Can animals tune tissue mechanics in response to changing environments caused by anthropogenic impacts?

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.

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.

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). Environmental temperature variation is particularly pronounced, and many animals show plastic responses to compensate for fluctuations in temperature over different time scales to maintain performance despite the potentially negative effects of temperature change (Rohr et al., 2018; Seebacher et al., 2015b). However, some species avoid extreme climatic conditions, such as extreme temperature and/or drought, via behavioural changes, including migration, or by undergoing periods of relative dormancy (such as hibernation or aestivation; Ingelson-Filpula and Storey, 2021; Staples et al., 2022). A few species, such as largemouth bass, Micropterus salmoides, and cunner, Tautogolabrus adspersus, use a combination of these approaches, utilising phenotypic plasticity until specific environmental conditions are reached, at which point they enter dormancy. The following sub-sections will review the chronic effects of environmental temperature on animal tissue mechanics; for muscle tissue, the focus will be on evidence provided by work loop data to better indicate the likely effects on locomotor performance.

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).

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).

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.

Chemical pollution, in particular, can affect muscle contractile performance either directly, such as by disrupting calcium (Ca²⁺) signalling at various points, or by altering hormone signalling. Additionally, hormones, particularly thyroid hormone, can affect muscle function by regulating proteins such as sarco/endoplasmic reticulum Ca²⁺-ATPase (SERCA) (Simonides and van Hardeveld, 2008). Disruption of Ca²⁺ signalling can have severe ecological and health consequences, and understanding the impact of such disruption becomes more difficult if different environmental signals interact. Below, we provide a brief summary of studies on different anthropogenic chemicals and light that can act as Ca²⁺ and endocrine disruptors and thereby affect muscle contractile function.

Acetylcholinesterase (AChE) breaks down acetylcholine at the neuromuscular junction. Disruption of AChE leads to accumulation of acetylcholine and a prolonged neural signal resulting in elevated Ca²⁺ concentrations in the myocyte (Tintignac et al., 2015). Consequently, the excitation–contraction–relaxation cycle is disrupted, leading to altered muscle contractile performance (Tintignac et al., 2015). For example, the organophosphate insecticide chlorpyrifos (at up to 5 mg kg⁻¹ body mass), which inhibits AChE, increased twitch stress as well as contraction and relaxation times, and fatigability in rat diaphragm muscle after 6 weeks of dietary supplementation (Sabbouri et al., 2022). These results are consistent with prolonged muscle contraction resulting from an elevation of cytoplasmic free Ca²⁺ as a consequence of AChE inhibition. Organophosphates may be found at a concentration of nanograms to milligrams per litre in aquatic environments (Boettger and McClintock, 2012; Wee and Aris, 2017), and the relevance of findings from laboratory studies using rats and mice to aquatic vertebrates and invertebrates remains to be demonstrated. Organic phosphates from organophosphate insecticides (in the milligram per litre range) reduced AChE activity and force production and slowed contraction and relaxation times in case studies utilising muscle associated with Aristotle's lantern in the sea urchin Lytechinus variegatus (Boettger and McClintock, 2012), and in the auricle of sea bream, Sparus aurata (Tryfonos et al., 2009), respectively. These data indicate that organophosphates disrupt contractile function across species although their specific effects differ between species. AChE inhibition may not be the only mechanism responsible because it is expected to lead to increased cytosolic Ca²⁺ and increased force, rather than the decrease observed in sea bream and sea urchins. Experimental research is needed to resolve these differences and to place them into a broader ecological framework of variation in other environmental factors such as temperature, and to assess their effects on whole-animal performance such as locomotion across a more representative sample of species.

