Metabolic Plasticity Improves Lobster´s Resilience to Ocean Warming but Not to Climate-driven Novel Species Interactions

doi:10.21203/rs.3.rs-829048/v1

Download PDF

Research Article

Metabolic Plasticity Improves Lobster´s Resilience to Ocean Warming but Not to Climate-driven Novel Species Interactions

https://doi.org/10.21203/rs.3.rs-829048/v1

This work is licensed under a CC BY 4.0 License

You are reading this latest preprint version

Marine species not only suffer from direct effects of warming oceans but also indirectly via the emergence of novel species interactions. While metabolic adjustments can be crucial to improve resilience to warming, it is largely unknown if this improves performance relative to novel competitors. We aimed to identify if spiny lobsters – inhabiting a global warming and species re-distribution hotspot - align their metabolic performance to improve resilience to both warming and novel species interactions.

We measured metabolic and escape capacity of two Australian spiny lobsters, resident Jasus edwardsii and the range-shifting Sagmariasus verreauxi, acclimated to current average- (14.0°C), current summer- (17.5°C) and projected future summer- (21.5°C) habitat temperatures.

We found that both species decreased their standard metabolic rate with increased acclimation temperature, while sustaining their scope for aerobic metabolism. However, the resident lobster showed reduced anaerobic escape performance at warmer temperatures and failed to match the metabolic capacity of the range-shifting lobster.

We conclude that although resident spiny lobsters optimise metabolism in response to seasonal and future temperature changes, they may be unable to physiologically outperform their range-shifting competitors. This highlights the critical importance of exploring direct as well as indirect effects of temperature changes to understand climate change impacts.

Scientific Communication

Jasus edwardsii

Sagmariasus verreauxi

spiny lobsters

species re-distribution

thermal acclimation

aerobic scope

metabolism

phenotypic plasticity

By the end of this century our oceans will likely be, on average, 3.5°C warmer relative to 1870-1899, RCP8.5, ¹. Local warming can be even more extreme, due to heat waves ², changing ocean currents ³, or cyclic weather patterns ⁴. Such warming hotspots show rapid change of ecosystems, characterised by altered species abundance, biodiversity decline and local extinctions ^5,6. Species persistence will depend on their ability to acclimate or adapt rapidly ⁷ or alternatively by ´escaping´ to geographically track suitable temperatures poleward ^8-10. As a result, species are now re-distributing globally, particularly in our ocean, where species ranges shift up to six times faster than on land 5.9 vs 1.1 km per year, ^9,11]. However, due to differences in physiological tolerance, species traits, behaviour, habitat availability, adaptive capacity or access to microclimates, species may shift at different rates leading to disassembly of existing communities or emergence of novel biotic interactions ^9,10. Shifting to keep pace with preferred temperatures, or conversely, maintaining presence in an existing part of a specie`s distribution, may be further complicated by changing predation or competition pressures as result of range-shifting species ^12-14. For many species, acclimation or adaptation will increase resilience to these challenges and be key for their survival ⁷.

Niche shifts via physiological adjustments in response to environmental change (i.e. physiological plasticity or acclimation) are a critical and rapid mechanism by individuals to improve resilience to increasing temperatures ^15-17 and reduce extinction risk ⁷. Energy metabolism plays an important role in this context. It powers fundamental processes such as growth, locomotion, or reproduction that require energy in the form of ATP produced either aerobically or anaerobically. Aerobic metabolism is far more efficient (~36 ATP/glucose molecule) and consequently the predominant process in most organisms to power sustained activities ¹⁸. Performance declines due to temperature changes are thus frequently compensated by plastic adjustments of aerobic pathways, characterized by shifts in e.g. metabolic rate ¹⁹ or mitochondrial function ^20,21. On the other hand, anaerobic sources of energy, such as free ATP, muscle phosphocreatine, or ATP derived from glycolysis, ^22,23 are quickly exhausted but can release energy more rapidly. This supports short, strong bursts of activity, and is critical to survival when e.g. escaping from predators ²⁴. Consequently, failure to sustain or adjust both aerobic and anaerobic energy metabolism may not only impair an animal`s performance but directly affect their survival in increasingly warmer waters.

A largely unexplored aspect has been how such metabolic plasticity shapes outcomes of species interactions, particularly between resident and range-shifting species ⁸. Most marine animals are unable to regulate their body temperature (i.e. they are ectothermic) and perform well only within a limited range of temperatures. Temperature, therefore not only limits species´ geographic distribution ²⁵ but also regulates how ectothermic species perform relative to each other, depending on the individual shape and overlap of their thermal windows ²⁶. Physiological plasticity can shift thermal niches and consequently the outcomes of direct interactions, such as competition ²⁷, resulting in the dominance of the resident or the range-shifting species. Given this, it is essential to understand species´ capacity for physiological plasticity to predict their future distributions and outcomes of biotic interactions ⁸.

Lobsters in a warming and range-shift hotspot

Lobsters are key to biodiverse underwater ecosystems, both as prey and predators ²⁸, and improve resilience to climate-driven catastrophic ecosystem shifts, by consuming invasive barren-forming sea urchins ^29,30. At the same time, lobsters are themselves highly vulnerable to climate warming, with local temperatures already exceeding thermal tolerance limits leading to local population declines ^31-33. This has not only consequences for the ecosystems they support but also their supply as a valuable resource to coastal and indigenous communities ^34,35 with a global annual market worth 3.3 billion USD ³⁶.

