for the consumers but good for their prey. The same
from a distant storm—​k nown as swell—​oscillate with peri- forces that cause disturbance also splash water high on the
ods of 8 to 20 seconds. On a typical day the waves imping- shore, transporting food to barnacles (Cirripedia) and keep-
ing on a shore are a complex combination of seas and swell. ing both plants and animals moist and cool. The dynamics of
The interaction of intertidal organisms with ocean waves—​ intertidal communities vary in predictable fashion along gra-
their wave exposure—​is mediated by the slope of the seafloor. dients of wave exposure at least in part in response to wave-
As waves progress from deep to shallow water, accompanying induced water motion. These patterns are discussed later in
water motion changes from a nearly circular orbit confined to the chapter in the context of intertidal ecology.

342  Ecosystems
Organisms of California’s Rocky Corallina) and soft turfs (e.g., Endocladia, Gelidium), tough
Intertidal Ecosystems rockweeds (e.g., Silvetia, Fucus), fleshy blades (e.g., Ulva, Chon-
dracanthus, Mazaella), branching bushes (e.g., Stephanocys-
The narrow ribbon of California’s marine coast hosts an tis, Sargassum), large bladed or bladdered kelps (e.g., Lami-
extraordinary diversity of flora and fauna. Terrestrial life naria, Eisenia, Egregia), and meadowy surfgrass (Phyllospadix)
resistant to saltwater encroaches from inland; subtidal spe- (Figure 18.5).
cies able to survive limited air exposure or dynamic tide pool
conditions extend up the shore; and other organisms thrive
solely within the rocky intertidal ecosystem. No exact enu- Suspension Feeders
meration of California shore species exists, even if tiny organ-
isms are not considered. At least 669 species of intertidal and As adults, many rocky intertidal invertebrates are sessile, an
subtidal seaweeds are known in California (Abbott and Hol- adaptation to hold space and minimize wave dislodgement.
lenberg 1976), while over 3,700 rocky and sandy coast inver- Their food arrives primarily as phytoplankton, zooplankton,
tebrates have been identified from central California to Ore- or detritus particles suspended in rushing seawater. Some spe-
gon (Carlton 2007). A major intertidal survey throughout cies use active mechanisms for straining this tiny food dur-
southern California found 213 seaweed species (Murray and ing submerged periods; these include sweeping sieve-like legs
Littler 1989) and 349 invertebrate species (Seapy and Littler (e.g., barnacles) and pumping water through comb-like filters
1993); however, a contemporary, intensive inventory within (e.g., sponges, bivalves, tunicates). Others feed more passively
mussel beds “conservatively” discovered 141 algae and 610 by extending sticky or filtering appendages for longer periods
invertebrate species (Kanter 1980). Adding to coastal diversity of time. Tube snails (e.g., Serpulorbis) employ mucous nets; sea
are tide pool and migratory intertidal fishes along with visit- anemones (Anthozoa) have stinging tentacles; crevice-dwell-
ing shorebirds and a few mammals. ing sea cucumbers (e.g., Cucumaria) and peanut worms (e.g.,
Rocky intertidal organisms belong to a broad range of evo- Themiste) have sticky, branched tentacles; and plume worms
lutionary (phylogenetic) groups that include seaweeds and (e.g., Spirobranchus) and colonial moss animals (Bryozoa)
flowering plants (Chromista and Plantae); sponges (Porif- extend feathery filters.
era); hydroids and sea anemones (Cnidaria); flatworms (Plat- Suspension feeders such as acorn (e.g., Chthamalus, Bala-
yhelminthes); peanut worms (Sipuncula); segmented worms nus) and stalked (e.g., Pollicipes) barnacles, and anemones (e.g.,
(Annelida); barnacles, isopods, amphipods, shrimps, crabs, Anthopleura), can dominate intertidal reefs through sheer
and insects (Arthropoda); octopus, chitons, snails, sea slugs, numbers. Other filter feeders are important habitat-forming
and bivalves (Mollusca); sea urchins, sea stars, brittle stars, bioengineers; these include sand-castle worms (e.g., Phrag-
and sea cucumbers (Echinodermata); and tunicates, fishes, matopoma) that fill in crevices with sandy tube colonies, mus-
birds, and mammals (Chordata). An ecologically useful way sels (e.g., Mytilus) that form dense thickened beds with inter-
to characterize intertidal life forms is by how they acquire stitial microhabitats, and pholad bivalves (e.g., Penitella) that
energy to sustain life. Common groupings include primary bore holes in sedimentary reefs. These holes then host numer-
producers (that acquire energy from sunlight), suspension ous small organisms.
feeders (that filter or trap drifting microbiota and detritus),
grazers (that consume seaweeds), and carnivores (that capture
animals). Species within and among these trophic groupings Grazers
interact in intricate food webs. From a resource management
perspective, another set of groupings includes those har- California’s intertidal seaweed consumers (herbivores) can
vested or impacted by humans, those designated for special be relatively sedentary if they trap drift seaweeds (e.g., aba-
protection, and those introduced from faraway shores. lone, sea urchins) or graze algal films within a small area
(e.g., many limpets and chitons); however, others, such as top
snails, sea hares, and shore crabs, forage more widely. Her-
Primary Producers bivorous mollusks have file-like radulas, urchins use beak-like
jaws, and shore crabs employ claws to scrape seaweed films
Photosynthetic seaweeds provide a productive nutritional or larger plants. Grazers such as periwinkles (e.g., Littorina),
base for intertidal food webs, compete for limited shore space, limpets (e.g., Lottia), turban snails (e.g., Chlorostoma), chi-
and often create structural habitat for other organisms. Cal- tons (e.g., Nuttalina), shore crabs (e.g., Pachygrapsus), and sea
ifornia’s diverse sun-lovers range from tiny blue-green bac- urchins (e.g., Strongylocentrotus) can occur in great numbers
teria (cyanobacteria) through commonly categorized green where conditions are suitable. Hermit crabs (e.g., Pagurus) may
(Chlorophyta), brown (Heterokonta), and red (Rhodophyta) be abundant in tide pools, scavenging plant and animal mate-
seaweeds, to true flowering surfgrass (Tracheophyta). Reds are rials. Owl limpets (Lottia gigantea) can dominate upper inter-
the most species-rich, followed by browns, greens, and the tidal rocks, where they maintain grazing territories by remov-
two species of surfgrass. Seaweed structural forms adapted ing most other organisms.
to intertidal lifestyles include wave-resistant films or crusts;
leathery, desiccation-resistant rockweeds; filamentous turfs
with high surface area for nutrient and light uptake; stony Carnivores
coralline algae; and larger, bushy growths and fleshy blades
that rise above the substrate when submerged. Diverse predators are ecologically important in upper levels of
Dominant primary producers on California shores often intertidal food webs. Some like crabs and octopus are active
create intricate structural habitats, hosting rich floral and crevice or tide pool residents, while other mobile predators
faunal assemblages that shelter within or attach as epiphytes. are migratory—​lobsters and fishes moving inshore to forage at
Key dominant producer types include erect corallines (e.g., higher tides and seabirds arriving to hunt at lower tides. Some

