Global temperatures are forecast to continue to increase (IPCC, 2018), and climate change has resulted in an increased frequency of extreme weather events. For instance, the frequency, intensity and duration of heatwaves and drought have increased and are expected to continue to do so (Chiang et al., 2021; Marx et al., 2021). Heat acclimation, changes in behaviour and migration are strategies used by some species to manage some of the sustained impact of environmental changes caused by climate change (Perry et al., 2005; Seebacher et al., 2015b; Nagelkerken and Munday, 2016). However, short-term extreme conditions present unavoidable challenges to animal survival. The impact of climate change is also exacerbated by interactions with other anthropogenic drivers such as pollution and artificial light at night (ALAN) (Hölker et al., 2021; Polazzo et al., 2022). These environmentally induced challenges to species' geographical distribution and survival may be underpinned by the impact of extreme weather events and pollution on skeletal muscle function – given the importance of skeletal muscle for animal locomotor performance and in driving fitness-related behaviours, such as escape responses, migration, competition for mates and prey capture (Miles, 2004; Lailvaux and Irschick, 2006; Husak et al., 2008). This Review will summarise the potential impact of anthropogenic effects on animal tissue mechanics to help indicate potential consequences for animal locomotor performance and behaviour. More specifically, in light of the available literature, the Review will focus on evaluating the acute and chronic effects of temperature on the mechanical function of muscle, assessing the impact of dehydration and potential influence of anthropogenic pollutants, and defining areas of future work.
At the outset, we would like to note that the literature, as a whole, has relatively poor coverage of different phylogenetic groups, and invertebrates in particular are undersampled. At the same time, there is considerable variation in muscle function between phylogenetic groups and the way in which muscle responds to environmental impacts. Therefore, given the paucity of data, for the purposes of this Review we have given examples of the effects of temperature and pollutants on vertebrate skeletal muscle without trying to account for phylogeny.
Models using isolated muscle have been integral to developing an understanding of the direct, contractile mode and muscle-specific effects of acute changes in temperature on skeletal muscle mechanics (James et al., 2007). Acute temperature changes have been shown to have profound but consistent effects on muscle function in both ectotherms and endotherms (Lannergren and Westerblad, 1987; Prezant et al., 1990; Rall and Woledge, 1990; Frueh et al., 1994; Altringham and Block, 1997; Ranatunga, 1998; Donley et al., 2007, 2012; James et al., 2012, 2015; Olberding and Deban, 2017). Experimentally, a specific skeletal muscle (or muscles) is isolated, the temperature of the muscle is externally manipulated and its mechanical performance is assessed via quantifying isometric (constant muscle length) function, force–velocity relationship and/or work loop power output (variable muscle length). Isometric studies have been used to evaluate temperature effects on muscle force production and the rate of muscle activation and relaxation. Whilst isometric performance is important for some in vivo actions (e.g. postural control), joint articulation is based on muscle force and power production during shortening. During force–velocity experiments, the muscle is maximally activated and only a discrete force and shortening velocity value are used to calculate power, thereby overestimating the power a muscle can generate when undergoing cyclical length changes (James et al., 1996; Caiozzo, 2002). The work loop technique (Josephson, 1993) is the best available for estimating power during dynamic activities as it can be utilised to more closely simulate the estimated in vivo muscle activity, accounting for the often submaximal activation patterns and length change patterns (James et al., 1996; Caiozzo, 2002).