Exposure of bullfrog, Lithobates catesbeianus, tadpoles to 17a-ethinylestradiol (EE2) at environmentally relevant concentrations (10 ng l⁻¹ for 96 h) induced tachycardia and increased isometric force of isolated ventricle strips across a range of stimulation frequencies (Salla et al., 2016). EE2 is an artificial agonist of oestrogen receptors that is most commonly used in birth control pills and hormone-replacement therapy, and which is commonly found in surface waters. Its effect on the heart is mediated by a PKA-dependent increase in Ca²⁺ release (Salla et al., 2016). The surfactant alkylbenzene sulfonate reduced activity and heart rates in L. catesbeianus tadpoles after 96 h exposure within legal environmental concentrations (0.5 mg l⁻¹) in Brazil (Jones-Costa et al., 2018). However, relative ventricular size, isometric force and speed of contraction of isolated ventricular strips increased, but not speed of relaxation (Jones-Costa et al., 2018). The polycyclic aromatic hydrocarbon phenanthrene, which is used in the manufacture of products ranging from plastics to pesticides, reduced isometric force generation of isolated ventricular and atrial strips by lowering myocyte Ca²⁺ transients in brown trout, Salmo trutta (Ainerua et al., 2020). EE2, alkylbenzene sulfonate and phenenthrene disrupted inotropic responses of the heart, but their effects were qualitatively different and possibly species specific, although more work is needed to resolve these trends. The link between contractile function of ventricular strips and responses to environmental variation is, as yet, tenuous. It is possible that pollutant-induced changes to heart muscle constrain cardiovascular function so that acute and plastic responses to environmental change are also altered, but this relationship would need to be tested experimentally.

Polychlorinated biphenyls (PCBs) were commonly used in various industries but have now been banned in many countries. However, PCBs are stable and remain in the environment, and are therefore still present almost ubiquitously in air, water, soil and animal tissues (Niknam et al., 2013), and also bioaccumulate so that internal concentrations can be higher than those of the environment (Berninger and Tillitt, 2018). PCBs disrupt Ca²⁺ homeostasis, at least partly, by interacting with ryanodine receptors (RyRs) and Ca²⁺ channels, and can thereby interfere with muscle excitation–contraction coupling (Niknam et al., 2013; Rebuzzini et al., 2018). Environmental concentrations may vary considerably between sites, depending on their history of human activity (Vanavermaete et al., 2023). Levels of PCBs (∼0–10 µmol l⁻¹) found in fish, human serum and sediments were within the range that was sufficient to interfere with RyRs (Pessah et al., 2010). Tissue concentrations in fish can also vary significantly, but lowest observed adverse tissue concentrations indicate that PCBs are likely to have an effect on reproduction, growth and survival (Berninger and Tillitt, 2018), although their effect on muscle contractile function remains to be demonstrated for fish. In a case study showing an in-principle effect of PCB on contractile function, relatively high concentrations of PCB19 (30 µmol l⁻¹) decreased contractile force in a dose-dependent manner and decreased Ca²⁺ transients by inhibiting L-type Ca²⁺ channels in guineapig, Cavia porcellus, ventricular myocytes (Jo et al., 2001).

