Download How do we Measure the Environment? Linking Intertidal Thermal Physiology

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COMP. BIOL., 42:837–845 (2002)
How do we Measure the Environment? Linking Intertidal Thermal Physiology
and Ecology Through Biophysics1
BRIAN HELMUTH2
University of South Carolina, Department of Biological Sciences and Marine Science Program, Columbia, South Carolina 29208
SYNOPSIS. Recent advances in quantifying biochemical and cellular-level responses to thermal stress have
facilitated a new exploration of the role of climate and climate change in driving intertidal community and
population ecology. To fruitfully connect these disciplines, we first need to understand what the body temperatures of intertidal organisms are under field conditions, and how they change in space and time. Newly
available data logger technology makes such an exploration possible, but several potential pitfalls must be
avoided. Body temperature during aerial exposure is driven by multiple, interacting climatic factors, and
extremes during low tide far exceed those during submersion. Moreover, because of effects of body size and
morphology, two organisms exposed to identical climatic conditions can display very different body temperatures, which can also be substantially different from the temperature of the surrounding air. These
same factors drive the temperature recorded by data loggers, and one logger type is unlikely to serve as an
effective proxy for all organisms at a site. Here I describe the difficulties involved in quantifying patterns
of body temperature in intertidal organisms, and explore the implications of this complexity for intertidal
physiological ecology. I do so using data from temperature loggers designed to mimic the thermal characteristics of the mussel Mytilus californianus, and deployed at multiple sites along the West Coast of the
United States. Results indicate a highly intricate pattern of thermal stress, where the interaction of climate
with the dynamics of the tidal cycle determines the timing and magnitude of temperature extremes, creating
a unique ‘‘thermal signal’’ at each site.
INTRODUCTION
Intertidal invertebrates and algae are marine ectotherms that must regularly contend with a terrestrial environment, and as such provide a unique perspective on the relationship between thermal stress
and organismal physiology and ecology. Indeed,
largely because of the steep gradient in thermal and
desiccation stresses that is presumed to occur during
low tide, the rocky intertidal zone has long been a
model system for examining relationships between
abiotic stresses, biotic interactions, and ecological
patterns in nature (Orton, 1929; Doty, 1946; Carefoot, 1977; Paine, 1994). Recent years have witnessed major advances in our understanding of the
role of body temperature in intertidal physiological
ecology (e.g., Hofmann and Somero, 1995, 1996a,
b; Stillman and Somero, 1996; Williams and Morritt,
1995; Roberts et al., 1997; Chapple et al., 1998;
Feder and Hofmann, 1999; Sanford, 1999, 2002; Tomanek and Somero, 1999, 2000; Dahlhoff et al.,
2001; Hochachka and Somero, 2002; also see other
papers in this issue). This field has further assumed
a sense of urgency given projected changes in global
climate, and the strong possibility that intertidal habitats may serve as a bellwether for change in other
ecosystems (Lubchenco et al., 1993; Barry et al.,
1995; Sagarin et al., 1999; Hughes, 2000).
However, our ability to extrapolate from detailed,
fine-scale measurements of physiological stress experienced by organisms exposed to controlled laboratory
conditions, or to generalize from limited field collections, is hampered by our limited knowledge of what
body temperatures are under actual field conditions,
and of how these temperatures change in space and
time.
Here I describe the underlying physical reasons
why quantifying spatial and temporal patterns in intertidal invertebrate and algal body temperatures is
complex, and I explain what pitfalls must be overcome if we are to effectively link climate change,
organismal physiology and ecology in the intertidal
zone. Most of the principles and methodologies that
I discuss are based on a long-standing history of biophysical studies in the terrestrial environment (e.g.,
Porter and Gates, 1969; Porter and Norris, 1969;
Porter et al., 1973; Reichert and Tracy, 1975; Kingsolver, 1979, 1989; Stevenson, 1985; Huey et al.,
1989). However, several of the problems that I describe are unique to the intertidal zone. While providing a general overview of thermal ecology in intertidal habitats, I use specific examples from my
own work with a competitively dominant invertebrate species on the west coast of the United States,
the mussel Mytilus californianus. Interestingly, results show that the same issues that make measurements of intertidal body temperatures particularly
difficult also lead to complex patterns in thermal exposure, and thus present a unique opportunity to explore the role of thermal history in driving the physiological ecology of animals inhabiting an important
ecosystem.