In tertidal  343
 FIGURE 18.5 A broad meadow of surfgrass (Phyllospadix torreyi) covers the low shore.
Photo: Carol Blanchette.

carnivores are slow-moving (e.g., predatory snails, sea slugs, discovered on the open coast. Maloney et al. (2006) found
and sea stars). Sedentary sea anemones snare creatures that 16 non-native species in representative outer-coast intertidal
wander or drift onto them. Intertidal adaptations for capture reefs (667 species were native and 59 others were of unknown
of prey include drilling (e.g., snails like Ceratostoma and Acan- origin). The most widespread invaders were two seaweeds: a
thinucella), poisoning (e.g., Octopus and the cone snail Conus), large brown bladderweed (Sargassum muticum) and a small red
rasping or piercing (e.g., nudibranchs), prying or engulfing turf (Caulacanthus ustulatus).
(e.g., sea stars, such as Pisaster spp.), stabbing or hammering
(e.g., black oystercatchers, Haematopus bachmani), and pick-
ing at or swallowing whole (e.g., most fishes and shorebirds). Benthic-pelagic Coupling
The ochre sea star (Pisaster ochraceus) is well known as a
keystone predator that can greatly affect ecological condi- Rocky intertidal ecosystems are inextricably linked to the
tions in communities of its mussel prey. Ochre sea star popu- oceanic environment through the delivery of food, nutrients,
lations have declined due to disease outbreaks associated with and propagules (both larval invertebrates and algal spores).
warm water conditions in the 1970s and the recent El Niño The oceanographic processes driving the delivery of these
periods of 1982–​1983 and 1997–​1998 (Eckert et al. 2000). A constituents span large spatial scales and thereby connect
massive sea star wasting disease epidemic that has not been distant communities (see Chapter 6, “Oceanography”). Rocky
associated with warm water, and has affected all species of sea intertidal organisms may also alter the amounts and kinds of
stars, began in summer 2013 and has extended as far north materials in the waters that pass over, among, and through
as Alaska (Stockstad 2014). Shorebirds commonly can be seen them, and transform the pelagic (offshore) waters arriving
foraging at low tide on intertidal reefs; more elusive terrestrial to benthic (bottom-dwelling) organisms further upshore
mammals (including rats, cats, raccoons, and foxes) may hunt or along the shoreline. The exchange of essential materials
for shore crabs and other invertebrates at night. between the two ecosystems is referred to as benthic-pelagic
coupling (Figure 18.6). The nature and degree of coupling can
strongly influence the rate and extent of recovery from natu-
Species of Special Concern ral or anthropogenic disturbances, productivity, and the rela-
tive abundances and diversity of species that make up rocky
Surfgrass (Phyllospadix) and sea palms (Postelsia palmaefor- intertidal communities (Menge et al. 2003, Blanchette et al.
mis), recognized as important but susceptible habitat-forming 2008).
plants, are specifically protected from disturbance and sport Sessile animals and plants that live attached to the rocks
harvest (although sea palms are not protected from commer- rely on ocean currents to deliver food and nutrients. Much
cial harvest in California). The black abalone (Haliotis crach- of the food of suspension-feeding invertebrates such as mus-
erodii), once abundant and extensively gathered for food, suf- sels and barnacles consists of phytoplankton, single-celled
fered such catastrophic declines, particularly in southern photosynthetic organisms (e.g., diatoms and dinoflagellates)
California, during the 1980s (due to overfishing and wither- common to coastal waters. Microscopic zooplankton, includ-
ing syndrome disease) that it was listed as a federally endan- ing meroplankton (larval forms of nonplanktonic adults)
gered species in 2009. Species introduced to California marine and mixotrophic plankton (plankton that depend on a vari-
waters by hitchhiking on ships or other means present eco- ety of carbon sources), that feed on smaller planktonic forms
logical threats to native species. Most introduced species are (including phytoplankton) are also ingested by sessile, sus-
known from sheltered bays and harbors, with relatively few pension-feeding invertebrates. Some suspension feeders feed

