Download Effects of temperature change on mussel, Mytilus

Integrative Zoology 2012; 7: 312–327
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doi: 10.1111/j.1749-4877.2012.00310.x
REVIEW
Effects of temperature change on mussel, Mytilus
Mackenzie L. ZIPPAY and Brian HELMUTH
Environment and Sustainability Program, Department of Biological Sciences, University of South Carolina, Columbia, South
Carolina, USA
Abstract
An increasing body of research has demonstrated the often idiosyncratic responses of organisms to climaterelated factors, such as increases in air, sea and land surface temperatures, especially when coupled with nonclimatic stressors. This argues that sweeping generalizations about the likely impacts of climate change on organisms and ecosystems are likely less valuable than process-based explorations that focus on key species and
ecosystems. Mussels in the genus Mytilus have been studied for centuries, and much is known of their physiology and ecology. Like other intertidal organisms, these animals may serve as early indicators of climate change
impacts. As structuring species, their survival has cascading impacts on many other species, making them ecologically important, in addition to their economic value as a food source. Here, we briefly review the categories
of information available on the effects of temperature change on mussels within this genus. Although a considerable body of information exists about the genus in general, knowledge gaps still exist, specifically in our ability to predict how specific populations are likely to respond to the effects of multiple stressors, both climate and
non-climate related, and how these changes are likely to result in ecosystem-level responses. Whereas this genus provides an excellent model for exploring the effects of climate change on natural and human-managed ecosystems, much work remains if we are to make predictions of likely impacts of environmental change on scales
that are relevant to climate adaptation.
Key words: climate change, mussels, Mytilus, organismal responses, temperature
PREDICTING IMPACTS OF CLIMATE
CHANGE USING MODEL SPECIES
An increasing number of studies have recognized the
difficulties inherent in predicting the likely impacts of
Correspondence: Mackenzie L. Zippay, Environment and
Sustainability Program, Department of Biological Sciences,
University of South Carolina, Columbia, SC 29208, USA.
Email: [email protected]
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climate change on natural ecosystems (Hampe 2004;
Kearney & Porter 2009). Because many environmental
conditions under climate change are likely to be novel, it
is unclear how well extrapolations from observations of
contemporary communities will serve as a guide for future responses to environmental change. Moreover, even
when we understand the physiological and demographic influence of single environmental parameters, the interaction of multiple stressors on organisms and communities can be difficult to predict (Crain et al. 2008).
Recent studies have further suggested that local adaptation and acclimatization are key factors in predicting
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© 2012 Wiley Publishing Asia Pty Ltd, ISZS and IOZ/CAS
M. galloprovincialis
M. californianus
M. edulis
M. galloprovincialis
Chemical contaminants
Food availability and wave exposure
Food availability, temperature and wave exposure
Metal bioaccumulation and temperature
Food availability and temperature
Wave exposure
Salinity
Species
M. californianus
M. edulis
M. galloprovincialis
M. edulis
M. galloprovincialis
M. edulis
M. galloprovincialis
M. californianus
M. galloprovincialis
M. trossulus
M. californianus
M. californianus
M. edulis
Stressors
Ocean acidification
Table 1 Interactive effects of biotic and abiotic stressors on Mytilus spp.
climate-related impacts (Kuo & Sanford 2009). Finally,
indirect effects, such as impacts on trophic cascades and
competitive ability, are also known to be affected by environmental conditions that are undergoing significant
change (Wethey 2002; Edwards & Richardson 2004;
Pincebourde et al. 2008; Broitman et al. 2009).
Therefore, exploring these intertwined issues represents a significant challenge, and suggests that a diversity of approaches, including statistically-based/correlative and mechanistic methods (and hybrids and
ensembles thereof) are needed if we are to prepare for
current and forthcoming climate change impacts (Brown
et al. 2011; Burrows et al. 2011). One way forward is to
focus on model species for which considerable existing
information is known. Especially important are species
that have a large impact on other species in their assemblage; for example, keystone predators and structural
species (Monaco & Helmuth 2011).
