Effects of temperature change on mussel, Mytilus · 2013-04-12 · 008). At the individual level, physiological stress im-posed by one factor may reduce the organism’s resis-tance

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Integrative Zoology 2012; 7: 312–327 doi: 10.1111/j.1749-4877.2012.00310.x

REVIEW

Effects of temperature change on mussel, Mytilus

Mackenzie L. ZIPPAY and Brian HELMUTHEnvironment and Sustainability Program, Department of Biological Sciences, University of South Carolina, Columbia, South Carolina, USA

AbstractAn increasing body of research has demonstrated the often idiosyncratic responses of organisms to climate-related factors, such as increases in air, sea and land surface temperatures, especially when coupled with non-climatic stressors. This argues that sweeping generalizations about the likely impacts of climate change on or-ganisms 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 physiol-ogy 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 eco-logically 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 consid-erable body of information exists about the genus in general, knowledge gaps still exist, specifically in our abil-ity 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 ge-nus provides an excellent model for exploring the effects of climate change on natural and human-managed eco-systems, 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

Correspondence: Mackenzie L. Zippay, Environment and Sustainability Program, Department of Biological Sciences, University of South Carolina, Columbia, SC 29208, USA.Email: [email protected]

PREDICTING IMPACTS OF CLIMATE CHANGE USING MODEL SPECIES

An increasing number of studies have recognized the difficulties inherent in predicting the likely impacts of

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 fu-ture responses to environmental change. Moreover, even when we understand the physiological and demograph-ic influence of single environmental parameters, the in-teraction of multiple stressors on organisms and com-munities can be difficult to predict (Crain et al. 2008). Recent studies have further suggested that local adap-tation and acclimatization are key factors in predicting

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Effects of temperature change on Mytilus

© 2012 Wiley Publishing Asia Pty Ltd, ISZS and IOZ/CAS

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 en-vironmental conditions that are undergoing significant change (Wethey 2002; Edwards & Richardson 2004; Pincebourde et al. 2008; Broitman et al. 2009).

Therefore, exploring these intertwined issues repre-sents a significant challenge, and suggests that a diver-sity of approaches, including statistically-based/cor-relative 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 assem-blage; for example, keystone predators and structural species (Monaco & Helmuth 2011).

As part of this volume on the biological effects of cli-mate 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, ge-netics and ecology. Our goal is not to provide an exhaus-tive review of all that is known. Not only would that be impractical, but several excellent overviews of this ge-nus already exist (Bayne 1976; Bayne et al. 1976a,b; Gosling 1984; Seed & Suchanek 1992). Rather, our in-tent is to provide examples of what types of information are known about thermal stress-related effects on mus-sels in this genus, and to identify where knowledge gaps still exist.

It is also critical to note that here we focus primari-ly on the impacts of thermal stress on Mytilus popula-tions, despite the fact that there are multiple stressors simultaneously acting upon a given organism at a par-ticular time (Table 1). Although significant progress has been made in exploring the independent effects of these stressors (Table 1), there is still a significant knowl-edge gap in our understanding of how multiple stress-ors affect organisms and ecosystems. For example, a recent review by Crain et al. (2008) of marine ecosys-tem studies found that the interaction of environmen-tal temperature with stressors ranging from pH to dis-ease to overfishing could be additive (effects reflect sum of individual stressors), synergistic (effect greater than sum of individual stressors) or antagonistic (overall ef-fect less than sum of individual stress effects). Many of these observations likely resulted from differential im-pacts operating at different trophic levels (Crain et al.

Tabl

e 1

Inte

ract

ive

effe

cts o

f bio

tic a

nd a

biot

ic st

ress

ors o

n M

ytilu

s spp

.

Stre

ssor

sSp

ecie

sR

efer

ence

Oce

an a

cidi

ficat

ion

M. c

alifo

rnia

nus

(Jon

es e

t al.

1995

)M

. edu

lis(B

erge

et a

l. 20

06; B

ibby

et a

l. 20

08; B

echm

ann

et a

l. 20

11)

M. g

allo

prov

inci

alis

(Mic

hael

idis

et a

l. 20

05; K

urih

ara

et a

l. 20

08)

Salin

ityM

. edu

lis(B

usse

ll et

al.