344  Ecosystems
on even smaller planktonic forms, such as the bacteria, cil-
iates, and flagellates that form the microbial food webs of Benthic Predators
Benthic-pelagic
pelagic waters. In addition to the living components of their coupling
diets, many of these animals consume small detrital particles
Herbivores
derived from the breakdown and decay of seaweeds and other
marine plants (collectively referred to as macrophytes) from Suspension
nearby algal beds, kelp forests, and seagrass meadows. Algae feeders
Macrophytes of rocky shores all depend on the flow of water
over their thalli or leaves to deliver nitrogen, phosphorus, and Pelagic
Larvae
other nutrients for use in essential metabolic pathways (such as Zooplankton
photosynthesis, protein synthesis, respiration, Adenosine Tri-
phosphate (ATP) synthesis, DNA replication, RNA transcrip- Dissolved
tion) supporting growth and reproduction. Nitrogen and phos- nutrients
phorous in seawater can be present in several inorganic and Phytoplankton
organic forms, but the inorganic forms nitrate (NO3-), ammo-
nium (NH4+), and (ortho-) phosphates (HPO42- and PO4 -3) are FIGURE 18.6 Conceptual diagram of coupling between the benthic
most readily available to macrophytes. Although both phos- marine intertidal ecosystem and the pelagic marine ecosystem.
phorus and nitrogen can limit macrophyte growth, nitrogen Dissolved nutrients fuel the growth of phytoplankton as well as
is generally more limiting along California’s coast. The most macroalgae. Larvae from the pelagic environment settle in the
benthic intertidal environment. Source: Carol Blanchette.
important source of new nutrients (as opposed to nutrients
remineralized and recycled through microbial food webs) for
macrophyte growth is from the process of coastal upwelling.
al. 2011). Locations closer to upwelling centers are more con-
ducive to lush growth of macrophytes, while those receiving
Coastal Upwelling more aged waters that deliver a rich suspension of planktonic
foods, or occurring just downshore from upwelling centers
Although upwelling regions are only about 1% of the ocean’s that receive detrital macrophytes and drift-algae, will tend to
surface, they are the source of approximately 50% of the sea- favor the growth of invertebrates the feed on suspensions of
food humans harvest from the oceans each year. The high organic particulates and larger drift-algae (Broitman and Kin-
primary productivity of phytoplankton in these regions prop- lan 2006, Lester et al. 2007).
agates upward to support a diverse and productive ocean food
web. Both intertidal macrophytes and suspension-feeding
invertebrates can benefit from the nutrient-rich waters deliv- Complex Life Histories
ered by coastal upwelling (see Chapter 6, “Oceanography”).
Upwelled waters fuel the growth of macrophytes, phyto- Many, but not all, intertidal animals have complex life his-
plankton, and, indirectly, the rest of the planktonic food web tories that include indirect development and dispersal of
that supports suspension-feeding invertebrates. Since both pelagic larval forms. Some invertebrates such as mussels have
macrophytes and phytoplankton can strip nutrients from the a plankton-feeding (planktotrophic) larval stage coupled with
water column, this productive boost fuels competitive inter- a suspension-feeding adult stage and thus experience strong,
actions between these two groups. The dense blooms of phy- direct benthic-pelagic coupling throughout their life cycles.
toplankton that can form in response to upwelled nutrients Invertebrates such as urchins (Echinoderms in the class
reduce light reaching benthic-dwelling macrophytes by pre- Echonoidea) without suspension-feeding as adults are still
emptively intercepting it for their own use (Kavanaugh et al. influenced by their larval transit through the pelagic realm
2009). Clearer, colder, nutrient-rich waters conducive to lush and may experience indirect coupling with the pelagic envi-
growth of macrophytes tends to prevail near and just to the ronment later in life through the availability of drift seaweed.
south of coastal upwelling centers (which often coincide with Invertebrates such as predatory whelks (e.g., Kelletia kelletii)
headlands) (Broitman and Kinlan 2006). with direct developing, crawl-away larvae (no pelagic phase)
As newly upwelled waters move away from where they were can still be influenced by benthic-pelagic coupling because
shoaled, they bring along an initial inoculum of phytoplank- their prey have pelagic larvae (Wieters et al. 2011). Not all
ton that will eventually proliferate and grow in the sunlit rocky intertidal invertebrates are strongly influenced by ben-
surface waters, but this occurs over a period of several days. thic-pelagic coupling. Chitons (molluscs in the class Poly-
Thus older, warmer, phytoplankton-rich waters tend to occur placophora), for example, have short-lived, nonfeeding (leci-
further downstream and/or offshore of upwelling centers. thotrophic) larvae and as adults depend primarily on in situ
Depending on the prevailing trajectory of newly upwelled algal resources.
waters and the strength and duration of upwelling favor- The influence of the pelagic phase of life on intertidal
able winds, the locations of “downstream” or “aged” waters invertebrate populations varies strongly and depends in part
with abundant phytoplankton can vary. Local topography on larval characteristics. Larval stages may be short-lived or
and bathymetry, including offshore banks and canyons, help long-lived. They may need to encounter and capture their
create relatively predictable nearshore circulation patterns own planktonic food or be accompanied by a maternally
(Woodson et al. 2012). This results in a mosaic of shoreline sourced, lipid-rich nutritional package instead, or sometimes
habitats with qualitative and quantitative differences in the a combination of the two (Denny and Gaines 2007). In feed-
degree of benthic-pelagic coupling with respect to inorganic ing larvae, such as the veligers of mussels (bivalve molluscs),
nutrients for macrophytes and organic nutrition for inverte- planktonic food availability can affect juvenile survivorship
brates (Blanchette et al. 2009, Krenz et al. 2011, Watson et and growth on the shore (Phillips 2002). Thus timing of lar-