As part of this volume on the biological effects of climate change, we focus on marine mussels in the genus
Mytilus. Given the ecological (Seed & Suchanek 1992)
and economic (FAO 2010) importance of this species,
an enormous amount is known about its physiology, genetics and ecology. Our goal is not to provide an exhaustive review of all that is known. Not only would that be
impractical, but several excellent overviews of this genus already exist (Bayne 1976; Bayne et al. 1976a,b;
Gosling 1984; Seed & Suchanek 1992). Rather, our intent is to provide examples of what types of information
are known about thermal stress-related effects on mussels in this genus, and to identify where knowledge gaps
still exist.
It is also critical to note that here we focus primarily on the impacts of thermal stress on Mytilus populations, despite the fact that there are multiple stressors
simultaneously acting upon a given organism at a particular time (Table 1). Although significant progress has
been made in exploring the independent effects of these
stressors (Table 1), there is still a significant knowledge gap in our understanding of how multiple stressors affect organisms and ecosystems. For example, a
recent review by Crain et al. (2008) of marine ecosystem studies found that the interaction of environmental temperature with stressors ranging from pH to disease to overfishing could be additive (effects reflect sum
of individual stressors), synergistic (effect greater than
sum of individual stressors) or antagonistic (overall effect less than sum of individual stress effects). Many of
these observations likely resulted from differential impacts operating at different trophic levels (Crain et al.
Reference
(Jones et al. 1995)
(Berge et al. 2006; Bibby et al. 2008; Bechmann et al. 2011)
(Michaelidis et al. 2005; Kurihara et al. 2008)
(Bussell et al. 2008; Deschaseaux et al. 2011)
(Solic et al. 2010; Gombac et al. 2011)
(Carrington 2002; Carrington et al. 2009; Wallin et al. 2011)
(Pfaff et al. 2011)
(Menge et al. 2008; Petes et al. 2008)
(Schneider et al. 2010)
(Schneider et al. 2010)
(Dahlhoff & Menge 1996)
(Dahlhoff et al. 2002)
(Weber et al. 1992; de Zwaan et al. 1995; Eertman et al. 1996; Parry & Pipe 2004; Baines &
Fisher 2008; Sokolova & Lannig 2008; Andral et al. 2011)
(Sunlu 2006; Besada et al. 2011, Maria & Bebianno 2011)
(Eufemia & Epel 2000)
(Hermsen et al. 1994; Luedeking & Koehler 2004; Apraiz et al. 2006; Hong et al. 2009)
(Fernandez et al. 2010; Fernandez-Tajes et al. 2011; Gueguen et al. 2011)
Effects of temperature change on Mytilus
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2008). At the individual level, physiological stress imposed by one factor may reduce the organism’s resistance to other stressors (Pörtner 2010) or the synergistic effect of multi-stressors may be irreversible and lead
to negative consequences. For example, changes in sea
surface temperature can alter the salinity concentration
of the open ocean, which has been shown to influence
the immune response of Mytilus edulis Linnaeus, 1758
(Bussell et al. 2008), thereby increasing the susceptibility to other stressors, such as physical disturbances. As
projected with climate change, an increase in storm frequency and flooding could lead to extended periods of
reduced salinity, thus significantly jeopardizing the wellbeing of this keystone species and ultimately altering
the marine ecosystem (e.g. changes in biodiversity and
aquaculture (Williams et al. 2011)). Similarly, M. trossulus Gould, 1850 and M. galloprovincialis Lamarck,
1819 show lowered resistance to elevated temperatures
in low food regimes (Schneider et al. 2010). Therefore,
although the long history of physiological and ecological studies of this genus will provide considerable insight into future responses to climate change, the interaction of multiple stressors within an ecological context,
the varying vulnerability of populations to changing environmental conditions and the subsequent impacts of
population changes on ecosystems remain relatively unexplored areas.
THE MUSSEL MYTILUS
Mussel beds occur worldwide, inhabiting soft bottoms in cold and temperate waters and rocky substrates
along the coast (Paine 1966; Seed & Suchanek 1992).
Mytilid species are considered ecologically dominant
organisms of the intertidal zone by overgrowing their
competitors (Paine 1994; Robles & Desharnais 2002)
and having the ability to physically alter their environment by attaching byssal threads to the substratum and
conspecifics (Gutiérrez et al. 2003). They also serve as
a food source for many other organisms, including humans (Seed & Suchanek 1992; FAO 2010). These ecosystem engineers (Crooks 2002; Gutiérrez et al. 2003)
are very important to their environment by creating diverse species assemblages (Seed & Suchanek 1992;
Seed 1996; Smith et al. 2006; Büttger et al. 2008; Buschbaum et al. 2009). Furthermore, these voracious filter
feeders provide ecosystem services by filtering toxins
and bacteria that may be in the water column at a rapid
speed of 3–5 l/h (Van Duren 2007).