With at least ten species, Australia hosts a rich diversity of spiny lobsters ³⁷. However, warming threatens this diversity, with lobster distributions predicted to contract by 40-100% ³⁸, particularly in South-East Australia, where waters are heating up 3-4 times faster than the global average ^3,39. This warming trend has led to dozens of species shifts from coastal mainland Australia to the cold-temperate waters of Tasmania ^40-44. Among them is the eastern rock lobster Sagmariasus verreauxi, the world´s largest spiny lobster reaching up to 20 kg and 70 cm total length ^37,45, that has become increasingly abundant in areas previously occupied exclusively by the resident southern rock lobster Jasus edwardsii ⁴¹ (Fig. 1).

Southern rock lobsters cannot evade warming trends due to the lack of coastal habitat further south ³⁹ (Fig. 1) and by 2070 may face up to 21.5°C on average during summer in South-East Tasmania (high emission scenario A1F1 in Pecl et al. 2009 ⁴⁶). These warm temperatures will exceed southern rock lobster thermal optima for growth 20.6°C, ⁴⁷, feed efficiency 19.3°C, ⁴⁷, and metabolic scope 19.6°C, ⁴⁸. Moreover, an increasing number, intensity and duration of heat waves will add up to an extra 2°C of warming ⁴⁹, posing an acute risk to physiological functioning e.g. declining oxygen consumption >22°C, ⁴⁷, declining cellular energy production >25°C, ⁵⁰] and survival of J. edwardsii > 23.3-24°C, ^47,51. Any additional stress by competition such as reduced quantity or quality of diet ⁵², disease ⁵³, loss of shelter ⁵⁴ or increased predation ⁵⁵, may be detrimental to the survival of local populations of J. edwardsii. Yet, if J. edwardsii can dynamically adjust thermal windows of essential processes such as energy metabolism, it may increase resilience to the dual climate-driven pressure of warming and a novel range-shifting competitor.

Although the thermal ecology of J. edwardsii and S. verreauxi has been relatively well studied ^48,50,56], it remains unknown whether metabolic plasticity changes their resilience to warming and the relative performance between the species.

This study aimed to identify if resident and range-shifting, co-occurring spiny lobster species inhabiting an Australian warming hotspot: 1) adjust their metabolism in response to seasonal and forecasted temperature changes and 2) if this leads to a relative shift of metabolic performance between the two species.

Measurements of oxygen consumption rates showed that both spiny lobster species decrease their standard metabolic rate with increasing acclimation temperature while sustaining their scope for aerobic metabolism. However, resident J. edwardsii showed decreased anaerobic escape capacity at 21.5°C acclimation temperature and failed to match the metabolic capacity of the range-shifting lobster. Although, metabolic plasticity aids resident lobsters to cope with direct effects of ocean warming, it does not suffice coping with indirect warming impacts such as novel range-shifting competitors.

Thermal plasticity of aerobic metabolism

Oxygen consumption measurements and exhaustion experiments showed that the resident and the range shifting lobster - inhabiting the same ocean warming hotspot – both decrease their standard metabolic rate with increasing acclimation temperature while sustaining aerobic scope (Fig. 2a-d). Following a minimum eight weeks of thermal acclimation to current average- (14.0°C), current summer- (17.5°C) and future summer- (21.5°C) habitat temperatures, standard metabolic rates were 29% lower in warm-acclimated (21.5°C) J. edwardsii (29.0 mg O₂h^-1 kg^-1 [21.4-36.5] at 21.5°C versus 44.3 mg O₂h^-1 kg^-1 [38.1-50.5] at 14.0°C, n = 6) and 36% lower in warm-acclimated S. verreauxi (30.0 mg O₂h^-1 kg^-1 [25.8-34.2] at 21.5°C versus 45.9mg O₂h^-1 kg^-1 [33.4-58.3] at 14.0°C, n = 6) compared to their cold acclimated (14°C) counterparts at an experimental temperature of 21.5°C (Fig. 2a-b). This was due to a lower thermal increase of standard metabolic rates with increasing experimental temperatures in warm-acclimated lobsters (Table 1). This difference in standard metabolic rate among acclimation groups increased successively from 14°C to 21.5°C experimental temperature (Fig. 2a-b). Unlike standard metabolic rates, which showed a relatively high thermal sensitivity, maximum metabolic rates increased only moderately with experimental temperatures in both species (Table 1) and were more similar among acclimation groups (Fig. 2a-b). Only warm-acclimated (21.5°C) J. edwardsii showed a 10-20% lower maximum metabolic rate compared to the 17.5°C and 14°C acclimation groups at 14°C experimental temperature (Fig. 2a). Interestingly, aerobic scope did not differ among acclimation groups in either of the two species (Fig. 2c-d), except for a minor trend of decreased aerobic scope for warm acclimated J. edwardsii at 14°C (Fig. 2c). Furthermore, thermal sensitivity of aerobic scope was low in both species and among acclimation groups (Table 1). Only warm acclimated S. verreauxi showed an increased aerobic scope from 14°C to 21.5°C experimental temperature (Fig. 2d), largely due to a more pronounced increase in maximum metabolic rate relative to standard metabolic rate (Fig. 2a). Factorial aerobic scope, which expresses the ratio between maximum metabolic rate and standard metabolic rate, generally decreased towards warmer experimental temperatures (ANOVA, F_{(2, 43)} = 42.04, p = 7.548 e^-11). Here, only S. verreauxi showed a significant increase of factorial aerobic scope following warm-acclimation to 21.5°C (6.5, [5.3-7.8], n = 6) compared to conspecifics acclimated to 14.0°C (3.9, [2.9-5.0], n = 6) at 17.5°C experimental temperature (Pairwise comparison, t₍₇₁₎ = -2.48, p = 0.046).