In both endotherms and ectotherms, peak force, shortening velocity, the speed of activation and relaxation and, as a consequence, mechanical work typically increase with temperature (Fig. 1) (Lannergren and Westerblad, 1987; Prezant et al., 1990; Rall and Woledge, 1990; Frueh et al., 1994; Altringham and Block, 1997; Ranatunga, 1998; Donley et al., 2007, 2012; James et al., 2012, 2015; Olberding and Deban, 2017). The magnitude of improvement in muscle performance reduces with every increment in temperature until maximal performance is achieved; beyond this, performance may be unchanged (James et al., 2015; Tallis et al., 2022), but in a number of cases is reduced (Donley et al., 2007, 2012; Tallis et al., 2022). For ectotherms, maximal muscle performance often occurs at temperatures typical for the natural environment of the species (Altringham and Johnston, 1986; Donley et al., 2007). In endotherms, maximal skeletal muscle performance occurs at around the regulated set point body temperature (James et al., 2015; Tallis et al., 2022). For example, an increase in temperature from 35°C to 40°C reduced isometric force of isolated mouse (Mus musculus) diaphragm (Tallis et al., 2022). Temperatures lower than optimal for maximal performance almost exclusively cause a reduction in muscle performance, but the impact of higher temperatures on different measures of mechanical performance may not be uniform between muscles, which may in part be influenced by regional thermal sensitivity (Angilletta et al., 2010; James et al., 2015; Rummel et al., 2021; Tallis et al., 2022). For instance, in bat (Carollia perspicillata) wing muscle, contractile properties of the pectoralis muscle were more temperature sensitive than those of more distal wing muscle (Rummel et al., 2021), which would experience greater thermal fluctuations.
Fig. 1.
The effect of temperature on the contractile function of isolated skeletal muscle. (A) The effect of increasing temperature (15°C, blue; 24°C, green; and 30°C, orange) on maximal isometric tetanus force of Xenopus tropicalis iliotibialis muscle (reproduced from James et al., 2012). (B,C) The impact of temperature on isometric tetanus activation (B) and relaxation time (C) of mouse (Mus musculus) soleus in a control diet-fed (circles) and high-fat diet-fed group (squares) (reproduced from Tallis et al., 2022). (D) The effect of temperature on the work loop power output cycle frequency relationship of muscle isolated from bonito (Sarda chiliensis) (reproduced from Altringham and Block, 1997).
Fig. 1.
The effect of temperature on the contractile function of isolated skeletal muscle. (A) The effect of increasing temperature (15°C, blue; 24°C, green; and 30°C, orange) on maximal isometric tetanus force of Xenopus tropicalis iliotibialis muscle (reproduced from James et al., 2012). (B,C) The impact of temperature on isometric tetanus activation (B) and relaxation time (C) of mouse (Mus musculus) soleus in a control diet-fed (circles) and high-fat diet-fed group (squares) (reproduced from Tallis et al., 2022). (D) The effect of temperature on the work loop power output cycle frequency relationship of muscle isolated from bonito (Sarda chiliensis) (reproduced from Altringham and Block, 1997).
Constraints to biochemical systems account for temperature-specific changes in contractile performance, where optimal temperature evokes rapid reaction kinetics and enzymatic stability (Rummel et al., 2021), influencing cross-bridge events and increasing force generation. Whilst an increased temperature may not increase the number of actin–myosin cross-bridges, higher temperatures have been shown to increase the number of cross-bridges in a high force-producing state (Bershitsky and Tsaturyan, 2002; Decostre et al., 2005; Colombini et al., 2008; Ranatunga, 2018). Furthermore, temperature influences Ca2+ sensitivity (Stephenson and Williams, 1985), the spread of the myofilament lattice altering the gap between the myosin and actin filaments (MacIntosh, 2003), myofibrillar ATPase activity and the rate at which parvalbumin binds to calcium (Bárány, 1967; Stein et al., 1982; Hou et al., 1992). Additionally, myosin ADP release and ATP-induced actin–myosin dissociation can be sensitive to temperature (Ranatunga, 2018). Collectively, these mechanisms account for the influence of temperature on skeletal muscle force production, speed of activation and relaxation, shortening velocity, and work output during cyclical length changes. Such submaximal muscle function brought about by fluctuations in temperature is likely to influence animal locomotor function and behaviour.