In tertidal  345
 regions (Lewis 1964, Stephenson and Stephenson 1972) even
where tidal range is only a few tens of centimeters. A typical
rocky shore can be divided into a spray zone or splash zone
above the mean high-tide line and covered by water only dur-
ing storms and an intertidal zone that lies between the high
and low tidal extremes (Figure 18.8). Along most shores, the
intertidal zone can be clearly separated into high, middle, and
low intertidal subzones with characteristic assemblages and
patterns of zonation. Along the California coast, barnacles
(Chthamalus and Balanus) characterize the high zone, rock-
weeds (Silvetia, Fucus) the upper-mid zone, mussels (Mytilus)
the lower-mid zone, and an assemblage of macrophytes, typi-
cally red algae, kelps, and surfgrass, the low zone.
Gradients in wave exposure provide an important back-
drop against which community structure varies horizontally
in space (Lewis 1964). Even over short distances, patterns of
distribution and species composition can shift dramatically
FIGURE 18.7 Examples of distinct bands of organisms (zonation) in from wave-exposed headlands to nearby wave-sheltered coves
the rocky intertidal. Photo: Jayson Smith. while still displaying sharp vertical zonation (e.g., Dayton
1971, Menge 1976). Exposure to sun as well as waves can also
influence species composition, with entirely different assem-
val release to match the availability of phytoplankton is prob- blages occurring on north-facing and south-facing rocky sur-
ably an important influence on survivorship of feeding lar- faces. At smaller scales within zones, organisms can also be
val forms (Phillips 2004). Planktonic larvae are also subject patchily distributed. Patchiness can be generated by wave-
to predation while in the pelagic zone. Fishes can markedly borne disturbance, which removes clumps of organisms from
reduce the survivorship of a well-fed cohort of larval barna- the rocks. The gaps formed in mussel beds are a classic exam-
cles previously destined to arrive on the rocky shores just ple of patchiness (Dayton 1971, Paine and Levin 1981). Distur-
beyond a kelp forest (Gaines and Roughgarden 1987). Despite bance due to wave action can, in some cases, determine the
their microscopic size, dispersing larvae are not always at structure of the entire intertidal community. This can hap-
the mercy of the currents; larvae can effect changes in their pen through a process of ecological succession, when species
horizontal position within the water column and thus move replace one another through time following a disturbance. A
themselves into onshore- or offshore-flowing waters. In the classic experiment examining the effects of disturbance and
end, most larvae do not make it back to shore. The realized succession on community structure took place in an inter-
dispersal, metamorphosis, and settlement of invertebrates tidal boulder field on the southern California coast (Sousa
to the intertidal zone depends on a highly favorable conver- 1979). The frequency with which boulders are overturned,
gence of the timing of release and duration of the larval stage, and therefore disturb the communities of organisms living
larval behavioral tactics, the nearshore circulation dynamics on them, depends on a combination of wave action strength
that generate currents, waves, fronts, and eddies, and condi- and the sizes of the boulders themselves. Sousa (1979) found
tions on the shore that permit or prevent survival of settling the greatest diversity of organisms on medium-sized boulders
larvae. that were overturned occasionally, providing an intermedi-
ate level of disturbance. Boulders that were overturned con-
stantly could only support ephemeral assemblages, and those
Intertidal Ecology rarely overturned were dominated by competitively superior
species. Sousa’s study and others in rocky intertidal ecosys-
Rocky intertidal ecosystems have long served as a proving tem have supported the general hypothesis that a moderate
ground for developing and testing ecological theory. Their level of disturbance is important to the maintenance of diver-
alternating exposure to marine and terrestrial conditions cre- sity in these ecosystems.
ates steep environmental gradients that help to explain the
striking patterns of distribution and abundance seen on most
rocky shores. Several features combine to make rocky shores Community Dynamics
ideal outdoor laboratories, including variable physical condi-
tions over short distances and the presence of small organ- For many years marine ecologists assumed that the struc-
isms that are mostly sessile or sedentary, often reach high ture of rocky intertidal communities was under largely physi-
densities, have short generation times, and are readily experi- cal control (e.g., Lewis 1964). Explanations for species distri-
mentally manipulated. butions, for example, were sought through study of species’
tolerances of waves, thermal stress, and desiccation. Many
thought that species could not live in particular zones
Patterns on the Shore because they could not tolerate the physical conditions there.
We now know that while physical factors are important, they
Zonation is the characteristic pattern of distribution and are only part of the story. In 1961, Joe Connell published two
abundance observable as successive bands of organisms as papers that elegantly and convincingly demonstrated that the
one moves from the low shore to the high shore (Figure 18.7). lower limits of two zone-forming barnacles were set by spe-
Zonation is perhaps the best-known pattern in rocky inter- cies interactions. At Millport, Scotland, he found that inter-
tidal communities. It occurs universally in rocky intertidal specific competition for space determined the lower limit of

346  Ecosystems
 Splash Zone
Splash Zone

UpperUpper
Intertidal Zone
Intertidal Zone
barnacle
Barnacle

Rockweed
rockweed

Middle
MiddleIntertidal
Intertidal Zone
Zone

Mussel
mussel

Ochre
ochre sea star
sea star

Lower
Lower Inter-
tidal Zone
Intertidal
Zone

FIGURE 18.8 Conceptual diagram of zonation depicting the intertidal zones. Source: Illustration by
Aeon Brady.

the upper-shore barnacle, and that both intraspecific compe- that the lower limits of species are set by biotic interactions
tition and predation by whelks determined the lower limit of while the upper limits are driven by physical factors.
the lower-shore barnacle (Connell 196la, Connell 196lb). Paine’s work not only demonstrated that predation could
While biotic drivers set the lower limits for both species, determine the lower distributional limit of a competitively
physical factors set the upper limits. Although upper-shore dominant intertidal organism but also made important con-
barnacles were outcompeted by lower-shore barnacles, the ceptual advances. His study was one of the earliest experi-
inability of lower-shore barnacles to persist in the high zone mental demonstrations of the predation hypothesis, which
due to desiccation stress provided refuge for upper-intertidal states that predation can control the diversity of species in
barnacles to exist, as they were more tolerant to long periods a community (Paine 1966). By selectively feeding on a dom-
of emersion. Five years later, Paine (1966) published the early inant competitor, thereby preventing competitive exclu-
results of a study on the Washington coast clearly demon- sion, predators can facilitate the coexistence of many spe-
strating that predation by a sea star (Pisaster ochraceus) main- cies of both dominant and subordinate competitors. In this
tained the lower limits of midshore mussel beds (Figure 18.9). case, sea star (Pisaster) predation mediated the abundance
Because the upper limit of sea stars typically reaches only the of the competitive dominant mussel (Mytilus), allowing for
lower intertidal zone, mussels can persist in the middle inter- a myriad of competitively inferior species, such as barnacles
tidal zone because of release of predation. Due largely to these and seaweeds, to persist. Paine’s study established the con-
two influential studies, attention shifted dramatically in the cept of “keystone species”—​species that have disproportion-
1960s toward the view that community patterns can be con- ately large effects on their communities relative to their abun-
trolled by biotic factors as well. Both studies provided evi- dances (Paine 1969, Power et al. 1996). Finally, Paine’s study
dence for the ecological paradigm in rocky intertidal habitats was one of the first clear demonstrations of indirect effects.

In tertidal  347
 FIGURE 18.9 The keystone predator, sea star (Pisaster ochraceus), feeding on its prey,
the California mussel (Mytilus californianus). Photo: Jayson Smith.