Table 1 Thermal coefficients (Q₁₀) for standard metabolic rate (SMR), maximum metabolic rate (MMR) and aerobic scope in comparison between J. edwardsii and S. verreauxi. Q₁₀ were calculated from data means covering the experimental temperature range from 14.0°C to 21.5°C.
Species	Trait	14.0°C	17.5°C	21.5°C
Jasus edwardsii	SMR	3.3	3.3	2.7
	MMR	1.3	1.2	1.6
	Aerobic scope	0.9	0.9	1.3
Sagmariasus verreauxi	SMR	3.7	3.1	3.2
	MMR	1.4	1.5	1.7
	Aerobic scope	1.0	1.2	1.4

Anaerobic escape performance

In addition to the aerobic component supporting exhaustive exercise in spiny lobsters, we assessed the anaerobic component expressed as excess post-exercise oxygen consumption rate (EPOC), which represents the additional oxygen required to return depleted anaerobic energy stores, pH and lactate levels during recovery back to pre-exercise levels ^57,58. Warm-acclimation to 21.5°C significantly reduced EPOC by 59% in J. edwardsii (156.7 mg O₂ kg^-1 [109.9-203.6], n = 18) compared to lobsters acclimated to 14°C (375.6 mg O₂ kg^-1, [311.1-440.1], n = 18), when averaged across experimental temperatures (Fig. 3a). EPOC decreased similarly by 36% in warm-acclimated S. verreauxi (238.3 mg O₂ kg^-1, [155.5-321.0], n = 18) compared to cold-acclimated conspecifics (398.4 mg O₂ kg^-1, [291.7-505.1], n = 18) but was less pronounced and only significant at 17.5°C experimental temperature (Fig. 3). Recovery time, which represents the time lobsters require to replenish depleted anaerobic energy stores and return to pre-exercise oxygen consumption rates (MO₂), was on average 4.7 and 5 hours shorter in warm-acclimated (21.5°C) J. edwardsii (12.0 hr [10.1-14.0] at 21.5°C versus 7.3 hr [5.2-9.4] at 14.0°C, n = 18) and S. verreauxi (12.4 hr [9.7-15.1] at 21.5°C versus 7.4 hr [5.4-9.4] at 14.0°C, n = 18) respectively compared to cold acclimated (14°C) individuals (ANOVA, F_{(2, 33)} = 9.69, p = 4.904 e^-4, Fig. 3c,d). This was most apparent at an experimental temperature of 21.5°C in both species (Fig. 3c, d). Although there was no significant effect of thermal acclimation on recovery rates (ANOVA, F_{(2, 33)} = 2.7 p = 0.082), warm-acclimated J. edwardsii tended to replenish 32.1% less oxygen per hour than cold acclimated conspecifics (22.0 mg O₂h^-1 kg^-1 [18.3-25.7] at 21.5°C versus 32.4 mg O₂h^-1 kg^-1 [28.1-36.8] at 14.0°C, n = 18), particularly at 14°C experimental temperature.

Further, warm-acclimation to 21.5°C reduced the escape performance – expressed as the total number of tail flips lobsters performed during the exhaustion experiments – of J. edwardsii at 14.0°C and 21.5°C experimental temperature (Fig. 3e) but not that of S. verreauxi (Fig. 3f). Escape speed was unaffected by thermal acclimation in both lobsters irrespective if expressed in absolute terms (cm × s^-1, ANOVA, F_{(2, 33)} = 2.44, p = 0.103) or relative to size (carapace length s^-1, ANOVA, F_{(2, 33)} = 2.18, p = 0.130). In addition, correlation analysis showed a significant relationship between tail flips and EPOC for J. edwardsii (Pearson, r₍₅₁₎ = 0.39, p = 3.835 e^-3) but not S. verreauxi (Pearson, r₍₅₁₎ = 0.23, p = 9.812 e^-2). Correlation between size dependent escape speed (carapace length s^-1) and EPOC was significant for both J. edwardsii (Pearson, r₍₅₁₎ = 0.34, p = 1.342 e^-2) and S. verreauxi (Pearson, r₍₅₁₎ = 0.28, p = 4.62 e^-2).

Resident versus range-shifting lobster

In addition to the effects of thermal acclimation, there were marked performance differences between the temperate J. edwardsii resident to Tasmania and the subtropical, range-shifting S. verreauxi. Most noticeable, on average, aerobic scope was 8-18% higher in S. verreauxi (ANOVA, F_{(1, 28)} = 11.37, p = 2.215 e^-3, 89.2 mg O₂ × h^-1 kg^-1 [83.3-94.6], n = 54), compared to J. edwardsii (75.6 mg O₂ × h^-1 kg^-1 [70.3-81.0], n = 54) particularly towards warmer experimental temperatures (≥ 17.5°C, Fig. 4, 5). This was due to a 6-14% larger maximum metabolic rate in S. verreauxi (ANOVA, F_{(1, 31)} = 9.54, p = 4.2 e^-3, 114.6 mg O₂ × h^-1 kg^-1 [108.5-120.6], n = 54) compared to J. edwardsii (101.7 mg O₂ × h^-1 kg^-1 [96.1-107.2], n = 54), while standard metabolic rates were similar among both species (ANOVA, F_{(1, 33)} = 0.05, p = 0.823, Fig. 4, 5).