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The California mussel M. californianus Conrad, 1837
has a broad latitudinal distribution spanning from the
Aleutian Islands of Alaska to northern Mexico of Baja
California (Morris et al. 1980). Its vertical zonation is
centrally located in the mid intertidal zone and found in
dense aggregated beds where wave action is most intense. In contrast, the bay mussel, M. edulis, commonly
inhabits soft bottom mussel beds with calmer waters in
the North Atlantic and North Pacific coasts of the USA,
Europe and even polar waters around the world. M. edulis also are found on hard substrata, and when exposed
to wave action tend to grow more slowly with thicker
shells. The European blue mussel M. galloprovincialis
displays the most global distribution from the Mediterranean, western Australia, Tasmania and New Zealand,
and was introduced to Great Britain, Ireland, France,
Japan and southern California (Lee & Morton 1985;
Geller 1999; Branch & Steffani 2004). This dominant
invader has been successful in replacing the native mussel M. trossulus, in many parts of the world (Brannock
et al. 2009), including the west coast of North America,
where it is thought to have invaded in the early 1900s
via commercial shipping transport (Geller et al. 1994).
M. trossulus exists in the northern Pacific from Siberia to central California, in the Canadian Maritimes, and
in the Baltic Sea. These 2 congeners have co-evolved to
establish a hybrid population in and around San Francisco Bay, California (McDonald & Koehn 1988; Rawson & Hilbish 1995; Geller 1994; Geller et al. 1994).
The patchiness and complexity of distribution patterns reflects ecological and biophysical drivers ranging
from broad biogeographic to microgeographical scales.
For example, M. galloprovincialis can tolerate high saline conditions, warmer water temperatures and more
wave action (Skibinski et al. 1983) than its lower salinity, cooler adapted and less wave-exposed counterpart
(Sarver & Foltz 1993; Wonham 2004; Braby & Somero 2006a). Such abiotic factors likely impact the distribution and performance patterns of the 2 species, and
could induce physiological stress affecting their competitive ability in the field.
For almost 12 000 years, Native Americans along
the west coast of the USA harvested mytilid mussels as
a food source. To this day, they are considered a staple
for some seafood dishes around the world (e.g. Spanish,
Portuguese, French, Dutch, Belgian and Italian) and, according to the Food and Agriculture Organization of the
United Nations (FAO 2010), in 2009, over 60 000 tons
were harvested. Until the early 1990s, M. edulis was the
most common mussel for consumption, but, recently,
© 2012 Wiley Publishing Asia Pty Ltd, ISZS and IOZ/CAS
Effects of temperature change on Mytilus
M. galloprovincialis has become popular. Market value
for mytilid mussels ranged from US $400 to US $1700
per ton in the year 2000, with an estimated average net
worth of US $2 480 000 to US $102 000 000.
PHYSIOLOGICAL EFFECTS
Temperature, one of the most studied abiotic factors,
is a primary driver in setting species’ ranges in terrestrial and marine systems, and has pervasive effects at the
molecular level of an organism that can be transduced to
influence their distribution, abundance and fitness (Hochachka & Somero 2002; Pörtner 2002; Somero 2005).
Changes in environmental temperature are thought to
be the cause of observed biogeographic shifts in many
taxa (Thomas & Lennon 1999; Parmesan & Yohe 2003;
Root et al. 2003; Parmesan 2007) including mussels (e.g.
Jones et al. 2009). Understanding the effects of environmental temperature on Mytilus can be complex, especially for intertidal populations that are exposed to the
aerial environment at low tide, often for many hours.
Given their relatively low metabolic rate, when submerged, a mussel’s body temperature closely approximates that of the surrounding water. In contrast, during aerial exposure at low tide, the body temperatures of
mussels are driven by multiple, interacting environmental factors, of which air temperature is but one. Thus,
aerial body temperatures of mussels are often considerably higher than the temperatures of the surrounding
air and substrate, so much so that air temperature can be
a poor predictor of animal temperature (Helmuth et al.