In skeletal muscle, arsenic exposure increased crayfish, Cherax destructor, chelae skinned muscle fibre isometric force after 40 days of exposure. Increased force was associated with increased Ca²⁺ sensitivity so that lower Ca²⁺ transients were needed to achieve a given force output. However, arsenic reduced myosin heavy chain (MHC) and tropomyosin content of muscle (Williams et al., 2014). Arsenic washes into rivers from gold mining operations, and it accumulates in crayfish tissues, which may lead to relatively long-term effects, even from transient exposure. Similarly, the heavy metal cadmium occurs naturally but human activities such as mining lead to increases in environmental concentrations, which can impact muscle function. Intake of cadmium occurs mainly via food, and it also bioaccumulates so that its effects can be amplified along the food chain (Elinder, 1992). For example, blood concentrations of human populations in Sweden were typically up to 10 mmol l⁻¹ with extreme values up to 50 mmol l⁻¹, which is within a range causing health problems (Järup and Akesson, 2009). Cadmium selectively blocks sarcolemmal L-type Ca²⁺ channels and Na⁺/Ca²⁺ exchangers in cardiac myocytes and can thereby compromise cardiac contractility (Prozialeck et al., 2006; Dal-Medico et al., 2014). Lithobates catesbeianus tadpoles exposed to environmental cadmium concentrations that are considered safe in Brazil (1 µg l⁻¹, 5 nmol l⁻¹) showed bradycardia and incomplete cardiac relaxation but no effects on isometric twitch force in isolated ventricular strips after 2 days of exposure. However, after 16 days of exposure, twitch force declined and there was a reduction in contraction velocity (Dal-Medico et al., 2014). Other metal ions can also impact Ca²⁺ signalling and contractile function. Mercury, which is often associated with mining and timber industries, also bioaccumulates (Lavoie et al., 2013) and can impact muscle function of aquatic organisms. Around contaminated sites, aquatic mercury levels can be high (e.g. 0.23 mg l⁻¹ around an industrial site in Germany) (Bollen et al., 2008). Exposure to aquatic concentrations of 0.1 mg l⁻¹ for 96 h, or dietary exposure (∼0.1 mg day⁻¹ for 30 days) decreased isometric twitch force of isolated ventricular strips in the freshwater fish Brycon amazonicus and Hoplias malabaricus and decreased rates of contraction and relaxation as a result of disrupted intracellular Ca²⁺ cycling (Monteiro et al., 2017).

Silver nanoparticles (nAg) are commonly used in medical applications and in the manufacture of consumer goods, because of their antibacterial and antifungal properties (Vance et al., 2015). Unlike ionic silver (Ag⁺), nAg can cross the epithelium and bioaccumulate, and their increasing commercial use also makes environmental contamination more likely, with environmental concentrations in the micromolar range being reported (Yu et al., 2013). In rainbow trout, O. mykiss, and killifish, Fundulus heteroclitus, exposure to high concentrations of nAg (up to 15 mg l⁻¹) resulted in decreased twitch force and slower contraction and relaxation rates of isolated ventricle strips (Callaghan et al., 2018). Because of the high concentrations used, these results are more relevant for topical applications of nAg in antibacterial products, for example, than reflecting impacts of environmental pollution. Copper sulphate (CuSO₄), a fungicide and algicide commonly used in aquaculture and agriculture, contributes to environmental copper concentrations of up to 20 mg l⁻¹ in aquatic ecosystems (Waldemarin et al., 2012). CuSO₄ (1 mg l⁻¹) caused similar effects to other metal ions and decreased twitch force and increased contraction and relaxation times in cardiomyocytes of tilapia, Oreochromis niloticus (Waldemarin et al., 2012). Together, these data indicate that environmental metal exposure has a negative effect on cardiac muscle, and may thereby constrain cardiovascular adjustment in response to increased metabolic demand during movement and with increasing temperature. Data in the literature are limited taxonomically, and differences in muscle structure and function, particularly between vertebrates and invertebrates, could alter the impact of pollutants and need further investigation.

The manufacture of plastics releases a massive amount of bioactive chemicals into the environment, either as direct effluents from manufacture or from the breakdown of discarded plastics (Tarafdar et al., 2022). Bisphenol A (BPA), used in the manufacture of polycarbonate plastics, is one of the most highly produced and ubiquitous chemicals and can be found at concentrations in the nanomolar to micromolar range in aquatic environments around the world (Tarafdar et al., 2022). BPA and other bisphenols are best known for their endocrine-disrupting effects (Rubin, 2011; Rubin and Seebacher, 2022). However, BPA can also disrupt neurophysiology, and in isolated rat hearts it altered (at micromolar concentrations) Ca²⁺ transients and reduced ventricular pressure and contractility in a dose-dependent manner (Posnack et al., 2015). BPA and its derivative tetrabromobisphenol A (TBBPA) (at concentrations of up to 30 µmol l⁻¹) disrupted Ca²⁺ handling and thereby the function of isolated rodent skeletal myotubes, albeit by different mechanisms. TBBPA activated RyRs but inhibited dihydropyridine receptors and SERCA; BPA had little effect on these proteins but altered cell excitability and thereby Ca²⁺ transients (Zhang and Pessah, 2017). These data are relevant as an in-principle demonstration that environmental concentrations of BPA can interfere with muscle contractile function, although experimental studies are needed to test these effects in wildlife, and their ecological relevance.