Performance indicators of anaerobic metabolism, including EPOC (ANOVA, F_{(1, 33)} = 2.02, p = 0.165), recovery time (ANOVA, F_{(1, 33)} = 0.03, p = 0.956) and recovery rate (ANOVA, F_{(1, 33)} = 2.98, p = 0.094) were indifferent between both species, despite S. verreauxi tending towards 14-17% higher EPOC and 10-19% faster recovery rates (Figure 3a-d). However, S. verreauxi escaped 11-20% faster (ANOVA, F_{(1, 25)} = 11.59, p = 2.247 e^-3) and performed 22-35% more tails flips (ANOVA, F_{(1, 21)} = 9.91, p = 4.793 e^-3) compared to J. edwardsii from 14-21°C experimental temperatures (Fig. 5).

Marine organisms are highly vulnerable to climate warming, not only by being exposed to (potentially) critically high temperatures but also indirectly by a global climate-driven redistribution of species that may bring novel prey, predators, and competitors ⁹. Phenotypic plasticity is one vital mechanism of species to reduce climate-driven temperature stress ¹⁵ and extinction risk ⁷, yet whether this improves resilience to novel competitors remains unknown.

In this study we found that both a resident and a range-shifting spiny lobster dynamically adjust aerobic metabolism to sustain physiological performance in response to seasonal and forecasted temperature changes. However, at future summer temperatures, resident lobsters lose anaerobic escape capacity and fail to match the metabolic performance of range-shifting lobsters. Resident Tasmanian spiny lobsters are thus mal-equipped to cope with the dual pressures of warming and novel competitors.

Metabolic plasticity

Plastic adjustments (phenotypic plasticity) of metabolic rate are a common means for organisms to balance performance and thermodynamic increases of energy expenditure when temperatures rise. This is particularly vital for organisms inhabiting ocean warming hotspots, such as South-East Australia, which is heating up to 3–4 times faster than the global average ^3,39. We found that resident spiny lobster J. edwardsii can respond to such drastic changes, by dynamic shifts of standard metabolic rate, which reduces its basic energy needs by 29% at projected summer temperatures of 21.5°C (by 2070) compared to cold-acclimated lobsters (14°C, Fig. 2). Without this crucial adjustment, basic metabolic energy demand would increase and require lobsters to invest more time, energy, and risk to find prey to fuel this extra demand as well as trigger risky behavioural responses to predators ⁵⁹.

Adjusted standard metabolic rates further aided to sustain aerobic scope (the range between standard- and maximum metabolic rate) in both lobster species at warmer temperatures (Fig. 1). This is because, given the lack of thermal compensation and a lower thermal increase of maximum metabolic rate (Table 1), aerobic scope would decline towards warmer temperatures without the observed reduction of standard metabolic rate. Such an adjustment aids both lobster species, particularly cold-temperate J. edwardsii, to sustain full capacity for other non-maintenance related oxygen-fuelled activities up to 21.5°C projected summer temperatures. This may include feeding, digestion, migration, social interactions, or highly stressful events like moulting, which can exhaust the full aerobic scope of individual lobsters (personal observation, Supplementary Figure S1).

As for the two spiny lobster species in this study, metabolic plasticity is an important means for several other species to cope with temperature changes, particularly for aquatic ectotherms, such as molluscs and fish, but also other decapod crustaceans ^15,60. Yet, the underlying patterns are less well understood. Plastic standard metabolic rates but more rigid maximum metabolic rate observed in J. edwardsii and S. verreauxi (Fig. 2), have been found in European perch too, and was coined as “plastic floors and concrete ceilings” ⁶¹. Although not being a universal strategy ⁶², this indicates that, like perch, spiny lobsters prioritise adjustments of standard metabolic rate over maximum metabolic rates, which has the dual benefit of lowering maintenance costs while maintaining scope for aerobic activities. A further increase of aerobic scope at higher temperatures is either not critical to sustain daily activities or further rate increases of maximum metabolic rate are limited, by exhausted mitochondrial densities or capacities ⁵⁰, cardiac performance ⁶³, ventilatory oxygen extraction, or blood oxygen transport ^64–66.

On the other hand, alternative mechanisms may cause the observed depression of standard metabolic rate. For example, variation of organ mass can be an effective way to modify basic energy consumption ¹⁸, particularly in case of highly active tissues such as hearts or liver, which can explain up to 38% of standard metabolic rate variation e.g. European eel ⁶⁷. Changes of mitochondrial activities and densities are additional means to modify energy consumption, as the case for American lobsters where the activity of mitochondria´s key enzyme citrate synthase declined by 35% in tail muscle under combined exposure to high temperatures and CO₂ ⁶⁸. Temperature induced changes in mitochondrial function, such as differential substrate use or improved efficiency of oxidative phosphorylation can further optimise energy consumption ^20,69. Lobsters can also enlarge muscle fibres - at least during development - to lower surface to volume ratio and consequently reduce energetic costs to maintain membrane potential ^70,71. This however is limited by larger intracellular diffusion distances limiting oxygen flux ⁷¹. Irrespective of the mechanism at work, the observed plasticity of standard metabolic rate aids resident J. edwardsii to reduce fundamental energetic costs, which increases resilience to future warming trends particularly for marginal populations at the warmer trailing edge ⁸.