Temperature influences how behaviours are performed and whether a behaviour is expressed (Abram et al., 2017). More specifically, temperature affects locomotion (Lehmann, 1999; Dillon and Frazier, 2006), foraging behaviours (Edwards et al., 2015), reproduction (Conrad et al., 2017), predator–prey interactions (Allan et al., 2015), and time in refuge and time to resume activity following predation threats (Brodie and Russell, 1999; Biro et al., 2010). Whilst there is evidence to suggest that temperature-specific behaviours rely on skeletal muscle function (Herrel et al., 2007; Seebacher et al., 2015a), studies that have evaluated the direct link between temperature-specific skeletal muscle mechanical function and whole-animal performance are sparse. Of note, Herrel et al. (2007) demonstrated that fight or flight responses of an agamid lizard (Trapelus pallida) were probably influenced by regional thermal sensitivity of skeletal muscle function. Isometric force of isolated jaw muscle, important for biting, was relatively constant when assessed between 20°C and 40°C; however, both isometric force and work loop power of caudofemoralis muscle, a limb muscle activated during sprinting, decreased at lower test temperatures. These results at least partly explain why lizards flee predation risk at higher temperatures but act aggressively, rather than flee, at lower temperatures (Hertz et al., 1982; Crowley and Pietruszka, 1983; Mautz et al., 1992).
High temperatures may also bring about water deprivation as a result of increased loss through thermoregulatory processes (Sawka et al., 2001) and exacerbate the effects of reduced availability (i.e. anthropogenic impacts on global drought frequency, duration and intensity; Chiang et al., 2021). The effects of temperature on skeletal muscle mechanical function may thereby be compounded by the effects of low water availability, and at its most extreme, dehydration. Data from dehydrated Wistar rats (Rattus norvegicus domestica) show that water loss primarily occurs in the skin and muscle (Nose et al., 1983), affecting metabolic and mechanical function (Lorenzo et al., 2019). Muscle glycogen storage and the function of insulin are influenced by water content (Lorenzo et al., 2019), and consequential effects on ATP generation would impact mechanical function. Muscle dehydration has also been suggested to impact processes important for myogenesis and excitation–contraction coupling (Lorenzo et al., 2019; Cleary et al., 2006). Water deprivation for 96 h reduced isometric function of rat extensor digitorum longus (EDL), but increased isometric function of the soleus (Farhat et al., 2018). Fast twitch muscle (EDL) has greater aquaporin-4 (AQP4) expression, resulting in hyperosmolality which, as a result, affects fibre cross-sectional area and lattice spacing. Whilst the current lack of evidence emphasises a need for further investigation of these effects among different animal species, a reduction in the mechanical performance of fast twitch muscle may further limit behaviours reliant on rapid high-force production. It should also be recognised that the effects of water deprivation are species specific. For example, in amphibians, isometric force of muscle isolated from Scaphiopus couchii, a dehydration-tolerant species, was maintained at lower tissue water content than that from Rana pipiens (Hillman, 1982), which corresponds with evidence showing a water deprivation-induced reduction in jumping performance in some amphibian species (e.g. Bufo americanus; Preest and Pough, 1989), but not in others that are routinely exposed to more arid environments (e.g. Rhinella granulosa; Prates et al., 2013).
In ectotherms and endotherms, tendons are subjected to variable environmental temperatures in a similar way to muscle (Wilson and Goodship, 1994; Yamasaki et al., 2001). Tendons have important roles in transferring force generated via muscle actions to their points of attachment, protecting muscle fibres from damage, storage and return of potential energy, and in optimising muscle shortening velocity to maximise force production (Magnusson et al., 2008). Therefore, effects of temperature on the mechanical function of tendons would substantially influence the operation of the muscle–tendon unit, and thus contribute to effects on animal locomotor performance and behaviour. Studies of mammalian tendon indicate limited effects of temperature on elastic modulus (Rigby et al., 1959; Wang et al., 1991). In bovine tail tendon, increasing the temperature from 24°C to 37°C had little effect on ultimate stress, toughness or elastic modulus. However, yield stress (the threshold for plastic deformation, i.e. initiation of damage) was increased at the higher temperature. In red-necked wallaby (Macropus rufogriseus) tail tendon, time to rupture at a fixed load was reduced when temperature was increased from 20°C to 40°C (Wang and Ker, 1995). Mechanisms underpinning increased overload-induced damage at higher ambient temperatures are yet to be thoroughly explored. Tendon fibroblasts may be resistant to hyperthermia, but repeated exposure to high temperature can compromise cell metabolism of tendon matrix components, resulting in tendon degradation (Birch et al., 1997; KarisAllen and Veres, 2020). Further work is needed to advance the understanding of temperature effects on tendon mechanics across in vivo temperature ranges, but current evidence indicates that the impact of temperature on skeletal muscle may be compounded by a temperature-induced increased susceptibility to tendon damage, preventing maximal mechanical performance of the muscle–tendon unit.