1 From the Symposium on Physiological Ecology of Rocky Intertidal Organisms: from Molecules to Ecosystems presented at the
Annual Meeting of the Society for Comparative and Intergrative
Biology, 2–7 January 2002, at Anaheim, California.
2 E-mail: [email protected]; 803-777-2100
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BRIAN HELMUTH
POTENTIAL PITFALLS OF QUANTIFYING
INTERTIDAL TEMPERATURES
Body temperature during aerial exposure is driven
by multiple, interacting climatic factors, and is
affected by organism size, shape, mass and color
Animals and algae inhabiting the intertidal zone are
ectothermic, and have body temperatures that are driven almost exclusively by external climatic conditions.
While submerged during high tide, an intertidal organism is likely to display a body temperature similar to
that of the surrounding water. In contrast, during aerial
exposure at low tide, climatic factors such as ground
and air temperature, wind speed, cloud cover, solar radiation and relative humidity interact to drive the flux
of heat into and out of an organism’s body (Johnson,
1975; Bell, 1995; Helmuth, 1998, 1999). As a result,
temperature extremes during low tide can far exceed
those experienced during submersion, often by 208C
or more (Williams and Morritt, 1995; Helmuth and
Hofmann, 2001), and exposure to these extremes has
been shown to cause significant damage at the cellular
and biochemical level (e.g., Hofmann and Somero,
1995, 1996a, b; other papers in this issue).
In general, six environmental factors determine the
rate of change in the amount of heat stored within the
body of an ectotherm (for which metabolic heat production is considered negligible): short-wave (visible)
solar radiation, long wave (infrared, IR) radiation to
and from the sky, IR radiation to and from the ground,
conduction to and from the ground, heat convected
between the animal and the surrounding air, and heat
lost through the evaporation of water (Porter and
Gates, 1969).
Importantly, the rate of heat transfer between an organism and its environment is to some extent determined by the size and morphology of the organism,
and can be strongly affected by characteristics such as
color and material properties (e.g., Porter and Gates,
1969; Porter and Norris, 1969; Porter et al., 1973;
Kingsolver, 1979, 1989; Stevenson, 1985; Etter, 1988;
Helmuth, 1998). As a result, organisms exposed to
identical environmental conditions can experience
quite different body temperatures (Fig. 1). For example, barnacles maintain a relatively large proportion of
their total surface area in contact with the underlying
substratum, and display body temperatures that are
tightly coupled with ground temperature (Harley,
2001; Wethey, 2002). Mussels, in contrast, are predicted to have body temperatures that are largely decoupled from the temperature of the underlying substratum, at least while living in beds of conspecifics,
and are often several 8C warmer than the surrounding
air (Helmuth, 1998). Organisms with wetted areas exposed to moving air can cool via evaporative water
loss, provided relative humidity is not too high (Brawley and Johnson, 1991; Bell, 1995; Helmuth, 1998).
For example, hydrated intertidal algae are often several
degrees cooler than air temperature, but when desiccated can be much warmer than the air (Bell, 1995),
and the same might be expected to hold true for animals such as seastars (Fig. 1a) and anemones.
By keeping track of the flux of heat energy into and
out of an animal’s body, and accounting for the effects
of organism size, morphology, etc. on those fluxes, one
can estimate the amount of heat energy stored in the
organism’s body, and from there, its temperature. Given sufficient time, an organism exposed to constant
environmental conditions will eventually achieve a
steady-state condition where the fluxes of heat into and
out of the body are equal, and the amount of stored
heat (and thus body temperature) remains constant.