Anaerobic escape performance

Spiny lobsters escape from predators or other threats by powerful tail-flips, largely fuelled by anaerobic energy metabolism ^72,73. Exhaustive escape trials in this study revealed that anaerobic capacity, measured indirectly as excess post-exercise oxygen consumption rate (EPOC), declined steeply by 59% in warm-acclimated (21.5°C) J. edwardsii (Fig. 2). This was further supported by fewer escape attempts (tail flips), aligning closely with decreased EPOC (Fig. 2). Therefore, although J. edwardsii´s aerobic performance remained stable, anaerobic performance declined considerably, compromising its endurance to escape repeated threats when climate warming or heatwaves increase ocean temperatures to 21.5°C or higher in South-East Australia.

But why would J. edwardsii´s escape performance decline when ocean temperatures rise? In crustaceans, including spiny lobsters, burst muscle contractions are fuelled anaerobically ⁷³, particularly in large white muscle fibres ⁷². Initial bursts compose rapid tail flips fuelled by intracellular arginine phosphate pools, followed by slower less powerful bursts supported by anaerobic glycogenolysis, generating ATP from stored glycogen ^74,75. Initial arginine phosphates stores did not seem limiting in warm-acclimated J. edwardsii, as it performed initial escape bursts at full speed. However, its inability to maintain similar numbers of repeated bursts as cold-acclimated conspecifics (Fig. 3e), suggests that instead anaerobic glycogenolysis was limiting. This could be explained by lower glycogen stores or decreased glycolytic enzyme activity induced by chronic warming, yet current evidence is lacking and abdominal glycogen rather seems to be enhanced in warm-acclimated European lobsters Homarus gammarus ⁷⁶. Alternatively, warmer temperatures may reduce J. edwardsii´s ability to buffer lactate and protons accumulated during anaerobic (glycolytic) ATP production, as is the case for American lobsters, which have limited capacity to buffer low haemolymph pH with HCO₃^- and ammonia at higher temperature and pCO₂ ⁶⁸. The resulting drop in intracellular pH would then inhibit glycolytic enzymes and limit anaerobic power supply ⁷⁷.

Following the anaerobic power phase, lobsters eventually enter a slow oxygen-consuming (aerobic) recovery phase (i.e. EPOC) to return glycogen, pH and lactate to pre-exercise levels ⁵⁷. Here, warm-acclimated J. edwardsii recovered 4.7 hours faster than cold-acclimated conspecifics (Fig. 2c), mirroring the lower oxygen depth accumulated during the limited anaerobic power phase. Yet interestingly, warm-acclimated J. edwardsii tended to have 32.1% lower recovery rates (i.e. oxygen replenished per hour) than cold-acclimated animals, indicating reduced capacity for aerobic recovery, due to e.g. reduced mitochondrial enzymes activity or densities ⁶⁸. This may link to the observed reduction in basic energy consumption and would be an interesting path for further investigation together with spiny lobster´s capacity to buffer lactate and pH at future ocean warming scenarios.

As a result, if ocean temperatures continue to rise till 21.5°C, J. edwardsii will sustain its ability to escape from predator attacks or other disturbances, however, only if they occur at low frequency. At higher frequencies, J. edwardsii will quickly exhaust and be highly vulnerable to vigorous predators.

Resident versus range shifting lobsters

Although we found that J. edwardsii improves resilience to future ocean warming, by energy-conserving metabolic adjustments, this did not improve physiological performance relative to a novel range-shifting competitor, the eastern rock lobster S. verreauxi. This subtropical species increasingly co-occurs in the resident temperate habitat of J. edwardsii (Fig. 1) and will likely compete for shelter and/or food ^78,79, particularly in resource impoverished localities ⁸⁰, such as recently formed urchin-dominated barren habitats ⁸¹. In addition to the fact that S. verreauxi grows faster and much larger ⁴⁵, we found that it consistently matches or exceeds physiological and escape performance of J. edwardsii between 14–21°C, which included higher maximum metabolic rate, aerobic scope, escape frequency and speed (Fig. 4, 5). Even at, for S. verreauxi, relatively cold temperatures of 14°C, which is far below its optimal temperatures for growth (21.2°C ⁵⁶ or aerobic scope (24.9°C ³³, it performed 35% more tail-flips and escaped 20% faster than J. edwardsii (Fig. 5). Furthermore, despite their different thermal origins, S. verreauxi´s standard metabolic rate closely matched that of J. edwardsii between 14-21.5°C, and equally decreased with warm acclimation conserving 36% of metabolic energy (Fig. 2b). These findings are in line with previous results of higher maximum metabolic rate and aerobic scope but similar standard metabolic rates between 22–24°C for S. verreauxi puerulus larvae and juveniles compared to J. edwardsii ⁴⁸. This indicates that various life stages of S. verreauxi will outperform J. edwardsii in situations where physiological capacities become critical, particularly at current and future summer temperatures. For instance, during summer, S. verreauxi would have a larger metabolic scope to support migration, ranging or feeding ⁸², which could become a vital factor if both lobsters increasingly share habitat and resources, particularly in resource-poor habitats such as urchin barrens. Moreover, although, S. verreauxi´s escape performance is below or at similar levels of J. edwardsii´s at larval and juvenile life stages ⁴⁸, our study showed that this relationship inverts once S. verreauxi matures. As a result, larger S. verreauxi will be better able to fend-off vigorous predators such as Maori octopus (Octopus maorum), which may then preferentially target J. edwardsii instead, benefiting further expansion of S. verreauxi. If such flow-on effects add to negative interactions with other range-shifting species (e.g. Octopus tetricus), resident J. edwardsii will face increasing risk of range contraction ⁸³.