2008

; Des

chas

eaux

et a

l. 20

11)

M. g

allo

prov

inci

alis

(Sol

ic e

t al.

2010

; Gom

bac

et a

l. 20

11)

Wav

e ex

posu

reM

. edu

lis(C

arrin

gton

200

2; C

arrin

gton

et a

l. 20

09; W

allin

et a

l. 20

11)

M. g

allo

prov

inci

alis

(Pfa

ff et

al.

2011

)M

. cal

iforn

ianu

s(M

enge

et a

l. 20

08; P

etes

et a

l. 20

08)

Food

ava

ilabi

lity

and

tem

pera

ture

M. g

allo

prov

inci

alis

(Sch

neid

er e

t al.

2010

)M

. tro

ssul

us(S

chne

ider

et a

l. 20

10)

Food

ava

ilabi

lity

and

wav

e ex

posu

reM

. cal

iforn

ianu

s(D

ahlh

off &

Men

ge 1

996)

Food

ava

ilabi

lity,

tem

pera

ture

and

wav

e ex

posu

reM

. cal

iforn

ianu

s(D

ahlh

off e

t al.

2002

)M

etal

bio

accu

mul

atio

n an

d te

mpe

ratu

reM

. edu

lis(W

eber

et a

l. 19

92; d

e Zw

aan

et a

l. 19

95; E

ertm

an e

t al.

1996

; Par

ry &

Pip

e 20

04; B

aine

s &

Fish

er 2

008;

Sok

olov

a &

Lan

nig

2008

; And

ral e

t al.

2011

) M

. gal

lopr

ovin

cial

is(S

unlu

200

6; B

esad

a et

al.

2011

, Mar

ia &

Beb

iann

o 20

11)

Che

mic

al c

onta

min

ants

M. c

alifo

rnia

nus

(Euf

emia

& E

pel 2

000)

M. e

dulis

(Her

mse

n et

al.

1994

; Lue

deki

ng &

Koe

hler

200

4; A

prai

z et

al.

2006

; Hon

g et

al.

2009

) M

. gal

lopr

ovin

cial

is(F

erna

ndez

et a

l. 20

10; F

erna

ndez

-Taj

es e

t al.

2011

; Gue

guen

et a

l. 20

11)

314

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M.L. Zippay and B. Helmuth


2008). At the individual level, physiological stress im-posed by one factor may reduce the organism’s resis-tance to other stressors (Pörtner 2010) or the synergis-tic 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 susceptibil-ity to other stressors, such as physical disturbances. As projected with climate change, an increase in storm fre-quency and flooding could lead to extended periods of reduced salinity, thus significantly jeopardizing the well-being of this keystone species and ultimately altering the marine ecosystem (e.g. changes in biodiversity and aquaculture (Williams et al. 2011)). Similarly, M. tros-sulus 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 ecolog-ical studies of this genus will provide considerable in-sight into future responses to climate change, the inter-action of multiple stressors within an ecological context, the varying vulnerability of populations to changing en-vironmental conditions and the subsequent impacts of population changes on ecosystems remain relatively un-explored areas.

THE MUSSEL MYTILUSMussel beds occur worldwide, inhabiting soft bot-

toms 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 environ-ment 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 hu-mans (Seed & Suchanek 1992; FAO 2010). These eco-system engineers (Crooks 2002; Gutiérrez et al. 2003) are very important to their environment by creating di-verse species assemblages (Seed & Suchanek 1992; Seed 1996; Smith et al. 2006; Büttger et al. 2008; Bus-chbaum 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).