2011).
To date, the majority of studies of thermal responses
has examined the effects of water temperature, or have
used experiments in water to characterize temperature
effects at low tide. An increasing number of studies are
examining the potential importance of aerial body temperature, and have suggested very different responses in
these 2 media. For example, Jones et al. (2009) found
that the LT50 of M. edulis from the east coast of the USA
ranged from 25 to 37 °C depending on the number of
exposures and time of year at which measurements were
made. In summer (June), thermal tolerances were similar in air and water, but differed by up to 5 °C (lower
in water) in fall (November). These results are generally consistent with those of earlier studies. For example,
Read and Cumming (1967) estimate the upper tolerance
level of M. edulis as 28 °C, and Ritchie (1927) shows
that exposures to water temperatures in excess of 28.9 °C
leads to death within 14 h. Wallis (1975) found that the
lethal temperature of M. edulis varies with acclimation
© 2012 Wiley Publishing Asia Pty Ltd, ISZS and IOZ/CAS
and body size, as well as with photoperiod and salinity
levels.
Denny et al. (2011) report aerial LT50s for M. californianus that range between 36 to 41 °C depending on
thermal history, which is consistent with the observation that these mussels regularly experience body temperatures that exceed 30 °C at several sites along the
west coast of North America during low tide (Elvin &
Gonor 1979; Helmuth et al. 2006a). In Europe, mussels acclimatized to ecologically relevant water temperatures (20–25 °C) had an LT50 of 30–31 °C (Jansen et
al. 2007). M. edulis, from Australia, had an upper lethal
temperature of 28.2 °C when acclimated to 20 °C (Wallis
1975). Tsuchiya (1983) reports mass death (>50% of the
population) of M. edulis following exposure to air temperatures >40 °C, and Harley (2008) reports death in intertidal M. californianus following unusually warm aerial temperatures.
Therefore, although the relative importance of body
temperature during submergence and aerial exposure remains unclear, results suggest that both have impacts
on survival and physiological performance, and that interactions between aerial and aquatic temperature affect mussel physiology (Schneider 2008). Because solar
energy is a dominant driver of aerial body temperature
(Marshall et al. 2010), much of the variability in thermal regimes within rocky intertidal sites is driven by
substratum angle (Denny et al. 2011), with non-shaded surfaces exposing mussels to much higher temperatures than shaded vertical surfaces (Helmuth & Hofmann 2001). As a result, intra-site variability in aerial
body temperature can easily exceed that observed over
latitudinal scales (Helmuth et al. 2006a; Denny et al.
2011). These intra-site variations can contribute to spatial variability in mortality events. For example, when
the timing of the low tide and weather conditions resulted in widespread death of M. californianus in Bodega Bay, CA in 2004 (Harley 2008), death primarily
occurred on southern (equator-ward) facing slopes. Similarly, Schneider and Helmuth (2007) found that levels
of death in M. trossulus and M. galloprovincialis were
higher on non-shaded surfaces, and found overall lower
levels of survival by M. trossulus, which is less thermal
tolerant (Lockwood & Somero 2011a).
One way to quantify responses to thermal stress is
with a temperature coefficient, Q10. An organism’s Q10
reflects the rate of change for a biological, chemical or
physiological processes as a consequence of a 10 °C increase in temperature. This metric varies depending on
levels of acclimation and the temperature range exam-
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ined, and, therefore, can vary between seasons (e.g. Jansen et al. 2007). For most reactions under ‘non-stressful’ conditions, the Q10 ranges from 1 to 3. In contrast,
some energy intensive reactions show Q10 between 4
and 6. Low Q10 values illustrate temperature independence where no significant acclimation to a temperature
change is evident.
Measurements of the effects of temperature on respiratory function can provide an understanding of an organism’s tolerance to the environment (Jansen et al.