In addition to direct impacts on calcium transients, chemical pollutants can interfere with hormone signalling. So-called endocrine-disrupting compounds (EDCs), such as bisphenols associated with plastic waste and manufacture, can act as agonists or antagonists for nuclear receptors, including thyroid (Moriyama et al., 2002; Lu et al., 2018; Zhang et al., 2018; Kupprat et al., 2021) and glucocorticoid signalling (Zhang et al., 2019; Dominoni et al., 2021). Their action can therefore stimulate or block hormone signals, and EDCs can also impact the transcription of hormone receptors (Gore et al., 2015). Similarly, ALAN can disrupt hormone signalling (Russart and Nelson, 2018). However, data showing a mechanistic link between endocrine disruption, muscle contractile function and ecologically relevant performance are rare, although known interactions strongly suggest that such links exist.

Glucocorticoids have a broad range of functions in mediating metabolism and behaviour in response to environmental inputs (Taff and Vitousek, 2016; de Bruijn and Romero, 2018; Schoenle et al., 2021), although any direct effect on muscle contractile function is less clear. Supplementation with glucocorticoid-based medication increased isolated mouse skeletal muscle isometric force in the short term (minutes) (Pérez et al., 2013), but longer-term administration of glucocorticoids may cause glucocorticoid myopathy, partly by increased break-down of muscle proteins (Pereira and de Carvalho, 2011).

Thyroid hormone (TH) is particularly susceptible to endocrine disruption (Beg and Sheikh, 2020; Zhang et al., 2017), and it also plays an important role in determining muscle function. It is likely, therefore, that disrupted TH signalling will also affect muscle contractile function (Little and Seebacher, 2013). At least in mammals, TH regulates gene expression of a range of muscle-specific proteins, including SERCA isoforms, with the overall effect of mediating a shift toward the fast muscle phenotype (Simonides and van Hardeveld, 2008; Salvatore et al., 2014). In agreement with a shift towards fast muscle, TH induces myoblast determination protein 1 (MyoD1), which is an upstream signalling protein of the fast muscle phenotype (Salvatore et al., 2014). In parallel, TH represses calcineurin and its downstream transcription factors that mediate slow muscle phenotypes. However, TH also promotes the peroxisome proliferator activated receptor co-activator gamma 1 alpha (PGC1a), which acts to increase mitochondrial capacity. The overall effect of TH on muscle function is therefore a shift to fast contractility accompanied by an increase in glycolytic and oxidative capacity (Salvatore et al., 2014). In zebrafish, hypothyroidism reduced swimming performance, SERCA activity, and mRNA levels of SERCA1 and fast myosin heavy chain isoforms (Little and Seebacher, 2013). Similarly, swimming performance and isolated skeletal muscle force production, but not fatigue resistance, were reduced in hypothyroid carp, Cyprinus carpio; however, these effects did not seem to be mediated by decreased SERCA activity (James et al., 2016). However, there is evidence that TH treatment in young rainbow trout can shift red muscle to slower contractile properties and reduce tailbeat frequency during swimming (Coughlin et al., 2001). Exposure to bisphenols paralleled effects of TH on locomotor performance and also disrupted thermal acclimation of locomotor performance in zebrafish (Wu and Seebacher, 2021). BPA exposure also altered SERCA activity in a temperature- and concentration-dependent manner in zebrafish (Little and Seebacher, 2015). In cardiac muscle, BPA increased activity at a lower, environmentally relevant concentration (20 µg l⁻¹) but decreased it at a higher concentration (500 µg l⁻¹) regardless of acute test or long-term acclimation temperatures. In contrast, in skeletal muscle, BPA decreased SERCA activity regardless of concentration and acute test temperature but only in fish acclimated to lower (18°C) temperatures; however, a direct link to endocrine signalling was not established (Little and Seebacher, 2015). Even though the causal link between bisphenol exposure, thyroid hormone signalling and muscle contractile function has not been established, the data briefly summarised above indicate that it is likely that these are linked and together alter the tuning of muscle function to environmental change. Worryingly, EDCs, ALAN and human-caused noise and heat can interact to modify hormone signalling. Although experimental evidence is sparse, these interactions are likely to produce novel and unpredictable effects (Seebacher, 2022). In future work, the effects of climate change on muscle function should be assessed in a multi-stressor context, because it will be rare for climate change to act in isolation from other pollutants.