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 in-tense. 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. edu-lis 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 Mediter-ranean, 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 mus-sel 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 Sibe-ria 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 Fran-cisco Bay, California (McDonald & Koehn 1988; Raw-son & Hilbish 1995; Geller 1994; Geller et al. 1994). The patchiness and complexity of distribution pat-terns reflects ecological and biophysical drivers ranging from broad biogeographic to microgeographical scales. For example, M. galloprovincialis can tolerate high sa-line conditions, warmer water temperatures and more wave action (Skibinski et al. 1983) than its lower salin-ity, cooler adapted and less wave-exposed counterpart (Sarver & Foltz 1993; Wonham 2004; Braby & Some-ro 2006a). Such abiotic factors likely impact the distri-bution and performance patterns of the 2 species, and could induce physiological stress affecting their compet-itive 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, ac-cording 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,

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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 EFFECTSTemperature, one of the most studied abiotic factors,

is a primary driver in setting species’ ranges in terrestri-al 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 (Ho-chachka & 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 environ-mental temperature on Mytilus can be complex, espe-cially for intertidal populations that are exposed to the aerial environment at low tide, often for many hours. Given their relatively low metabolic rate, when sub-merged, a mussel’s body temperature closely approx-imates that of the surrounding water. In contrast, dur-ing aerial exposure at low tide, the body temperatures of mussels are driven by multiple, interacting environmen-tal factors, of which air temperature is but one. Thus, aerial body temperatures of mussels are often consid-erably 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 tem-perature, 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 sim-ilar in air and water, but differed by up to 5 °C (lower in water) in fall (November). These results are general-ly 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

and body size, as well as with photoperiod and salinity levels.

Denny et al. (2011) report aerial LT50s for M. cali-fornianus that range between 36 to 41 °C depending on thermal history, which is consistent with the observa-tion that these mussels regularly experience body tem-peratures 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, mus-sels acclimatized to ecologically relevant water temper-atures (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 tem-peratures >40 °C, and Harley (2008) reports death in in-tertidal M. californianus following unusually warm aer-ial temperatures.

Therefore, although the relative importance of body temperature during submergence and aerial exposure re-mains unclear, results suggest that both have impacts on survival and physiological performance, and that in-teractions between aerial and aquatic temperature af-fect mussel physiology (Schneider 2008). Because solar energy is a dominant driver of aerial body temperature (Marshall et al. 2010), much of the variability in ther-mal regimes within rocky intertidal sites is driven by substratum angle (Denny et al. 2011), with non-shad-ed surfaces exposing mussels to much higher temper-atures than shaded vertical surfaces (Helmuth & Hof-mann 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 spa-tial variability in mortality events. For example, when the timing of the low tide and weather conditions re-sulted in widespread death of M. californianus in Bo-dega Bay, CA in 2004 (Harley 2008), death primarily occurred on southern (equator-ward) facing slopes. Sim-ilarly, 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 in-crease 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. Jan-sen et al. 2007). For most reactions under ‘non-stress-ful’ 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 indepen-dence where no significant acclimation to a temperature change is evident.

Measurements of the effects of temperature on respi-ratory function can provide an understanding of an or-ganism’s tolerance to the environment (Jansen et al. 2007). When exposed to non-stressful temperatures (13–22 °C), the oxygen consumption of M. california-nus in the field has been shown to be relatively temper-ature independent, with a Q10 of 1.20, although the fil-tration 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. gallo-provincialis) with Q10 values >2, with good acclimatiza-tion 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 car-diac function in Mytilus may reflect a temperature-com-pensation adaptation, and help to explain the successful replacement of native species by invasive species (Braby & Somero 2006b).

Physiological responses of mussels exposed to stress-ful temperatures are more complex, especially when considering the interactions between physiological stress experienced by intertidal mussels alternating be-tween aerial and aquatic habitats. Mytilus spp. show a reduction in aerobic capacity at high and low tempera-tures (Bayne et al. 1976a; Anestis et al. 2007) and dis-play 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 de-privation. Diffusion of oxygen into water trapped by the mantle cavity during periods of aerial exposure is com-mon among intertidal bivalves; however, congeneric differences in aerial rates of oxygen consumption have been reported for mussels. For example, M. california-nus, a species with marked shell gaping in air, consumes