2007). When exposed to non-stressful temperatures
(13–22 °C), the oxygen consumption of M. californianus in the field has been shown to be relatively temperature independent, with a Q10 of 1.20, although the filtration rate is more temperature-dependent (Q10 = 2.10)
(Bayne et al. 1976a). Similarly, Widdows (1976) reports
a Q10 for M. edulis of 1.5–2.1 after cycling between 11
and 19 °C for 30 days. Van der Veer et al. (2006) report
an Arrhenius temperature in M. edulis of 5800 K, which
corresponds to a Q10 of 2. Respiration rate increases
with temperature in the Mediterranean mussel (M. galloprovincialis) with Q10 values >2, with good acclimatization between 6 and 19 °C (Barbariol & Razouls 2000).
Filtration rate and heart beat frequency in Mytilus spp.
are also completely temperature dependent (Bayne et al.
1976a), such that differences in thermal tolerance of cardiac function in Mytilus may reflect a temperature-compensation adaptation, and help to explain the successful
replacement of native species by invasive species (Braby
& Somero 2006b).
Physiological responses of mussels exposed to stressful temperatures are more complex, especially when
considering the interactions between physiological
stress experienced by intertidal mussels alternating between aerial and aquatic habitats. Mytilus spp. show a
reduction in aerobic capacity at high and low temperatures (Bayne et al. 1976a; Anestis et al. 2007) and display tissue-specific anaerobic activities (Lockwood &
Somero 2011a). For example, during short periods of
aerial exposure accumulation of alanine and malate,
end-products of anaerobic metabolism, were elevated in
the adductor muscle of M. californianus (Bayne et al.
1976b), probably an attempt to maintain redox balance
and to make up for energy deficiency from oxygen deprivation. Diffusion of oxygen into water trapped by the
mantle cavity during periods of aerial exposure is common among intertidal bivalves; however, congeneric
differences in aerial rates of oxygen consumption have
been reported for mussels. For example, M. californianus, a species with marked shell gaping in air, consumes
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a high rate of oxygen between 30 and 80% of the immersed rate (Bayne et al. 1976b) compared to M. edulis
and M. galloprovincialis, whose shell valves are typically closed in air and consume much less oxygen, 4–17%
of the immersed rate (Widdows et al. 1979; Widdows &
Shick 1985). Different species of mussels utilize different metabolic processes as a means to conserve energy
during aerial exposure by decreasing their metabolic activity when shifting from aerobic to anaerobic metabolism (Page et al. 1998; Anestis et al. 2007; Anestis et al.
2010). Results by Bayne et al. (1976a) suggest an interaction between stress experienced during aerial exposure and during submergence, in which a ‘debt’ accrued
during low tide is then ‘paid’ at high tide (Bayne et al.
1976b). Schneider (2008) shows that mussels acclimated to warmer water temperatures (18 °C) were less susceptible to death during aerial exposure (30 °C). However, when animals were grown in cooler (12 °C) water
temperatures, M. trossulus showed higher death and
lower growth than compared to M. galloprovincialis.
Temperature can have a major effect on organismal
performance and growth by influencing filtration rates,
absorption and utilization of available food (Widdows
1976; Kittner & Riisgard 2005; Jansen et al. 2007).
Mussel growth has been linked to temperature and food
availability (Page & Hubbard 1987; Blanchette et al.
2007; Schneider et al. 2010), where mussels are more
likely to grow faster or larger at warmer climatic sites
when food abundances are greater (Lesser et al. 2010)
from phytoplankton blooms, upwelling events and/or
coastal currents (Menge et al. 2008). The costs associated with acclimatizing to thermal stress could be offset
by the availability of significantly higher concentrations
of food (Lesser et al. 1994; Dahlhoff et al. 2002), consequently compounding physiological trade-offs by allocating energy from reproduction towards physiological defenses (Bayne 2004).
The timing and success of reproduction is heavily
weighed upon temperature and food availability (Sastry
1966; Suarez et al. 2005; Lemaire et al. 2006; Okaniwa
et al. 2010). For example, mussels (M. californianus)
near the high edge of the mussel bed invested less energy into reproduction and spawned early in the summer
compared to those in the lower edge, where food availability was high and reproduction occurred throughout
the year (Petes et al. 2008). Thus, by mobilizing more
energy to reproduction, less energy is devoted to physiological defenses (Petes et al. 2008). These trade-offs
become economically important when temperature influences Mytilus in aquaculture and hatchery facili-
© 2012 Wiley Publishing Asia Pty Ltd, ISZS and IOZ/CAS
Effects of temperature change on Mytilus
ties (LeBlanc et al. 2005, Ruiz et al. 2008) by reducing
the capacity for growth and the maturation of gametes
(Fearman & Moltschaniwskyj 2010). Similarly, in natural populations, reproduction and growth are vital to
the formation of stable populations. More recently, biophysical approaches (e.g. dynamic energy budget models) have been tested on different Mytilus spp. to predict
how much energy is assimilated and assigned to physiological processes (i.e. growth, development and reproduction) under fluctuating environmental conditions,
such as thermal variation and food availability (Cardoso et al. 2006; van der Veer et al. 2006; Freitas et al.