The direct impact of water deprivation on tendon mechanical performance is yet to be investigated. However, should results from previous studies examining dehydration effects on collagen fibrils (Bigi et al., 1987; Turunen et al., 2017; Wells et al., 2017; Haverkamp et al., 2022) translate to water deprivation effects seen in vivo, then muscle–tendon unit mechanical performance could be substantially impaired.
Prolonged shifts in environmental temperature cause many species to undergo physiological changes that can lead to beneficial alterations in the thermal sensitivity of muscle performance (Johnston and Temple, 2002; Seebacher, 2005; Angilletta, 2009). Seasonal thermal acclimation of skeletal muscle occurs in some species of fish, reptiles and amphibians, with many examples of underlying biochemical and molecular changes (Johnston and Temple, 2002; Seebacher, 2005; Angilletta, 2009). Seasonal thermal acclimation can alter the thermal sensitivity of ‘red’ and ‘white’ skeletal muscle performance to optimise power output at different seasonal temperatures. However, there is a wide range of responses to such chronic temperature changes. For instance, cold-acclimated red muscle from Arctic char, Salvelinus alpinus, produced higher work loop power output than warm-acclimated muscle at cold temperatures (Gamperl and Syme, 2021) (Fig. 2). In Atlantic Salmon, Salmo salar (Hittle et al., 2021), and rainbow smelt, Osmerus mordax (Woytanowski and Coughlin, 2013), there was significantly greater work loop power output of white muscle in 5°C-acclimated fish versus 20°C-acclimated fish when both were tested at 10°C. In some fish species, skeletal muscle (red muscle from cunner, T. adspersus: Moran et al., 2020; white muscle from short-horn sculpin, Myoxocephalus scorpius: Johnson and Johnston, 1991; Temple et al., 2000) from warm-acclimated fish produced higher work loop power output at higher environmental temperatures compared with muscle from cold-acclimated fish; however, at colder environmental temperatures, acclimation treatment had no effect on muscle power output. In contrast, red lateral line muscle from S. salar (Gamperl and Syme, 2021; Hittle et al., 2021) (Fig. 2), O. mordax and rainbow trout, Oncorhynchus mykiss (Shuman and Coughlin, 2018), and red abductor superficialis muscle from tautog, Tautoga onitis (Moran et al., 2020) demonstrate limited or no ability to acclimate muscle (work loop) power output across a range of realistic environmental test temperatures. In some species, individuals acclimated to one temperature demonstrate muscle performance surpassing that of individuals in other acclimation treatments across the whole of their seasonal temperature range. For instance, cold-acclimated caudofemoralis skeletal muscle from estuarine crocodiles, Crocodylus porosus, produced higher work loop power output at warm and cold acclimation temperatures, indicative of summer and winter, than did warm-acclimated muscle (Seebacher and James, 2008); cold-acclimated red muscle from scup, Stenotomus chrysops, subjected to in vivo operating conditions produced higher power output at cold acclimation temperatures than did warm-acclimated muscle (Swank and Rome, 2001).
Fig. 2.
Net power produced by red skeletal muscle from 6°C- and 15°C-acclimated Arctic char and Atlantic salmon at a range of test temperatures. Power is expressed relative to muscle mass of each preparation. The key shows the species and acclimation state (char: 6°C acclimated N=7, 15°C acclimated N=8; salmon: 6°C acclimated N=7, 15°C acclimated N=8). Values are means+s.e.m for char and means for salmon (figure produced from data in table 3 of Gamperl and Syme, 2021). There was a significant effect of acclimation temperature on net power output for char at 2, 6 and 15°C test temperatures.
Fig. 2.
Net power produced by red skeletal muscle from 6°C- and 15°C-acclimated Arctic char and Atlantic salmon at a range of test temperatures. Power is expressed relative to muscle mass of each preparation. The key shows the species and acclimation state (char: 6°C acclimated N=7, 15°C acclimated N=8; salmon: 6°C acclimated N=7, 15°C acclimated N=8). Values are means+s.e.m for char and means for salmon (figure produced from data in table 3 of Gamperl and Syme, 2021). There was a significant effect of acclimation temperature on net power output for char at 2, 6 and 15°C test temperatures.