This equilibrium condition is often termed the ‘‘operative’’ body temperature and is a useful metric for exploring the effect of changes in one or a few environmental factors (e.g., Porter and Gates, 1969; Bakken,
1980, 1992; Huey et al., 1989). For example, models
of operative body temperature of mussels (and other
ectotherms: Stevenson, 1985) suggest that larger animals will eventually heat to higher temperatures than
will smaller animals exposed to the same conditions
(Helmuth, 1998). However, by necessity this metric
ignores the fact that climatic conditions can change
rather rapidly with time, and that organismal temperatures require some time to reach equilibrium.
At issue here is the difference between heat (energy)
and temperature (a measure of average kinetic energy). All materials, regardless of shape or size, can be
defined on the basis of their specific heat capacity (or,
simply, specific heat), a description of the amount of
heat energy (in Joules, J) needed to raise one kg of
material 1 K (Kelvin; a change of 1 K 5 a change of
18C). Therefore, to convert from the heat stored in an
organism’s body to the temperature (Tb) of its body,
we not only need to keep track of the fluxes of heat
into and out of the body, but also of the organism’s
mass (m) and specific heat (cp):
Heat stored 5 mc p Tb 5 Heat gained 2 Heat lost
(1)
Thus, the flux of heat (energy) into any system increases the temperature of the object at a rate proportional to the product of the object’s mass and specific
heat (m cp). A larger, more massive organism, or one
composed of a material with a high specific heat, requires substantially more heat energy to raise its temperature to the same degree as a smaller organism. The
capacity to dampen the response in body temperature
to fluctuations in the environment is termed ‘‘thermal
inertia,’’ and is quantified as a time constant (t), a ratio
of factors that resist changes in temperature (mass and
specific heat) to those that promote them (such as areas
of exposure and the coefficient of heat transfer; Spotila
et al., 1973; Buatois and Croze, 1978; Spotila and
Standora, 1985; Kingsolver, 1981; Helmuth, 1998,
1999). In other words, when environmental conditions
fluctuate at a rate faster than the time constant of an
organism, the thermal inertia of the body will tend to
dampen the temperature response of the body to those
fluctuations, and the organism will be less likely to
suffer from brief, transitory extremes in environmental
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OF INTERTIDAL
THERMAL STRESS
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FIG. 1. Animals exposed to identical climates experience different body temperatures. A. Image of Pisaster ochraceous feeding on a bed of
Mytilus californianus, and (inset) the same image, viewed through a thermal (infrared) imaging camera (FLIR systems Thermacam 695; scale
bar ranges from 11.0–22.48C). This image shows that under the same set of climatic conditions, Pisaster maintained a much lower body
temperature than did its prey. B. Infrared image showing thermal heterogeneity at Strawberry Hill, OR.
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BRIAN HELMUTH
protected site (China Point) at the Hopkins Marine Station in Pacific Grove, California from July to August
2000. Figure 2a shows an example of a ;4.5 hr, midday tidal exposure where heating occurred rather rapidly. In this example, the smallest mussel heated more
quickly than the larger mussels, and achieved a maximum temperature of almost 5 degrees above those of
the two larger mussels. In contrast, Fig. 2b shows temperatures of these same mussels on a day where heating occurred more slowly over a long period of aerial
exposure (;6 hr) and which began in early morning.
In this case, the large mussels reached temperatures
slightly above that of the smallest individual. Thus,
depending on environmental conditions, increasing
size can have variable effects on body temperature. As
predicted by heat budget models (Helmuth, 1998),
larger mussels display higher operative temperatures
when conditions permit the equilibrium temperature to
be reached (Fig. 2b). When environmental conditions
fluctuate rapidly, or when wave splash inundates the
mussel before equilibrium temperature is reached,
small mussels may experience more extreme temperatures (Fig. 2a). Thus, not only is there an effect of
mussel size on body temperature, but the effect of size
is likely to change with location and environmental
conditions. Figure 2c, for example, shows that over the
course of the 2 month deployment (the smallest mussel
was only deployed for 2 wk), the effects of size on
maximum temperature changed from week to week,
with the intermediate-sized (108 mm) mussel most often experiencing the highest temperature.