2009; Sará et al. 2011). The functionality of these models could provide an understanding of the possible constraints on current intertidal distribution and abundance,
while forecasting how they might be altered under predicted climate change scenarios (Kearney et al. 2010).
A host of new molecular and biochemical techniques have opened the door to a deeper understanding
of the subcellular level responses that ultimately result
in whole-organism responses to stress, such as growth
(Dahlhoff 2004; Somero 2011). A commonly used approach has been to measure the heat shock response, a
complex of molecular chaperones that mitigate cellular
damage and restore cellular homeostasis (Hochachka &
Somero 2002; Kültz 2005). Molecular chaperones, collectively known as heat shock proteins (Hsps), stabilize
the unfolding of proteins to prevent further denaturation
and assist in the refolding to its native stable state. Hsps
play an important role in protein homeostasis and are
strong indicators of stress-induced protein damage. Mytilus spp. show changes in cellular response to thermal
stress across geographic scales (Place et al. 2008, 2012;
Dutton & Hofmann 2009; Lesser et al. 2010) and seasonal changes have been demonstrated as well (Chapple et al. 1998; Jansen et al. 2007; Gracey et al. 2008;
Ioannou et al. 2009; Banni et al. 2011). Measurement
of the heat shock response at small spatial scales has
revealed the importance of microhabitat (Hofmann &
Somero 1995; Buckley et al. 2001; Halpin et al. 2004).
For example, the body temperatures of M. californianus
are consistently higher on horizontal (non-shaded) surfaces than on vertical shaded surfaces, which is reflected in the amount of inducible Hsp70 that they produce
(Helmuth & Hofmann 2001). Differences in protein homeostasis have also been measured using ubiquitin, a
regulatory protein that covalently binds to degraded and
miss-folded proteins (Glickman & Ciechanover 2002);
M. galloprovincialis exhibits more warm adapted proteins, while M. trossulus are more cold-adapted (Hofmann & Somero 1995, 1996; Dutton & Hofmann 2008).
© 2012 Wiley Publishing Asia Pty Ltd, ISZS and IOZ/CAS
More recently, some physiologists investigating cellular stress are turning their attention to ‘omic’ experimentation to understand how the ‘whole’ organism confronts these environmental factors and how it may affect
energy allocation. Studying the expression of thousands
of genes at the transcriptional level, known as transcriptomics, is a tool that has begun to translate the understanding of how environmental signals affect physiological responses. In M. californianus, transcriptional
differences have been seen across spatial (Place et al.
2008, 2012) and temporal (Gracey et al. 2008; Banni et
al. 2011) scales, while also revealing a comparative response between invader and native blue mussels (Lockwood et al. 2010; Lockwood & Somero 2011b). Similarly, proteomics have provided more information about
the temperature-dependent patterning between congeners of Mytilus (Lopez et al. 2002; Tomanek & Zuzow
2010) by analyzing the changes in protein pool composition. Investigating sublethal thermal stress at the cellular level can reveal important information about the
subtle patterns of cellular damage and repair, while providing physiologists with molecular ‘biomarkers’ for
characterizing the degree of stress and sensitivity among
species and how it may impact the energy allocation of
an organism. Importantly, recent studies have also demonstrated the presence of circadian rhythms in transcription of proteins in intertidal animals, potentially complicating interpretations of field measurements (Gracey et
al. 2008; Connor & Gracey 2011).