Whilst thermal acclimation effects have been found to occur in skeletal muscle of many fish, the reverse is true for amphibians. Only the aquatic African clawed frog, Xenopus laevis, has been found to acclimate in terms of locomotor performance and lower-level muscle mechanics traits (isometric properties, as no work loop tests were undertaken) of those species tested (Wilson et al., 2000).
In comparison to work on skeletal muscle, fewer studies have investigated the long-term effects of environmental temperature on cardiac muscle. In fish, there was no difference in work loop power output between cold-acclimated and warm-acclimated cardiac muscle across the whole environmental temperature range in S. alpinus or in S. salar (Gamperl and Syme, 2021).
The studies reviewed indicate that some species, particularly of fish, have the capacity to acclimate their skeletal muscle mechanical properties in response to chronic temperature changes. However, many species seem unable to acclimate, such that climate change could shift environmental temperatures to a point whereby skeletal muscle performance is unlikely to be optimal for key fitness-related behaviours; this could underpin shifts in species ranges.
Many species avoid the effects of extreme climatic conditions, often coupled with reduced food availability, by undergoing periods of months or years of torpor/dormancy (e.g. hibernation or aestivation) involving dramatically reduced metabolism and a multitude of biochemical and molecular changes (Ingelson-Filpula and Storey, 2021; Staples et al., 2022). The effects of periods of dormancy on skeletal muscle mechanics and locomotion have not been extensively studied, yet they present real challenges to individuals in terms of avoiding muscle atrophy and physiological changes that could greatly impact subsequent performance in behaviours related to fitness, such as movement towards and acquisition of a mate and escape from predation (Cotton, 2016; Reilly and Franklin, 2016). What is less clear is the likely effect of the alteration of dormancy duration on subsequent performance and survival of individuals, due to the influence of climate change on the duration of extreme weather events, such as freezing temperatures or drought.
The only study on the effects of aestivation on work loop muscle power output suggested that 9 months of aestivation in the green-striped burrowing frog, Cyclorana alboguttata, caused limited changes in the maximal power output or fatigue resistance of isolated iliofibularis and sartorius muscles (Symonds et al., 2007). These results are in keeping with previous findings that 3 months of aestivation did not significantly alter isometric force production of gastrocnemius muscle or burst swimming performance in this species (Hudson and Franklin, 2002).
Similarly, maximal work loop power output of muscle was unaffected by 3 or 4 months of hibernation in either sartorius muscle of the common frog, Rana temporaria (West et al., 2006) (Fig. 3), or soleus muscle from thirteen-lined ground squirrel, Ictidomys tridecemlineatus, although fatigue resistance was reduced in the latter (James et al., 2013).
Fig. 3.
Effect of dormancy on maximal work loop power output. Power–cycle frequency relationships (means±s.e.m.) at 4°C for sartorius (A) and external oblique muscles (B) taken from (4°C) air-access control frogs, normoxic cold-submerged frogs (12–16 weeks in air-equilibrated water) and hypoxic cold-submerged frogs (12–16 weeks in 60 mmHg O2) (reproduced from West et al., 2006). A general linear model was used to test for changes in power with cycle frequency and treatment, considering power as the dependent variable and frequency and treatment as independent variables. Power was significantly affected by cycle frequency but there was no significant effect of treatment (frequency F6,40=7.208, P<0.001; treatment F2,40=1.381, P=0.265).
Fig. 3.
Effect of dormancy on maximal work loop power output. Power–cycle frequency relationships (means±s.e.m.) at 4°C for sartorius (A) and external oblique muscles (B) taken from (4°C) air-access control frogs, normoxic cold-submerged frogs (12–16 weeks in air-equilibrated water) and hypoxic cold-submerged frogs (12–16 weeks in 60 mmHg O2) (reproduced from West et al., 2006). A general linear model was used to test for changes in power with cycle frequency and treatment, considering power as the dependent variable and frequency and treatment as independent variables. Power was significantly affected by cycle frequency but there was no significant effect of treatment (frequency F6,40=7.208, P<0.001; treatment F2,40=1.381, P=0.265).