Indirect effects are the effects of one species on a second, nacle populations and the impact of variable recruitment or
mediated through a third. In the Mytilus-Pisaster example, settlement densities on adult density (e.g., Gaines and Rough-
Pisaster has large, positive indirect effects on many subordi- garden 1985, Connell 1985, Raimondi 1990). In central Cali-
nate competitors of Mytilus. The existence of indirect effects fornia, for instance, abundances of adult Balanus glandula in
was first noted through the unexpected or surprising out- the high zone vary from nearly complete coverage of the avail-
comes of experiments investigating species interactions (e.g., able rock surface at wave-exposed sites to low cover on more
Paine 1966 and 1974, Dayton 1971). The broader significance wave-sheltered sites (Gaines and Roughgarden 1985). Rates of
of indirect effects was underappreciated, however, until theo- recruitment were up to twenty times higher at wave-exposed
rists (e.g., Holt 1977, Bender et al. 1984) helped spur research sites compared to wave-sheltered sites. These and other stud-
to explicitly quantify their impact on community structure ies also strongly suggest that when recruitment is low, pat-
(see, e.g., Dungan 1986, Schmitt 1987, Wootton 1994). terns of abundance and community structure may be more
strongly influenced by the supply rate of new individuals than
by agents of postrecruitment mortality. For example, the neg-
Recruitment Dynamics ative relationship between an index of upwelling intensity
and the recruitment of barnacle larvae (Roughgarden et al.
In rocky shore ecosystems two aspects of larval biology pow- 1988) is a strong indicator that offshore transport dictates bar-
erfully influence population dynamics and community struc- nacle densities via negative effects on recruitment.
ture. The first is the behavior of larvae in selecting settlement
sites; the second relates to the quantities of larvae that recruit
to the shore. A considerable body of work has shown that bar- Community Regulation
nacle larvae have very specific requirements when they settle.
The position of larvae in the water column (Grosberg 1982), Whether and when biological communities are regulated by
the texture of the rock face (Crisp and Barnes 1954), the pres- consumers (top-down) or primary productivity (bottom-up)
ence of conspecifics (gregarious settlement) (Knight-Jones remains a fundamental question in all of ecology (Oksanen et
1955, Minchinton and Scheibling 1993), and chemical cues al. 1981, Fretwell 1987, Polis et al. 2000, Schmitz et al. 2000,
from coexisting species (Raimondi 1988) are among many White 2001). Some recent research in marine ecosystems has
factors that influence recruitment success. provided evidence for both top-down and bottom-up controls
The effect of a variable supply of new individuals on ben- on communities (Burkepile and Hay 2006). A unique aspect
thic populations has also long been of interest in marine ecol- of rocky shores is the occupation of primary space by two dis-
ogy (see reviews by Underwood and Denley 1984, Young 1987 tinctly different groups of competing organisms: algae and
and 1990, Grosberg and Levitan 1992) and has been dubbed filter-feeding invertebrates. Marine ecologists have spent con-
“supply-side ecology” (Lewin 1986). However, ecologists have siderable effort to understand the factors that contribute to
only recently focused explicitly on the relative degree to the community pattern resulting from differences in the rel-
which community structure is affected by settlement (the act ative proportion of these two groups. One major mechanis-
of colonization and metamorphosis by propagules; Connell tic hypothesis linking nearshore oceanography to commu-
1985) and recruitment (survival of settlers for some longer but nity pattern relates to the spatial and temporal variability in
usually arbitrary period of time Connell 1985) versus postre- coastal upwelling. Latitudinal variation in upwelling inten-
cruitment factors, such as predation and competition. Most sity has been suggested as an important factor in the recruit-
early research on the influence of recruitment dealt with bar- ment of benthic invertebrates along the U.S. West Coast.

348  Ecosystems
 The upwelling/relaxation model asserts that planktonic regimes, and modified biota such as the introduction of non-
larvae are swept offshore by Ekman transport, where they native species. Water pollution in the rocky intertidal can be
accumulate along coastal fronts and are occasionally returned linked to terrestrial runoff, storm drain flow, aerial deposi-
to shore when upwelling-favorable winds relax (Roughgarden tion, sewage effluent, wastewater discharges, and oil spills,
et al. 1988, Shanks et al. 2000). Consistently strong upwell- and can involve chronic or pulse disturbances from either
ing along much of the California coast has been proposed to point or nonpoint sources. The impacts of water pollution on
limit invertebrate recruitment (Gaines et al. 1985, Gaines and rocky intertidal species’ health and normal ecosystem func-
Roughgarden 1985, Roughgarden et al. 1988, Strub and James tioning are highly variable but are relatively understudied
1995), resulting in communities dominated by macrophytes (Crowe et al. 2000, Thompson et al. 2002).
in areas of strong upwelling. Regions of strong coastal upwell- Although chronic input of oil washed into storm drains far
ing may also influence community structure through positive exceeds oil spills (Foster et al. 1988, Suchanek 1993), the low
direct effects on macroalgae, which compete for space with rate of input as well as quick dilution has made it difficult
mussels and barnacles (Schiel 2004, Blanchette et al. 2006). to measure direct effects of the former. Pulse disturbances of
Coastal upwelling delivers cold, nutrient-rich water to shore, large quantities of oil have received more attention. The com-
and locations of strong upwelling are characterized by high bined impacts of oil coating, direct lethal toxicity, sublethal
nutrient concentrations, which have been shown to have pos- impacts on health, and clean-up efforts using chemical dis-
itive effects on the abundance (Bustamante et al. 1995, Broit- persants and physical removal can harm many rocky inter-
man et al. 2001) and growth rates (Blanchette et al. 2002, tidal populations. Mass mortality of macroalgae and benthic
Nielsen and Navarrete 2004) of benthic macroalgae. Strong invertebrates can result from chemical toxicity and smoth-
coastal upwelling is predicted to favor macroalgal dominated ering by oil, while high-pressure, hot-water clean-up efforts
communities through both direct positive effects of nutrients can have equally devastating, if not worse, effects including
on algae and indirect effects of reduced competition with lengthened recovery time (Paine et al. 1996, Peterson et al.
recruitment-limited invertebrates for space. However, the rel- 2003). Sublethal impacts include physiological, carcinogenic,
ative importance of these two mechanisms is still not well and cytogenic effects, resulting in population-level and com-
understood. munity changes (Suchanek 1993, Peterson et al. 2003).
The largest oil spill in California and the third largest in
the United States occurred near Santa Barbara in 1969, dump-
Human Impacts ing about 4 million gallons of crude oil (Clarke and Hemphill
2002). Notable short-term impacts included marked losses
With approximately 68% of Californians living near the of rocky intertidal barnacles and macrophytes (Foster et al.
shoreline in 2008 (Wilson and Fischetti 2010), coastal ecosys- 1971, Straughan 1973); understanding of the spill’s long-
tems experience multiple threats from human activities. High term effects, however, remains poor. Also near Santa Barbara,
urbanization can affect coastal ecosystems through air and the 1997 Torch/Platform Irene Oil pipeline rupture spilled
water pollution, land development, habitat destruction, com- 6,846 gallons of petroleum, oiling approximately 17 miles of
mercial and recreational harvest, recreational use, and intro- coastline. In 2007 the container ship Cosco Busan struck a
duction of non-native species, among other human-induced San Francisco bridge, spilling 53,569 gallons of fuel, which
environmental changes. Rocky intertidal ecosystems are espe- oiled 200 miles of wave-protected and wave-exposed coast-
cially under threat because they lie at the land-ocean inter- line. In 2009 the tank vessel T/V Dubai Star spilled 400 gal-
face and thus receive direct runoff of terrestrial pollutants, lons of oil, reaching 10 miles of San Francisco Bay shoreline.
coincide with settling locations for oceanic oil spills, and can Oil from these more recent spills coated portions of the rocky
be easily accessed during low tides for exploitation. Over the intertidal zone and its inhabitants, but their impacts were
past several decades, many changes in species abundances complex to measure, complicated by natural temporal varia-
have been observed in the rocky intertidal, including large tion and a lack of baseline information (Torch/Platform Irene
declines in black abalone populations in southern and cen- Trustee Council 2007, Raimondi et al. 2009 and 2011). Some
tral California (Miller and Lawrenz-Miller 1993, Richards and generalized effects of the spills included declines in barna-
Davis 1993, Altstatt et al. 1996); shifts in southern California cles, mussels, and rockweeds and increases in opportunistic
macroalgal community structure from large fleshy species to algae.
more disturbance tolerant, turf-forming seaweeds (Widdow- In addition to oil, surface runoff from urban and agricul-
son 1971, Thom and Widdowson 1978, Goodson 2004, Ger- tural sources discharges high amounts of fresh water, nutri-
rard 2005); declines in mussels in southern California (Smith, ents, heavy metals, pesticides, and other substances into Cali-
Ambrose, and Fong 2006) and mussel bed–​associated macro- fornia coastal waters (Schiff et al. 2000). Influxes of nutrients
invertebrate diversity statewide (Smith, Fong, and Ambrose can cause declines in perennial seaweeds and increases in
2006); regional extinction of the dorid nudibranch (Felimare opportunistic seaweeds that use the nutrients to grow and
californiensis) (Goddard et al. 2013); shifts in species range bloom. For example, the addition of nutrients, in this case
limits (Sagarin et al. 2007, Zacherl et al. 2003), and increases sewage-based, on San Clemente Island led to a decrease in
in non-native species (Cohen and Carlton 1995, Murray et slowly growing brown algae and seagrasses and an increase
al. 2005). in opportunistic green algae and cyanobacteria (Littler and
Murray 1975). Little work has examined the field effects of
even single heavy metals on rocky intertidal ecosystems
Water Pollution (Crowe et al. 2000), let alone of synergistic effects of multiple
contaminants. Effects of sublethal levels of heavy metals and
Water pollution includes manufactured chemicals such as other contaminants can include opportunistic algal blooms
DDT, elevated levels of naturally occurring chemicals such (Castilla 1996) and impacts on larval development of benthic
as heavy metals and nutrients, altered natural temperature invertebrates (Fichet et al. 1998).