INDIRECT EFFECTS OF
TEMPERATURE-TROPHIC CASCADES
AND RATES OF COMPETITION
Changes in environmental conditions have a direct
impact on an organism’s physiology; however, indirect
effects that operate through impacts on an organism’s
prey, predators and competitors may be equally as important (e.g. Wethey 2002). Sanford (1999, 2002) shows
that predation rates by the seastar Pisaster ochraceus
(Brandt, 1835) on M. californianus are significantly affected by water temperature. Pincebourde et al. (2008)
shows that aerial (low tide) body temperatures also affect rates of predation by Pisaster, but that this effect
differs markedly depending on the duration of exposure
to elevated aerial temperatures.
Because body temperature can be affected by an organism’s morphology and behavior, the thermal niche
of a predator (e.g. a sea star) and its prey (mussel) can
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be significantly different even though they occupy identical microhabitats in the intertidal zone (Broitman et al.
2009). The predator–prey interactions between Pisaster
and Mytilus can be sensitive to slight shifts in temperature due to the timing and intensity of seasonal events
(Sanford 1999; Pincebourde et al. 2008, 2009; Harley 2011), and this could ultimately change the intertidal ecosystem by altering the food web of the community assemblage (Paine 1966). For example, whether ‘prey
stress’ or ‘consumer stress’ models apply (Menge & Olson 1990) will likely vary from site to site, as well as
between seasons (Monaco & Helmuth 2011).
The ability for an organism to invade a new region
may be closely linked to its thermal adaptation (Stachowicz et al. 2002), and understanding the attributes that
facilitate or interfere with the success of an invasion
is vital to predict and forecast future invasions. In the
USA and Japan, invasion by M. galloprovincialis has replaced the naturally occurring M. trossulus (Wilkens et
al. 1983; Geller 1999), and hybrids between M. galloprovincialis and both M. edulis (Hilbish et al. 1994) and
M. trossulus (Suchanek et al. 1997) are common. This
effect can be observed over geographic scales (Hilbish
et al. 2010) as well as within sites due to high thermal
heterogeneity (Schneider & Helmuth 2007). Currently, on the west coast of the USA, the cold-water adapted
mussel (M. trossulus) resides primarily in northern California and Oregon, while the warm-adapted mussel (M.
galloprovincialis) is almost exclusively in southern California (Sarver & Foltz 1993; Suchanek et al. 1997). At
smaller scales, both species coexist at central California sites, but M. galloprovincialis is most common on
sunny intertidal substrata and M. trossulus is more common on shaded surfaces (Schneider & Helmuth 2007).
Substantial evidence supports that these species differ
in their thermal physiology, including cellular processes (Hofmann & Somero 1996; Fields et al. 2006; Braby
& Somero 2006b; Evans & Somero 2010), enzymatic
activity (Lockwood & Somero 2011a), molecular function (Lockwood et al. 2010; Tomanek & Zuzow 2010),
growth rate (Braby & Somero 2006a; Schneider 2008;
Shinen & Morgan 2009) and survival (Matson et al.
2003; Schneider 2008). Differences found between these
two species suggest that climate change might facilitate
species invasion, with the invader species (M. galloprovincialis) having a higher capacity to cope with elevated
temperatures, therefore having a competitive advantage
over the native species. Recent data suggest that current
environmental conditions, such as temperature, could
318
be preventing M. galloprovincialis from further invading northward into California (Hilbish et al. 2010). How
these patterns will likely be altered by climate change
remains an open question (Jones et al. 2010).
OBSERVED CHANGES IN NATURE
Range shifts in nature can occur either through gradual change in average conditions or through rare but extreme events (Cury & Shannon 2004; Wooster & Zhang
2004; Wethey et al. 2011). Compared to terrestrial ecosystems, marine organisms tend to have larger range
distributions, and marine distribution patterns also appear to be changing much more rapidly than terrestrial range edges (Helmuth et al. 2006b). Often, these distribution patterns are far more complicated than simple
poleward range shifts. For example, M. californianus
along the west coast of the USA experience thermal mosaics rather than latitudinal gradients (Helmuth et al.