There is some limited evidence, from isometric studies on isolated muscle preparations, that the mechanical properties of cardiac muscle change in preparation for winter torpor bouts. Maximum isometric force was more thermally sensitive in papillary muscle preparations from ground squirrels, Spermophilus undulatus, in torpor when compared with those obtained between torpor bouts or from spring or summer animals (Zakharova et al., 2009). Papillary muscles from S. undulatus coped well with cooling and reheating, enabling them to produce the same isometric force at 30°C before and after cooling to 10°C, whereas papillary muscles from Sprague–Dawley rats produced significantly (∼40%) lower force when reheated after cooling (Nakipova et al., 2017). These studies indicate that ground squirrels undergo physiological changes, including enhancement of store-operated Ca2+ entry (SOCE) through cardiac muscle plasma membrane, to enable them to cope with cycles of hyperthermia and reheating associated with torpor bouts during hibernation (Nakipova et al., 2017).
The evidence presented suggests that some species are able to undergo periods of relative dormancy, such as hibernation or aestivation, with limited effects on muscle mechanics despite the evidence that most species tested, that do not undergo dormancy, exhibit atrophy and decreases in mechanical performance of muscle in response to periods of immobilisation (James, 2010; Reilly and Franklin, 2016). However, climate change is increasing the frequency of extreme weather events and will probably alter the duration of inhospitable climates in a way that could extend required dormancy periods beyond durations for which individuals are able to maintain subsequent performance and/or sufficient stored energy reserves to survive (van Beurden, 1980).
Variability is an intrinsic characteristic of most environments and has acted as a selection pressure shaping phenotypes and their plasticity over evolutionary time (Boonekamp et al., 2018; Brass et al., 2021). Temperature variation is particularly pronounced and many animals show plastic responses to compensate for fluctuations in temperature at different time scales to maintain performance despite the potentially negative effects of temperature change (Seebacher et al., 2015b; Rohr et al., 2018). However, the ‘modern’ world is different from conditions most animal species have evolved under. Human activity has now introduced new environmental drivers that can impact most biological functions. In addition to climate change, chemical pollution and ALAN are two of the most pervasive anthropogenic environmental drivers that affect ecosystems worldwide (Borrelle et al., 2020; Sanders et al., 2020). Importantly, both chemical pollution and ALAN can interact with ‘natural’ drivers such as temperature fluctuation to elicit phenotypic responses (Bradshaw and Holzapfel, 2010; Maulvault et al., 2019; Polazzo et al., 2022). These interactions are likely to be novel and existing knowledge is insufficient to predict how animals will respond to variation in temperature when anthropogenic chemicals or ALAN are present (Seebacher, 2022). Interactions between environmental variables – anthropogenic or natural – can affect a broad range of biological functions (Halfwerk and Slabbekoorn, 2015; Dominoni et al., 2021). For example, in intertidal snails (Nerita atramentosa), wave action and temperature interacted in their effect on isolated foot muscle tenacity and endurance. Increased wave action elicited a positive tenacity training effect on muscle, but increasing temperature caused a trade-off between tenacity and endurance (Clayman and Seebacher, 2019). Interactions and consequent trade-offs would prevent animals from ‘tuning’ to novel environmental conditions such as those caused by climate change, which is predicted to increase temperature and wave action (Clayman and Seebacher, 2019). Similarly, climate change often causes decreases in aquatic dissolved oxygen levels as a result of decreased aquatic oxygen solubility at higher temperatures and eutrophication (Hale et al., 2016). Temperature and hypoxia may therefore interact in their effects on muscle contractile function; hypoxia was found to increase twitch duration and reduce power output in myocardial strips from O. mykiss (Carnevale et al., 2021).
Temperature may also affect the impact of chemical pollutants, although the possible effects of that interaction on muscle contractile performance have not been quantified. Nonetheless, chemical pollution and temperature interact to modify locomotor performance (Little and Seebacher, 2015; Wu and Seebacher, 2021) and endocrine signalling (Seebacher, 2022), which makes it likely that muscle contractile performance is also affected. However, to date, the literature has focused mainly on single stressor impacts on isometric force production in cardiac and skeletal muscle.
留言 (0)