Findings from studies investigating the effects of chronic temperature change on muscle mechanics indicate a wide variety of responses between species, and many species that do not respond. The consequences of impaired skeletal muscle contractile function would primarily lie in curtailing ecologically important locomotor activities such as dispersal and migration, foraging and behavioural interactions (Seebacher et al., 2015a; James and Tallis, 2019). The consequences of altered cardiac muscle contractile performance – either increased or decreased – are a disruption of co-ordination in excitation–contraction–relaxation coupling. Disruptions may result in a mismatch between cellular demand and supply by the cardiovascular system of oxygen and nutrients, which can decrease the overall health and fitness of the organism. An important future research direction would be testing the potential link between environmentally induced changes in contractile function and ecologically relevant responses such as the effects of limited cardiac scope on migration or thermal tolerance (Pörtner and Knust, 2007; Eliason et al., 2011). Even those species that are currently able to avoid some current extreme climates, e.g. via hibernation or aestivation, may be adversely affected by climate change as it could alter the duration of dormancy required; in turn, the viability of dormancy could be limited by energy stores in the body and increased variability in the occurrence of extreme climatic conditions may make it more difficult for animals to determine changes in season to cue the physiological alterations needed for successful re-emergence from dormancy.

Further studies are needed to determine the acute and chronic effects of temperature on the mechanical properties of animal tissues other than skeletal and cardiac muscle. For instance, fish rearing temperature affects the timing and development of bone and cartilage, which may impact swimming performance (Ackerly and Ward, 2016; di Santo, 2019; Campbell et al., 2021), but the impact on tissue mechanics is unclear; temperature effects on bone are limited to very few studies of acute effects (e.g. Ma et al., 2020). Whilst there is reasonable coverage in the literature of the acute effects of temperature on tendon mechanics, there is a lack of understanding of what potential chronic effects might occur, which in turn could affect the function of the muscle–tendon unit. Another challenge in the interpretation of studies considering chronic effects of temperature is the usage of constant acclimation temperature, given that, for some species, daily variation in temperature is significant and may affect acclimation responses (Huey and Buckley, 2022).

Aside from temperature effects, there is a relative dearth of literature systematically investigating the effects of anthropogenic environmental changes on animal tissue mechanics. This is a major area for future work, for instance to ensure that the effects of pollutants at likely environmental concentrations are determined using mechanical tests that simulate the in vivo action of animal tissues. Therefore, there is some evidence, particularly in the thermal acclimation of some fish species, that some animals can tune tissue mechanics in response to changing environments caused by anthropogenic impacts. However, future work needs to determine the direct effects of anthropogenic environmental changes on animal tissues and related changes in locomotor performance and behaviour, accounting for currently unknown interactions between environmental factors such as temperature and pollutants.

We thank the anonymous reviewers of this paper for their constructive and helpful comments.