FIG. 2. The interacting effects of organism size and fluctuating environmental conditions on body temperature. A. Data collected on
1, July 2000 in Monterey, CA. On this day, aerial exposure occurred
during mid-day, and the smallest mussel shell (filled with silicone
and a data logger) tracked changes in the environment quickly,
reaching higher temperatures than larger, adjacent mussels. B. On
16 July at the same site, larger animals heated slowly, and were able
to achieve a high equilibrium temperature before being inundated
by the tide. C. Weekly maximum temperature recorded by each logger during July and August 2000.
conditions. However, when conditions change at a rate
that is slower than the thermal response time of the
organism, body temperatures will tend to track environmental conditions more closely (Kingsolver, 1981;
Helmuth, 1999).
While time constants have yet to be calculated for
most intertidal organisms, those for mussels range
from a few minutes for very small individuals to 40
min or more for large animals living in beds (Helmuth,
1998, 1999). Figure 2 presents temperature data recorded from mussel shells of different sizes (Length
5 42 mm, 77 mm, 108 mm, 135 mm) each filled with
silicone (to approximate the specific heat of tissue) and
encasing a series of Thermochron ibuttons (Dallas
Semiconductor) that were programmed to record a single temperature measurement every 20 min. Mussels
were deployed using Z-spar epoxy putty in a wave-
The temperature recorded by a data logger is
affected by its physical characteristics
Given that body temperatures can vary markedly
between species (Fig. 1), and with size within a species
(Fig. 2), how are we to quantify patterns in body temperature under field conditions? Using mathematical
models that keep track of the exchange of heat between an organism and its environment, it is possible
to predict body temperatures of organisms from measurements of local microclimatic parameters, and these
energy balance methods have been used successfully
in both terrestrial (Porter and Gates, 1969; Porter et
al., 1973; Kingsolver, 1979) and intertidal (Johnson,
1975; Thomas, 1987; Bell, 1995; Helmuth, 1998,
1999) environments. However, such an approach requires very detailed knowledge of microclimatic conditions, which can change over very small spatial and
temporal scales.
An alternative method is to measure field temperatures directly. This approach has been used extensively
in terrestrial environments (e.g., Heath, 1964; Kingsolver, 1979; Huey et al., 1989; Huey, 1991) but only
recently have instruments become commercially available that are sufficiently rugged to resist destruction
by waves in most rocky intertidal zones for extended
periods of time (e.g., Tomanek and Somero, 1999;
Dahlhoff et al., 2001; Harley, 2001; Helmuth and Hofmann, 2001; Harley and Helmuth, 2001; Wethey,
A BIOPHYSICAL VIEW
OF INTERTIDAL
2002). There is a potential complication in using these
instruments, however. Namely, the same morphological factors that affect heat flux and body temperature
of organisms will also drive the temperatures of data
loggers (Heath, 1964). Not only will logger shape, size
and color affect the temperature that it records, but
loggers with a time constant that is greater than that
of the organism they are supposed to mimic may miss
brief temperature extremes. Conversely, small loggers
may record temperature maxima that were never experienced by larger organisms. For example, Helmuth
and Hofmann (2001) used morphologically and thermally-matched loggers (where mass*specific heat was
comparable to live animals) to record long-term temperature records of intertidal mussels, and found that
temperatures from the thermally-matched loggers were
generally much more accurate than were adjacent, unmodified (Onset corp., Tidbit) loggers. Fitzhenry et al.
(2001) tested these instruments under controlled conditions, and found that, depending on the position
within the mussel bed, unmodified loggers incurred errors of up to 148C, as opposed to errors of only a few
degrees by the thermally-matched loggers. Thus, while
the use of miniature temperature loggers will undoubtedly serve a significant role in efforts to link physiological and ecological studies of intertidal organisms,
their use must be carefully considered in the context
of the organism in question, and a single logger is
unlikely to serve as an accurate proxy for several species at a given site (e.g., Fig. 1).