In tertidal  349
Recreational Human Visitation and Exploitation coastal waters) are now under the jurisdiction of the Califor-
nia Department of Fish and Wildlife. Within reserves, marine
Rocky intertidal habitats during low tide provide a glimpse life is protected through limitations or bans on harvesting.
of the natural marine world without the need for specialized MPAs in northern California also explicitly protect tribal
underwater equipment and training. In heavily urbanized rights to ceremonial and subsistence harvest of intertidal
areas of California, visitation to some rocky intertidal loca- organisms. MPAs are very effective in protecting subtidal
tions can reach fifty thousand to seventy-five thousand visi- marine life (Halpern 2003), but their effectiveness in protect-
tors per year (Ambrose and Smith 2005, Ware 2009, Laguna ing rocky intertidal habitats needs to improve. Collecting in
Ocean Foundation 2012). People visit these habitats for rec- rocky intertidal MPAs continues to occur despite regulations
reation, education, and subsistence harvesting and engage (Murray 1997, Murray et al. 1999, Ambrose and Smith 2005).
in activities such as collecting, rock turning, handling, and In addition, management is solely focused on collecting while
trampling. Through both experimental manipulations and other impacts are not clearly addressed (Smith et al. 2008).
observational comparisons of high- and low-use locations, While current management practices are strong and suc-
some detrimental impacts of these activities have been docu- cessful, improved conservation requires adaptive management
mented. These effects include locally depleted floral and fau- and supplemental strategies. Publicly owned treatment works
nal populations, reduced biodiversity, shifts in the size and (POTWs) are well regulated, but storm water runoff manage-
age structure of populations, and altered ecological processes ment is still in its early stages, as is understanding of the sin-
(e.g., Castilla and Bustamante 1989, Duran and Castilla 1989, gular and synergistic effects of pollutants. Continued and
Brown and Taylor 1999, Espinosa et al. 2009). expanded long-term monitoring of rocky intertidal resources,
Harvesting of rocky intertidal organisms is relatively com- such as that conducted by the Multi-Agency Rocky Intertidal
mon in California and extends back thousands of years (Braje Network (MARINe), provides vital baseline information to
et al. 2007). People engage in legal harvesting as well as ille- document impacts from oil spills and other anthropogenic dis-
gal poaching of protected species. Commercial harvesting of turbances. Increased support is needed for local organizations
intertidal seaweeds is a growing cottage industry, especially that help fill some management gaps. Groups such as numer-
in northern California (Thompson et al. 2010). Subsistence ous regional Baykeepers organizations, the Orange County
and ceremonial harvesting of intertidal mussels, seaweeds, MPA Council, Heal the Bay, and others provided essential local
and other intertidal organisms remains an important prac- oversight, monitoring and research, and educational and out-
tice for the members of California’s many Native American reach services. Restoration of rocky intertidal habitats is still
tribes. Organisms are harvested for food, fish bait, and sou- nascent but could aid species recovery, as shown through the
venirs, with mussels, octopuses (Octopus), abalone (Haliotis), successful reestablishment of rockweeds (Whitaker et al. 2010)
limpets (Lottia), urchins (Strongylocentrotus), snails (e.g., Chlo- and surfgrass (Bull et al. 2004) following localized extirpation.
rostoma), crabs (Pachygrapsus), seaweeds (e.g., Postelsia), and Finally, conservation efforts of the future can be expanded by
sea stars (Pisaster) often targeted. promoting public understanding of the economic and other
Local declines in the abundances of many of these species values of rocky intertidal shores (e.g., Hall et al. 2002).
have been attributed to overharvesting. For example, mussels
(Smith et al. 2008), large conspicuous invertebrates such as
keyhole limpets and sea hares (Ambrose and Smith 2005), and Climate Change
various echinoderms and gastropods (Addessi 1994) occur in
lower abundances at heavily visited sites. Recreational har- Global climate change is the backdrop against which all eco-
vest of red abalone virtually eliminates it from the intertidal logical and socioeconomic interactions now occur. The rocky
zone, although it can be found intertidally in locations well intertidal zone has long served as a model system for exam-
protected from both legal harvest and poaching (Rogers-Ben- ining the effects of the physical environment on the phys-
nett et al. 2013). Overharvesting can shift the size structures iology and ecology of organisms, and as such has emerged
of intertidal populations (e.g., owl limpets) toward smaller as a natural laboratory for exploring the effects of environ-
and younger individuals, as humans tend to be size-selective mental change (Connell 1972, Paine 1994). Impacts of cli-
predators (Fenberg and Roy 2008, Kido and Murray 2003, mate change on patterns of distribution, abundance, and the
Ambrose and Smith 2005, Sagarin et al. 2007). provision of ecosystem services have been reported world-
wide (Helmuth, Broitman et al. 2006), with numerous exam-
ples in California (e.g., Barry et al. 1995, Zacherl et al. 2003,
Management Smith et al. 2006, Hilbish et al. 2010). While the exploration
of the complex and often nonlinear effects of environmental
Along the California coast, especially adjacent to heavily change on intertidal ecosystems remains an active and grow-
urbanized centers, a clear need exists to manage and protect ing area of research, several key themes—​as well as knowledge
rocky intertidal ecosystems. Conservation of rocky shores gaps—​have emerged in the search to understand and poten-
currently focuses on designations such as areas of special tially forecast likely impacts (Howard et al. 2013).
biological significance (ASBS) and/or marine protected areas
(MPAs). The ASBS designation focuses on water quality, with
thirty-four locations (32% of the California coast) managed Future Scenarios
by the State Water Resources Control Board. Within ASBS
boundaries, state policy prevents discharge of any wastes in Coastal habitats face myriad threats from global change,
order to maintain natural water quality (SWRCB 2005). MPAs including increases in temperature, increased rates of coastal
focus on the protection of marine organisms. As a result of erosion, sea level rise, decreases in ocean pH, and altered circu-
the California Marine Life Protection Act passed in 1999, a lation patterns (Howard et al. 2013). Globally, ocean acidity has
network of 124 MPAs and 15 special closures (covering 16% of increased by 30% (from an average pH value of 8.2 to 8.1) over