a high rate of oxygen between 30 and 80% of the im-mersed rate (Bayne et al. 1976b) compared to M. edulis and M. galloprovincialis, whose shell valves are typical-ly 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 differ-ent metabolic processes as a means to conserve energy during aerial exposure by decreasing their metabolic ac-tivity when shifting from aerobic to anaerobic metabo-lism (Page et al. 1998; Anestis et al. 2007; Anestis et al. 2010). Results by Bayne et al. (1976a) suggest an inter-action between stress experienced during aerial expo-sure 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 acclimat-ed to warmer water temperatures (18 °C) were less sus-ceptible to death during aerial exposure (30 °C). How-ever, 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 associ-ated 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), con-sequently compounding physiological trade-offs by al-locating energy from reproduction towards physiologi-cal 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 ener-gy into reproduction and spawned early in the summer compared to those in the lower edge, where food avail-ability was high and reproduction occurred throughout the year (Petes et al. 2008). Thus, by mobilizing more energy to reproduction, less energy is devoted to phys-iological defenses (Petes et al. 2008). These trade-offs become economically important when temperature in-fluences Mytilus in aquaculture and hatchery facili-

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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 nat-ural populations, reproduction and growth are vital to the formation of stable populations. More recently, bio-physical approaches (e.g. dynamic energy budget mod-els) have been tested on different Mytilus spp. to predict how much energy is assimilated and assigned to physi-ological processes (i.e. growth, development and repro-duction) under fluctuating environmental conditions, such as thermal variation and food availability (Cardo-so et al. 2006; van der Veer et al. 2006; Freitas et al. 2009; Sará et al. 2011). The functionality of these mod-els could provide an understanding of the possible con-straints on current intertidal distribution and abundance, while forecasting how they might be altered under pre-dicted climate change scenarios (Kearney et al. 2010).

A host of new molecular and biochemical tech-niques 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 ap-proach 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, col-lectively 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. Myt-ilus 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 sea-sonal changes have been demonstrated as well (Chap-ple 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) sur-faces than on vertical shaded surfaces, which is reflect-ed in the amount of inducible Hsp70 that they produce (Helmuth & Hofmann 2001). Differences in protein ho-meostasis 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 pro-teins, while M. trossulus are more cold-adapted (Hof-mann & Somero 1995, 1996; Dutton & Hofmann 2008).

More recently, some physiologists investigating cel-lular stress are turning their attention to ‘omic’ experi-mentation to understand how the ‘whole’ organism con-fronts these environmental factors and how it may affect energy allocation. Studying the expression of thousands of genes at the transcriptional level, known as transcrip-tomics, is a tool that has begun to translate the under-standing of how environmental signals affect physio-logical 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 re-sponse between invader and native blue mussels (Lock-wood et al. 2010; Lockwood & Somero 2011b). Simi-larly, proteomics have provided more information about the temperature-dependent patterning between conge-ners of Mytilus (Lopez et al. 2002; Tomanek & Zuzow 2010) by analyzing the changes in protein pool compo-sition. Investigating sublethal thermal stress at the cel-lular level can reveal important information about the subtle patterns of cellular damage and repair, while pro-viding 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 dem-onstrated the presence of circadian rhythms in transcrip-tion of proteins in intertidal animals, potentially compli-cating 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 im-portant (e.g. Wethey 2002). Sanford (1999, 2002) shows that predation rates by the seastar Pisaster ochraceus (Brandt, 1835) on M. californianus are significantly af-fected by water temperature. Pincebourde et al. (2008) shows that aerial (low tide) body temperatures also af-fect 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 or-ganism’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 iden-tical microhabitats in the intertidal zone (Broitman et al. 2009). The predator–prey interactions between Pisaster and Mytilus can be sensitive to slight shifts in temper-ature due to the timing and intensity of seasonal events (Sanford 1999; Pincebourde et al. 2008, 2009; Har-ley 2011), and this could ultimately change the intertid-al ecosystem by altering the food web of the communi-ty assemblage (Paine 1966). For example, whether ‘prey stress’ or ‘consumer stress’ models apply (Menge & Ol-son 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 (Stacho-wicz 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 re-placed the naturally occurring M. trossulus (Wilkens et al. 1983; Geller 1999), and hybrids between M. gallo-provincialis 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). Current-ly, on the west coast of the USA, the cold-water adapted mussel (M. trossulus) resides primarily in northern Cal-ifornia and Oregon, while the warm-adapted mussel (M. galloprovincialis) is almost exclusively in southern Cal-ifornia (Sarver & Foltz 1993; Suchanek et al. 1997). At smaller scales, both species coexist at central Califor-nia sites, but M. galloprovincialis is most common on sunny intertidal substrata and M. trossulus is more com-mon on shaded surfaces (Schneider & Helmuth 2007). Substantial evidence supports that these species differ in their thermal physiology, including cellular process-es (Hofmann & Somero 1996; Fields et al. 2006; Braby & Somero 2006b; Evans & Somero 2010), enzymatic activity (Lockwood & Somero 2011a), molecular func-tion (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. gallopro-vincialis) 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