Local microclimatic conditions are strongly
dependent on the aspect of the substratum
Intertidal organismal body temperatures can strongly depend on solar radiation, and so even small differences in the angle of the substratum relative to the
sun can have large impacts on body temperature (Williams and Morritt, 1995). Helmuth and Hofmann
(2001) showed that populations of mussels on horizontal, upwards-facing substrata often experienced
temperature maxima that were over 108C hotter than
did populations on vertical, north-facing slopes located
only a few cm away. Furthermore, seasonal temperature patterns varied between these two microsites, with
yearly maxima on horizontal substrata occurring three
months before the yearly maxima experienced by mussels on the vertical substratum (Helmuth and Hofmann, 2001).
These effects of substratum aspect on microclimatic
conditions can have significant effects on communitylevel ecological interactions. Wethey (1983, 1984)
showed that the competitive dominance of one species
of barnacle (Balanus) over another (Chthamalus) varied with substratum aspect, presumably as an indirect
effect of thermal and/or desiccation stresses on the relative physiological performance of each species. Menconi et al. (1999) found that community structure at
an intertidal site in the Mediterranean varied as much
as a function of substratum angle as it did as a function
of tidal height, and Aveni-Deforge and Wethey (2001)
THERMAL STRESS
841
have recently shown that the upper intertidal distribution of the barnacle Chthamalus fragilis changes
markedly with the aspect of the substratum.
Thus, regardless of how ‘‘hot’’ climatic conditions
are at a site, the microclimate in the immediate vicinity
of the organism is the only environment with which
its physiological machinery must contend at that particular stage of its life. This statement at first seems
simple and perhaps axiomatic, but it has significant
implications for how we conduct intertidal ecological
research (Guichard et al., 2001; Hutchinson and Williams, 2001).
If we ascribe patterns in mortality or species distribution to environmental factors such as wave force,
temperature extremes or desiccation stress, we must be
careful to define what the relevant scales are over
which these parameters operate (Guichard et al.,
2001). If, for example, we hypothesize that temperature extremes prevent a species of invertebrate from
inhabiting that particular site, we must also be prepared to explain why the animal is absent from shaded
(e.g., north-facing) microhabitats within the site of interest, where these temperature extremes may not occur.
Movement behavior can rapidly relocate organisms
into different thermal microhabitats
To a sessile or slow-moving organism, the world can
comprise an exceedingly small space, by human standards. Some species of limpets have been shown to
spend their entire lives within a few cm of their home
scars, while others can move upwards of 1 m during
a single tidal cycle (Williams and Morritt, 1995). Organisms such as barnacles, once settled, have virtually
no ability to relocate to a new habitat. Other species,
however, can move very rapidly, and in doing so can
potentially have rather fine-scale control over their
thermal microhabitat (e.g., as in Huey et al., 1989;
Huey, 1991; Williams et al., 2000).
Often, the distance that organisms need to move to
relocate into a different thermal environment is not
great. Schneider et al. (2001) have proposed that differential rates of movement from the bottoms to the
tops of mussel beds leads to selective mortality (due
to thermal stress or dislodgment from waves) of one
species of Mytilus over another, and have recorded
temperature differences of 88C or more between these
microhabitats. Sanford (1999) found a strong correlation between temperature and the maximum intertidal
height at which the seastar Pisaster ochraceous will
feed, although this behavior was much more closely
linked to water temperature than to air temperature.
The timing of exposure to terrestrial conditions is set
by the tidal cycle
Unlike their terrestrial counterparts, intertidal organisms are alternately exposed to two very different
physical environments, and it has long been recognized that the timing of exposure at low tide is likely
to have a critical effect on temperature extremes ex-
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BRIAN HELMUTH
perienced by organisms at a particular site (e.g., Orton,
1929; Bell, 1992; Helmuth, 1998, 1999). However,
only recently have these concepts been explicitly modeled and tested.