350  Ecosystems
the past century (Feely et al. 2004) with a further decline of 0.3
46.0ºN
pH
to 0.4 pH units expected by 2100 (Orr et al. 2005). The aver-
Model 8.10
age temperature of the upper layers of the ocean has increased
0.2°C since 1955 (Bindhoff et al. 2007) and is expected to
44.0ºN 8.08
increase by 0.4°C to 1.1°C in the next few decades. Projections
of future climate, which depend significantly on greenhouse 8.06
gas emissions, suggest an increase in mean air temperature of
42.0ºN 8.04
2°C to 5°C by 2100 in California, with the greatest amount of
change occurring in summer (Cayan et al. 2009).
8.02
Notably, these global averages mask much higher levels
40.0ºN

Latitude
of variability in environmental change (Hoegh-Guldberg 8.00
and Bruno 2010), and coastal environments are likely being
altered more quickly than offshore waters. Measurements of 7.98
pH in Monterey Bay show a decrease about 8.1 to 8.05 from 38.0ºN
7.96
1993 to 2009, although this is one of the few longer-term mea-
surements from the region (Monterey Bay Aquarium Research 7.94
Institute 2010 Annual Report. 2011). Hofmann et al. (2011) 36.0ºN
describe the results of a one-month time series of continu- 7.92
ous pH measurement at seven sites along the coast of Califor-
34.0ºN 7.90
nia and report high variability from site to site, with fluctua-
tions of 1 pH unit (i.e., an order of magnitude variability) at 7.88
sites such as Elkhorn Slough and levels at some sites approach-
ing those predicted for the open ocean in 2100. California’s 32.0ºN
130.0ºW 126.0ºW 122.0ºW 118.0ºW
coastal upwelling waters are typically very acidic, with pH val-
Longitude
ues as low as 7.5 (Feeley et al. 2008, Gruber et al. 2012). Mod-
els predict a continuing decline in pH in these waters over
FIGURE 18.10 Model simulated snapshot of surface pH for the month
time (Hauri et al. 2009) (Figure 18.10). Recent work has shown of August. Low-pH waters in nearshore areas are the result of
a mosaic of pH along the California coast, with persistent spa- seasonal upwelling in summer, while the elevated pH in offshore
tial variation in the cumulative frequency of exposure to rela- waters reflects the photosynthetic removal of CO2 from the water as
tively corrosive (pH <7.7) conditions (Hofmann et al. 2014). it is transported offshore. Source: Hauri et al. 2009.
Nearshore water temperatures vary considerably from
northern to southern California. Water temperatures in
northern California are fairly homogeneous across latitude the abundance of ecologically and economic important spe-
(31.5–​40.5°N) with a mean temperature of 13.5°C and a mean cies have been reported worldwide, including on the coast of
annual range of 3.4°C (Payne et al. 2011). South of Point Con- California (Harley et al. 2006, Howard et al. 2013).
ception in the Southern California Bight, waters are consid-
erably warmer (17.8°C) and more variable (annual range of
5.6°C) (Payne et al. 2011). Geographic patterns of intertidal Interactions between Stressors
(aerial) temperature are even more complex, exhibiting a
mosaic pattern in which extremes in temperature do not nec- Climate change is often “the trigger that fires the bullet,”
essarily increase with decreasing latitude (Helmuth, Miesz- delivering the coup de grace on organisms already impacted
kowska et al. 2006). by other stressors such as overharvesting and eutrophication
In general, the impacts of climate and related change in (Harley and Rogers-Bennett 2004, Crain et al. 2008, Firth
the intertidal can be categorized as direct physiological and Williams 2009). As such, the impacts of environmental
effects—​t he influence of environmental change on the sur- stressors are best considered in the context of other climatic
vival, growth, reproduction, and physiological performance and nonclimatic drivers of physiology and ecology. Crain
of individual organisms—​a nd indirect effects, the cascad- et al. (2008) conducted a meta-analysis of marine studies
ing influence of altered behavior and physiological perfor- that examined multiple stressors and found that cumulative
mance on species interactions, including predation, compe- effects were more or less evenly divided among additive (sum
tition, and facilitation (Harley et al. 2006, Blanchette et al. of individual stressors), synergistic (overall impact more than
2008). Direct effects are better understood. Sanford (2002) the sum of the individual stressors), and antagonistic (impact
showed that increased water temperatures enhanced feed- less than the sum of the individual effects) types. Overhar-
ing rates by the keystone sea star on mussel prey in central vesting, for example, predisposes populations of fish to col-
California. In contrast, increased sea star temperatures in air lapse when exposed to stressors such as pollution and climate
reduced feeding by 40% at the same site (Pincebourde et al. change (Hsieh et al. 2008, Sumaila et al. 2011). Taken in sum,
2008). Competitive ability between barnacles in experiments these studies signal a need to understand the processes by
depends on their relative physiological tolerances to thermal which climate change impacts intertidal organisms, at scales
stress (Wethey 1984), and field collections in San Francisco ranging from subcellular to ecosystem (Helmuth 2009).
Bay showed that small-scale distributions of native and inva-
sive species of mussels were linked to aerial body tempera-
ture (Schneider and Helmuth 2007). Although understanding Summary
of emergent impacts on species assemblages remains incom-
plete, shifts in species phenology and ranges, increases in Intertidal ecosystems exist at the interface between land and
rates of species invasions and disease spread, and changes in ocean and occupy a narrow band of the coast that is above