Metabolic performance differences have shown to influence competitive outcomes in other species. For example, a 3.2-fold higher routine metabolic rate linked to a three times higher feeding rate and a 6.7 time higher attack coefficient in the invasive Chinese mitten crab Eriocheir sinensis, compared to the co-existing native European crayfish Austropotamobius pallipes ⁸⁴. Similarly, at 9°C cold-adapted Arctic staghorn sculpin Gymnocanthus tricuspis had a lower aerobic scope than sculpins from warmer latitudes, which outcompeted Arctic staghorn sculpin in the search for protective shelter ⁸⁵. Both examples indicate that a larger metabolic scope for activity supports competitive dominance. However, given that differences of aerobic scope were much reduced at 4°C among sculpins, it further highlights the modulating role of temperature. For example, warm-acclimated freshwater crayfish Cherax destructor won over cold-acclimated conspecifics, supported by up-regulated mitochondrial ATP production capacity in chelae (pincer) muscle ⁶⁹. Further, in case of two co-existing Australian crayfish, temperatures markedly changed tail-flip performance, which peaked at different temperatures for each species, benefiting warm-adapted crayfish to better escape predators when temperatures rise ⁸⁶. This is in line with our findings, underlining that range-shifting subtropical S. verreauxi´s higher aerobic and escape performance, will provide a clear advantage over resident temperate J. edwardsii at current and future summer temperatures. This short-coming was not set-off by J. edwardsii´s adjustments of standard metabolic rates as range-shifting S. verreauxi mirrored this metabolic plasticity.

In this study we showed that resident J. edwardsii increased its resilience to ocean warming by metabolic plasticity, helping to conserve basic energy consumption and sustain scope for aerobic activities at future summer temperatures. However, this did not aid J. edwardsii to overcome the metabolic performance deficits in comparison to the range-shifting spiny lobster S. verreauxi and was further set back by reduced anaerobic escape capacities of J. edwardsii in response to future summer temperatures. We conclude that resident species like Tasmanian spiny lobsters may be able to cope with the direct effects of increasing ocean temperatures but will struggle to endure additional indirect pressures brought by warming such as novel interactions with range-shifting competitors. Trends exhibited for American lobsters, where distributions shifted poleward and offshore in response to warming, shell disease and novel invasive species ^32,87 may foreshadow J. edwardsii´s future. Yet, the lack of coastal habitat hinders any poleward shift for J. edwardsii, stressing the importance to ease environmental and fishing pressures, particularly for northern populations being most exposed to warming and novel species interactions.

Animals

Study animals comprised two species of Australian spiny lobsters. Cold-temperate southern rock lobsters (Jasus edwardsii, body mass 1074.6 g [976.0-1173.2], 12 males, 7 females) were caught from the Taroona marine research reserve at Crayfish point, Tasmania, using baited lobster pots from 5–9th February 2018. Subtropical eastern rock lobster (Sagmariasus verreauxi, body mass 1138 g [1054.1-1222.6], 12 males, 7 females) were obtained from commercial rock lobster fishermen (from Triabunna marina, Dover Seafoods and Leale Fishing, St Helens, Tasmania) from August 2017 till February 2018, who caught S. verreauxi as bycatch in coastal waters of eastern Tasmania. Lobsters were transported in ice-chilled polystyrene boxes to the IMAS Taroona research facilities, and each species kept separately in two 4000-L fiberglass outdoor tanks, supplied with flow-through seawater till the beginning of acclimation experiments.

Their distribution ranges from southern Victoria, around Tasmania and across South Australia into Western Australia as well as New Zealand waters for J. edwardsii, and along the east Australian coastline between Brisbane and the North-East coast of Tasmania, including the northern waters of New Zealand for S. verreauxi (Fig. 1). Both species live at depths ranging from 5–200 m at the Australian continental shelf ³⁷. Natural temperature ranges are ~ 10.8–17.5°C for J. edwardsii (Ion Pot, Tasmania ^2,88) and ~ 12–28°C for S. verreauxi ⁸⁹. Animal ethics were not required at the time of experimentation.

Temperature acclimation

Animals were acclimated to three temperatures for at least eight weeks. Acclimation temperatures were i) the annual average- (14.0°C, [14.1–14.2], n = 46,764), ii) the average summer- (17.5°C, [17.4–17.5], n = 7,988, for the two warmest months February-March) and iii) the average summer sea water temperature predicted for the East-Coast of Tasmania in 2070 (21.5°C, predicted temperature increase of 4°C based on IPCC AR5 scenario RCP8.5 following Hobday 2018 personal communication and the A1FI scenario in Pecl et al. 2009 ⁴⁶). Temperature means were calculated from temperature records at 9 m depth, Ion Pot, Tasmania from 2006–2016 ^2,88 (data and R script in Supplementary File S1). As only two lobsters could be examined within 48 hours, lobsters were acclimated, sequentially in pairs of one lobster for each species. This assured similar acclimation times at the time of the first measurement and further reduced variability introduced by parallel respirometry setups and handling by multiple experimenters. Lobsters were added randomly to acclimation tanks while accounting for balanced body mass distribution between acclimation groups (ANOVA, F_{(1, 38)} = 0.78, P = 0.384) and species (ANOVA, F_{(1, 38)} = 1.16, P = 0.289). Although we were unable to obtain equal numbers of females and males, we assured even distribution of sex across species and acclimation groups (Supplementary File S3).