2006a) in aerial body temperature, which is reflected
in their physiological performance (Place et al. 2008,
2012). For example, Place et al. (2008) show that mussels in central Oregon, where local conditions can lead
to high temperatures, exhibit higher levels of upregulation in genes related to thermal stress than do mussels several thousand kilometers to the south. Similarly,
changes in distribution are not monotonic in time, and
reversals have been observed (Hilbish et al. 2010), in
accordance with the overlay of increases in temperature
resulting from climate change with temporally varying patterns such as the El Niño-Southern Oscillation
(ENSO). Regions influenced by ENSO can cause rapid
warm episodes and ‘set backs’ during cool periods (Walther et al. 2002). Populations can shift their competitive
abilities at their northern and southern boundaries and
at the upper vertical distributional boundary (Denny &
Paine 1998) where temperatures may be too high or too
low for growth, reproduction and/or survival. This marginal shift could lead to a downward swing, resulting in
local extinction, poleward expansion or range retraction.
Range shifts vary greatly between species, and the distributions of Mytilus populations all over the world are
responding differently to climate change. For example,
M. californianus along the Strait of Juan de Fuca near
Washington state have decreased their vertical distribution by 51% over the past 52 years (Harley 2011), and
along the western coast of North America, M. galloprovincialis has contracted southward over 540 km over the
past 10 years (Hilbish et al. 2010).
© 2012 Wiley Publishing Asia Pty Ltd, ISZS and IOZ/CAS
Effects of temperature change on Mytilus
FORECASTING FUTURE RESPONSES
Global climate change is now the backdrop against
which all ecological interactions occur. As a result, understanding the processes by which temperature and
other climate-related environmental factors drive organismal biology and population and community ecology
have taken on a new urgency. In particular, because climate change in many cases will present organisms with
conditions never before experienced, the ability to project changes in nature from studies conducted under controlled conditions that reflect those novel environments
is becoming increasingly vital (Chown & Gaston 2008).
Several approaches have been used to project future
changes. Climate envelope models (predictions of future shifts in range edges produced by correlating environmental conditions at existing range boundaries) have
become useful tools for making broad-scale predictions about how climate change is likely to affect species boundaries (Hampe 2004). However, a number of
recent reviews have criticized these methods because:
(i) they often extrapolate from current environmental conditions to novel conditions; (ii) they ignore indirect effects, such as biotic interactions (although these
might be implicit in the observed correlations); (iii) they
are unable to account for local adaptation and/or acclimatization (Kuo & Sanford 2009); and (iv) they do not
incorporate non-climatic factors that might change on
local and regional scales (Mustin et al. 2007). As a result, the ‘stationarity’ of these models (i.e. the ability to
predict changes in one part of the world from measurements made in another part of the world) is a serious issue. Alternative approaches base future projections on
physiological performance (Chown & Gaston 2008).
These mechanistic, or process-based models, are inherently much more time consuming than statisticallybased models, but have been shown to produce different
predictions than envelope models (Kearney et al. 2008).
By comparing physiological limits made via measurements under controlled conditions against future conditions estimated at local or regional scales, these models
can predict changes in range boundaries that are much
more reflective of the actual mosaics that are being observed (as opposed to monotonic range shifts [Helmuth
et al. 2006a; Burrows et al. 2011]).
Newer approaches have begun to connect biophysical models with energetics models to predict not only
changes in range boundaries, but also to predict altered
growth and reproduction (Kearney et al. 2010; Sará et
al. 2011). These models fully incorporate what is known
© 2012 Wiley Publishing Asia Pty Ltd, ISZS and IOZ/CAS
about physiological responses to changing environmental conditions using energetics approaches, such as Dynamic Energy Budget models (Kooijman 2009). For
example, Sará et al. (2011) apply this approach to M.
galloprovincialis in the Mediterranean; their results suggest that while range limitations in the intertidal zone
were set by lethal limits at some sites, at others the absence of mussels was more likely set by conditions that
led to reproductive failure.
The obvious drawback of these latter approaches is
that they require considerable detail about the organism
in question and, therefore, are not practical for examining large numbers of species. In this regard, model species such as Mytilus might serve as an excellent focal
point because of their economic and ecological importance, and the extensive knowledge compiled about animals in this genus. Nevertheless, a host of challenges
remain, including a better understanding of the roles of
acclimatization and local adaptation in determining the
sensitivity of animals to either gradual or abrupt change;
the role of indirect effects on community-level processes, and especially the role of interacting stressors, both
climatic and non-climatic in nature. An understanding
of all of these processes will be key if we are to project
the likely impact of climate change on this animal.
ACKNOWLEDGMENTS
The authors were supported by grants from NASA
(NNX07AF20G) and NSF (OCE-0926581).
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