be preventing M. galloprovincialis from further invad-ing 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 NATURERange shifts in nature can occur either through grad-

ual change in average conditions or through rare but ex-treme events (Cury & Shannon 2004; Wooster & Zhang 2004; Wethey et al. 2011). Compared to terrestrial eco-systems, marine organisms tend to have larger range distributions, and marine distribution patterns also ap-pear to be changing much more rapidly than terrestri-al range edges (Helmuth et al. 2006b). Often, these dis-tribution patterns are far more complicated than simple poleward range shifts. For example, M. californianus along the west coast of the USA experience thermal mo-saics 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 mus-sels in central Oregon, where local conditions can lead to high temperatures, exhibit higher levels of upregu-lation in genes related to thermal stress than do mus-sels 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 vary-ing patterns such as the El Niño-Southern Oscillation (ENSO). Regions influenced by ENSO can cause rapid warm episodes and ‘set backs’ during cool periods (Wal-ther 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 mar-ginal shift could lead to a downward swing, resulting in local extinction, poleward expansion or range retraction. Range shifts vary greatly between species, and the dis-tributions 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 distribu-tion by 51% over the past 52 years (Harley 2011), and along the western coast of North America, M. gallopro-vincialis has contracted southward over 540 km over the past 10 years (Hilbish et al. 2010).

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FORECASTING FUTURE RESPONSESGlobal climate change is now the backdrop against

which all ecological interactions occur. As a result, un-derstanding the processes by which temperature and other climate-related environmental factors drive organ-ismal biology and population and community ecology have taken on a new urgency. In particular, because cli-mate change in many cases will present organisms with conditions never before experienced, the ability to proj-ect changes in nature from studies conducted under con-trolled 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 fu-ture shifts in range edges produced by correlating envi-ronmental conditions at existing range boundaries) have become useful tools for making broad-scale predic-tions about how climate change is likely to affect spe-cies boundaries (Hampe 2004). However, a number of recent reviews have criticized these methods because: (i) they often extrapolate from current environmen-tal conditions to novel conditions; (ii) they ignore indi-rect 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 accli-matization (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 re-sult, the ‘stationarity’ of these models (i.e. the ability to predict changes in one part of the world from measure-ments made in another part of the world) is a serious is-sue. Alternative approaches base future projections on physiological performance (Chown & Gaston 2008). These mechanistic, or process-based models, are in-herently much more time consuming than statistically-based models, but have been shown to produce different predictions than envelope models (Kearney et al. 2008). By comparing physiological limits made via measure-ments under controlled conditions against future condi-tions 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 ob-served (as opposed to monotonic range shifts [Helmuth et al. 2006a; Burrows et al. 2011]).

Newer approaches have begun to connect biophys-ical 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

about physiological responses to changing environmen-tal conditions using energetics approaches, such as Dy-namic Energy Budget models (Kooijman 2009). For example, Sará et al. (2011) apply this approach to M. galloprovincialis in the Mediterranean; their results sug-gest that while range limitations in the intertidal zone were set by lethal limits at some sites, at others the ab-sence 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 examin-ing large numbers of species. In this regard, model spe-cies such as Mytilus might serve as an excellent focal point because of their economic and ecological impor-tance, and the extensive knowledge compiled about an-imals 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 process-es, 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.

ACKNOWLEDGMENTSThe authors were supported by grants from NASA

(NNX07AF20G) and NSF (OCE-0926581).

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Effects of temperature change on mussel, Mytilus · 2013-04-12 · 008). At the individual level, physiological stress im-posed by one factor may reduce the organism’s resis-tance