Lobsters were housed in identical coated glass-fibre tanks (W × L × H, in cm, 100 × 100 × 75) for each acclimation temperature, and prior to each addition, transitioned to the new acclimation temperature overnight in a separate 300 L tank at a temperature change rate of 0.5°C per hour. Both species shared one tank but were physically separated by an oyster mesh barrier (Supplementary Figure S2). Tanks were equipped with two-level oyster mesh dwellings (W × L × H, in cm, 40 × 50 × 50), one for each species, to provide shelter and additional vertical space (Supplementary Figure S2). Each acclimation tank was filled up to 0.65 m³ and supplied with 14.0°C ([14.0–14.0], n = 784,797) cold sea water, temperature controlled via an external heat-chill unit. Additional submersible 2000 W titanium heaters maintained the water temperature in the summer temperature acclimation tanks at 17.5°C ([17.5–17.5], n = 750,404) and 21.4°C on average ([21.4–21.4], n = 775,440) respectively. The temperature for each tank was continuously monitored and logged using open-hardware components ⁹⁰, i.e. an open-source microcontroller (Arduino Uno R3, Italy), three waterproof digital temperature probes (DS18B20, China) and a SD card logger module (Adafruit data logger shield, USA), fitted in a custom designed 3D printed plastic enclosure. Two RGB flood lights supplied weak blue light to illuminate acclimation tanks under a 12:12 light:dark photoperiod, controlled remotely via infra-red LEDs and a custom programmed open source microcontroller (Arduino Uno R3, Italy).

Acclimation vessels received filtered and disinfected (sand filtration, foam fractionation, ozonation and activated carbon filtration) flow through sea water at an exchange rate of the tank volume approximately every two hours (flow rate ~ 300 L h^-1) and regular removal of debris and left-over mussel shells every 2–3 days. Previous testing showed that water quality parameters such as nitrate, ammonia or heavy metals were below critical levels at those water exchange rates.

Animals were fed on Monday, Wednesday, and Friday with live blue mussel (Mytilus galloprovincialis) or frozen, chopped sardines (Sardina pilchardus). Lobsters that moulted were not used for experiments and allowed to recover for at least two weeks. Three southern rock lobsters and two eastern rock lobsters had to be replaced due to excess moulting stress and cannibalism following moulting. At the end of all experiments, we took final measurements of body mass, body volume, carapace length, carapace width, blood pH and Brix index, and returned lobsters to IMAS aquaculture holding tanks.

Metabolic rate measurements

Once each lobster pair completed its respective acclimation period and was starved for at least 48 hrs, we measured oxygen consumption rates using intermittent respirometry over a 48–72 hr period. Measurements followed a repeated measures design, starting at the respective acclimation temperature for each lobster pair, followed by measurements at the other two acclimation temperatures. This cross-over design allowed to compare acclimation effects at identical measurement temperatures. To avoid carry-over effects by repeated experiments, animals were given at least two weeks’ time between experiments to recover in their original acclimation tanks. In addition, experiments with a large difference between acclimation- and experimental temperature (e.g. 14.0°C ◊ 21.5°C) were performed last and included a short, stepwise acclimatization period to the final experimental temperature for at least three hours prior to measurements to reduce acute temperature stress. To minimise effects by capture and transfer stress immediately before experiments, each lobster was placed overnight in a covered bucket floating in the same acclimation tank. The next morning, lobsters could be moved directly from the bucket to the chase tank with minimal visual or physical disturbance by the experimenter, to assure lobsters were fully rested before chasing.

In the 300 L chase tank (W × L × H, in cm, 120 × 60 × 50), lobsters were exhausted to fatigue, to allow subsequent measurements of maximum metabolic rate (MMR) and aerobic scope in the respirometer. Due to variable effectiveness of single chasing methods among individuals we applied the following multi-step chase protocol to assure that lobsters were fully exhausted: i) touching of antennae and ii) gentle pressing of the ventral soft tissue, located between the last pair of pereiopods and the abdomen, to trigger tail flips and iii) lastly turning of the lobster on its back till it failed to turn back within 60 secs three times. Steps i) and ii) were considered completed till lobsters failed to respond five or more times to the respective procedure. Each chase procedure was video recorded using a camera (GoPro Hero5, GoPro Inc., USA) mounted on top of the chase arena with a flexible gooseneck clamp. A waterproof RGB multi-colour LED strip (5 m 5050 RGB, 60 SMD LEDs / m, Brightness: 900 LM, China) layered 20 cm below the translucent bottom of the chase tank, illuminated the chase arena with yellow light and provided a sharp contrast for the subsequent video analysis. The temperature of the chase tank was set to the experimental temperature using a 2000 W titanium heater modified with a programmable PID (proportional–integral–derivative) controller (SmartPID, Arzaman, Italy). The heating was performed via an external buffer tank, connected to a recirculation pump, to allow an obstruction free chase arena.