In tertidal  351
water at low tide and under water at high tide. Organisms Denny, M. W., and S. D. Gaines, editors. 2007. Encyclopedia of tide-
occupying intertidal areas have evolved unique adaptations pools and rocky shores. University of California, Press, Berkeley,
California.
to withstand the wide variation in physical conditions (tem-
Morris, R. H., D. P. Abbott, and E. C. Haderlie. 1980. Intertidal inver-
perature, salinity, desiccation) characteristic of these environ- tebrates of California. First edition. Stanford University Press,
ments. Although intertidal habitats can have either soft (sand, Stanford, California.
mud) or hard (rocky) bottom substrates, we have focused this Ricketts, E. F., J. Calvin, and J. Hedgpeth. 1939. Between Pacific tides.
chapter on rocky intertidal ecosystems, which occur along Fifth edition. Stanford University Press, Stanford, California.
the entire California coast. Rocky intertidal ecosystems of the
Pacific coast support a high diversity of invertebrate and algal
species and have served as a model ecosystem for experimen- Glossary
tal marine ecology.
The organisms inhabiting rocky intertidal ecosystems tend Benthic  This refers generally to organisms that live in close
to occur in characteristic bands or zones determined in part relationship with the substrate bottom and many that are
by time of submergence (underwater) and emergence (above permanently attached to the bottom.
water). Along the coast of California the high intertidal zone, Biogeographic  Refers to the distribution of organisms in the
which is inundated only during high tides, has species includ- context of geographical space.
ing rockweed, acorn barnacles, turban snails, and lined shore Competitive exclusion  The proposition that states that two
crabs. The middle intertidal zone, exposed to the air at least species competing for the same resources cannot coexist if
once a day, is home to creatures such as sea lettuce, aggre- other ecological factors are constant. When one species has
gating anemones, chitons, gooseneck barnacles, mussels, and even the slightest advantage or edge over another, then the
ochre stars. The low intertidal zone, exposed only during very one with the advantage will dominate in the long term.
low tides, is inhabited by kelps, coralline algae, surfgrass, giant Conspecific  Members of the same species.
green anemones, purple sea urchins, and bat stars. Ecological Emersion  Refers to the time that organisms spend out of or
processes, such as competition, predation, and recruitment, uncovered by water.
play an important role in determining the species composi-
Franciscan complex  An assemblage of sandstone, shale,
tion of intertidal assemblages. Many invertebrate and algal
chert, and mildly metamorphosed basalts derived from
species that occupy the shoreline as adults have early life his- ocean floor material accreted onto the California coast by
tory stages such as spores and larvae that may spend days to subduction. These rocks comprise large portions of the
months drifting in the ocean before settlement on the shore. California coast and Coast Range mountains.
These early life history stages are one important connection Marine terrace  Broad, flat expanses of coastal land originally
between the benthic (rocky bottom) habitat of the intertidal created by erosion of waves when the land was at sea level.
and the pelagic (open ocean) realm. Intertidal organisms also Multiple sea level changes and tectonic uplift later raise the
depend on water movement for delivery of food and nutrients flat terraces above sea level, leaving characteristic stepped
as well as reproduction and dispersal. hills.
People use intertidal ecosystems for food and recreation; Orogenic  Any geological process that leads to the formation
however, these ecosystems are also sensitive to anthropo- of mountains. Often caused by the pressures of colliding and
genic impacts from water pollution, oil spills, harvesting, subducting tectonic plates or volcanic activity.
and trampling. Following the California Marine Life Protec- Pelagic  This refers to organisms that are not associated with
tion Act (1999) a statewide network of marine protected areas the bottom and occur in the water column or in the open sea.
has been established along the California coast, and many of
Perennial  These are plants and seaweeds that live for more
these reserves include significant portions of rocky intertidal than two years and is generally a term used to differentiate
habitat. Climate change likely poses the most serious threat from annuals, which complete their life cycle in one year.
to intertidal ecosystems, where many species are already liv-
Sessile  This refers to organisms that are directly attached to the
ing close to their physiological tolerance limits. Increases in
bottom or substrate.
temperature, coastal erosion rates, and sea level rise; decreases
in ocean pH; and altered circulation patterns resulting from Shoal  This term refers to when water becomes more shallow.
changing climate conditions all could significantly impact Subduction  The geologic process by which the edge of an
intertidal ecosystems in the coming decades. oceanic tectonic plate is forced beneath another plate.
Subduction can create coastal mountains due to pressure
lifting land behind the subduction zone.
Acknowledgments Thalli  These are the undifferentiated vegetative tissues of
macroalgae, and generally refer to the entire individual
The authors thank the U.S. Department of the Interior Bureau seaweed organisms in the case of macroaglae.
of Ocean Energy Management, the Multi-Agency Rocky Inter- Veliger  The planktonic larva of many kinds of gastropod and
tidal Network, the Partnership for Interdisciplinary Studies of bivalve molluscs.
Coastal Oceans (PISCO), the Tatman Foundation, and Aeon
Viscous  Refers to the properties of fluid that resist deformation
N. Brady.
to stress. Viscous fluids are generally thought of as being more
“thick” (e.g., honey).
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