For example, in the inner parts of Puget Sound, WA,
the timing of low tides during summer months is consistently closer to mid-day (the time of day with highest levels of solar radiation, and thus, for mussels, the
hottest time of day) than at outer coast sites. Heat budget models for mussels suggest that this effect of timing alone can lead to differences in average body temperatures of 38C between sites separated by only 50–
100 km (Helmuth, 1999). Similarly, because noontime low tides in this region are more common in
spring than in summer, body temperatures are predicted to be hottest during spring months, despite on average hotter climatic conditions during the summer. In
other words, at these sites the climatic conditions are
‘‘hotter’’ near midday in the spring than they are earlier or later in the day in summer (Helmuth, 1999).
Similar patterns are expected to occur over latitudinal gradients. I deployed a series of temperature loggers designed to mimic Mytilus californianus at multiple sites ranging from northern Washington to southern California. All loggers were fixed to horizontal
substrata at a still tidal height of ;MLLW 1 1.5 m.
Up to 5 loggers were deployed at each site, and all
loggers recorded average temperature every 10 min.
Data for each logger and for each site were collapsed
into monthly extremes and monthly average daily
maxima, measures of ‘‘acute’’ and ‘‘chronic’’ stresses,
respectively (Helmuth and Hofmann, 2001).
Preliminary results show that temperature maxima
are surprisingly similar between sites, even though
sites spanned a latitudinal gradient of several thousand
km (Fig. 3). These data also show that even though
differences are small, maximum temperatures are not
necessarily higher at southern sites than at northern
sites. For example, maximum temperatures (Fig. 3a)
at Piedras Blancas (central/southern California) were
more comparable to temperatures recorded at Tatoosh
Island (northern WA) than to Monterey (central CA)
or Strawberry Hill (central OR). During the summer
of 2000, average daily maximum temperatures
(‘‘chronic’’ high temperature exposure) were highest
at the Oregon site (Fig. 3b). Furthermore, the timing
of temperature maxima varied between sites. For example, extreme high yearly maxima at Strawberry Hill
(OR) were recorded in July, as were extreme high temperatures at Tatoosh (WA). Extreme high maxima at
Monterey, in contrast, occurred in September 2000.
Chronic high temperature exposures (Fig. 3b) in
Oregon coincided with yearly extremes in July, but
those at Monterey preceded extreme maxima at that
site by one month (Helmuth and Hofmann, 2001).
These preliminary results suggest that patterns in thermal stress along the west coast of the U.S. are quite
complex, and that each site presents a unique thermal
‘‘signal’’ which varies not only in magnitude, but also
in time history.
FIG. 3. A. Maximum monthly temperatures (‘‘acute’’ high temperature exposure) and B. average daily maxima (‘‘chronic’’ temperature stress) recorded by thermally-matched loggers designed to mimic mussels at sites along the west coast of the U.S. Error bars represent standard deviations of up to 5 loggers per site.
Thermal stress may depend not only on exposure to
temperature extremes, but also to the thermal history
of the temperature signal
While obstacles to measuring and predicting spatial
and temporal patterns in temperature can be overcome,
one large and looming question remains: what aspect
of temperature exposure ‘‘matters’’ to the physiological performance of intertidal organisms? Studies of
heat shock protein (Hsp) production suggest that not
only are the duration and magnitude of exposure to
high temperature important, but also that the thermal
history leading up to the high temperature event may
be crucial (Buckley et al., 2001; Somero, 2002; To-
A BIOPHYSICAL VIEW
OF INTERTIDAL
THERMAL STRESS
843
manek, 2002). The threshold temperature at which
Hsps in Mytilus spp. are induced has been shown to
change seasonally (Roberts et al., 1997; Buckley et al.,
2001), and Tomanek (2002) found that thermal stress
in the intertidal gastropod Tegula appeared to be closely related to daily temperature range, rather than simply to maximum temperature. Krebs and Loescheke
(1994) showed that prior exposure to high temperatures predisposed Drosophila to survive subsequent
exposures, but that this protection reduced their fecundity. Harley and Helmuth (2001) have suggested that
while the upper intertidal distribution to some intertidal species may be set by extreme high temperature
exposure at some sites (as was also shown by AveniDeforge and Wethey, 2001), those of other species
may be related to duration of aerial exposure, which
in turn could be driven by chronic temperature stress,
desiccation, limited feeding, hypoxia or by some combination of these factors (Boyd and Burnett, 1999;
Dahlhoff et al., 2001).
Consider, for example, the two temperature patterns
presented in Figure 4. In the first example (Fig. 4a),
the daily maximum temperature increases gradually
over the course of the tidal series, and may present an
opportunity for the organism to acclimate to thermal
stress. In contrast, high temperature events that are
preceded by periods of cool temperatures (Fig. 4b)
may present a more physiologically challenging signal
to an intertidal organism.
CONCLUSIONS
Measuring patterns of body temperature in intertidal
habitats is by no means as simple as placing a thermometer or temperature logger at the site of interest.
Organisms respond differently to environmental conditions, and one site that is considered relatively ‘‘hot’’
for one species may actually be ‘‘cool’’ for another,
even when organisms are exposed to identical microclimates (Fig. 1). This observation alone argues that
we need a much better understanding of the thermal
ecology of intertidal species if we are to explore the
roles of climate and climate change on these ecosystems. For example, environmental stress models (Menge and Olson, 1990) predict that some prey species are
thermally stressed when their predator is not, or vice
versa. This effect could result not only from differences in physiological response to temperature by
predator and prey, but also from differences in body
temperature under identical climates. As has been
shown by Wethey (1983, 1984), relative competitive
ability between species can be set by thermal exposure.
Conversely, modification of the thermal environments
by other species plays a role in ecological facilitation
(Brawley and Johnson, 1991; Bertness and Leonard,
1997; Jones et al., 1997). Understanding the mechanisms that underlie these interactions requires that we
first investigate the physiological ecology of individual
organisms (Maltby, 1999), and demands that we consider how climate drives the body temperature of each
species.
FIG. 4. Examples of differences in thermal history due to the interactions of climate with tidal cycle, as recorded by thermallymatched loggers designed to mimic mussels, and deployed in southern California (Jalama) in 2001. On days where daily maximum
temperatures increase gradually (A), organisms may be better able
to acclimate to temperature extremes, as opposed to days where
temperature maxima are preceded by cool days (B).
While mass mortality events related to thermal extremes have been reported to occur in intertidal systems (e.g., Suchanek, 1978; Tsuchiya, 1983; Liu and
Morton, 1994; Hutchinson and Williams, 2001), other
less catastrophic physiological effects may also have
important implications to intertidal ecology. For example, Hofmann and Somero (1995) have suggested
that there is a significant energetic cost to heat shock
protein production in mussels, a relationship that has
been clearly demonstrated for Drosophila (Krebs and
Loescheke, 1994; Krebs and Feder, 1997).
Finally, and perhaps most importantly, intertidal
ecologists and physiologists need to uncover the role
of thermal history in driving physiological responses
to high and low temperature exposures (Widdows,
1976; Krebs and Loescheke, 1994; Buckley et al.,
2001; Tomanek, 2002). Not only do intertidal sites display a unique ‘‘thermal signatures’’ as a result of the
interactions of terrestrial climate, tidal cycle and wave
exposure, but significant within-site differences due to
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BRIAN HELMUTH
tidal height and substratum angle also occur. Thus,
while the complex mosaic of thermal stresses in intertidal ecosystems is difficult to quantify, it also has the
potential to serve as an ideal testing ground for examining the role of climate and climate change, and
specifically of fluctuating environmental conditions, on
the physiological ecology of organisms in nature.
ACKNOWLEDGMENTS
The research presented in this paper was funded by
NSF IBN-9985878; support for this symposium was
provided by NSF IBN-0131317. Logistical support for
logger deployment was provided by C. Blanchette, C.
Harley, P. Halpin, M. O’Donnell, C. Svedlund, and the
PISCO research group. C. Blanchette, K. Castillo, T.
Fitzhenry, P. Halpin, C. Harley, M. Henry, G. Hofmann, R. Huey, J. Jost, B. Menge, M. O’Donnell, K.
Schneider and B. Timmerman contributed their insight
into many of the concepts discussed in this paper.
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