Immediately after chasing, we measured the lobster’s oxygen consumption rates (MO₂) as a measure of aerobic metabolism using intermittent flow respirometry. For this, we placed lobsters into two cylindrical 10 L custom-made Perspex respirometry chambers (L×D in cm, 66 × 15), tail first to prevent blocking and injury due to the lobster’s guarding posture ⁹¹. Lobsters could gain traction to oyster mesh added to the bottom of the respirometer, held in place with an open cut piece of plastic pipe (see Fig. 7A in Oellermann et al. 2020 ⁵⁰). Chambers were sealed within two minutes after addition of lobsters.

Oxygen concentration was measured every 10 seconds using a fibre optic two-channel oxygen meter (HQ40d, Hach, USA) and oxygen probes positioned into an external recirculation loop. Re-circulation pumps provided continuous mixing of water via Tygon® tubing within respirometers at a flow of 1200 L min^− 1. Following a six-minute respiration cycle, flush pumps re- oxygenated chambers at a flow of ca. 1500 L min^− 1 for eight minutes, using a time controlled digital recycling timer (DRT-1, Sentinel, USA). The two adjacent respirometers were housed in a buffer tank (W×L×H in cm, 102 × 52 × 50), filled with 190 L filtered and filtered flow-through sea water at a flow rate of 130–150 L h^− 1. The water temperature of the buffer tank was maintained at the respective experimental temperature using a 2000 W titanium heater. An air stone ensured homogenous mixing and aeration. Black building foil covering the experimental setup and corrugated plastic sheet between respirometers prevented the lobsters from being visually disturbed during the trials. A yellow LED flood light illuminated the setup permanently to reduce dark-induced activity of the nocturnal lobsters ⁹². After completion of respirometry, we returned lobsters to their original acclimation tanks. After each experiment, the chambers and buffer tank were cleaned and flushed with fresh water. Preliminary tests confirmed appropriate mixing of water in the chamber, the lack of leaks (i.e. dye test) and appropriate flush/respiration cycles.

Oxygen consumptions rates were calculated as in Svendsen et al. ⁹³. Oxygen saturation in respiration chambers decreased to a minimum of 86.6% ([85.8–87.3], n = 108) on average, and never fell below 77%. Individual body volume of lobsters was accounted for in MO₂ calculations and measured as the volume overflow in ml after adding lobsters to a water levelled container. Body density did not differ significantly between species (ANOVA, F_{(1, 45)} = 2.31, P = 0.136) and averaged 1.12 g ml^− 1 ([1.10–1.14], n = 46). Background respiration was recorded before and after each experiment and accounted on average for 4.5 % ([3.9–5.1], n = 105) or 5.0 % ([4.3–5.6], n = 105) respectively of standard metabolic rate. Maximum metabolic rate (MMR) was the single highest MO₂ measured over the entire experiment, and routine metabolic rate the mean MO₂ following a 16 hr recovery period till the end of the trial (16 hrs was observed to be the maximum time all lobsters required to recover). Standard metabolic rate was calculated as the mean of the 10% lowest MO₂ values ^33,94. The time at which MO₂ fell three times below routine metabolic rate + one standard deviation after exercise, was marked as recovery time. Excess post-exercise oxygen consumption (EPOC) was calculated as the area under the MO₂ curve from the start of MO₂ measurements till recovery time. Aerobic scope was calculated as maximum metabolic rate – standard metabolic rate ^33,94. Recovery rate was calculated as EPOC divided by recovery time and expressed as mg O₂ per kg body mass and hour.

Data and statistical analysis

We analysed the chase videos using a customised Python script (Python 3.8, Supplementary File S1) to record total number of escapes and escape speed. Here we marked individual lobster positions (by mouse clicks) before and after each tail flip and saved the x and y pixel positions and the respective video frame number in a csv file. All further data processing and statistical data analysis was performed using R statistical software ⁹⁵ and RStudio ⁹⁶. In R we calculated the Euclidian distance Eq. (1) and divided this by the number of video frames for each corresponding escape event, times the recording frame rate (24 frames sec^− 1) and a conversion factor to scale pixels to cm to obtain the escape speed (cm sec^− 1, R scripts in Supplementary Files S2).

For the statistical analysis we employed linear mixed effect models to test the effects of acclimation- and experimental temperatures on each of the measured variables (MO_2Standard, MO_2Routine, MO_2Max, aerobic scope, fractional aerobic scope, EPOC, recovery time, escape speed and total escapes) using the lme4 package ⁹⁷. For all models, we included acclimation temperature, experimental temperatures and species and their three-way interaction as fixed factors. As random effects, we had lobster ID as intercepts, to account for individual variation between lobsters. Initially we constructed a more complex model for each response variable using maximum likelihood estimation (ML), which included sex, body mass, respirometer chamber, experimental duration, and acclimation time as additional fixed factors. We then identified the simplest model using a stepwise backward elimination process of fixed factors, via Sattethwaite's approximation of p-values, using the lmerTest package ⁹⁸. We then re-fitted the final model using restricted maximum likelihood (REML) estimation and performed post hoc pairwise comparisons with Bonferroni correction between levels of acclimation temperature and experimental temperature using the emmeans package ⁹⁹. We assessed the linearity, homoskedasticity and normality of residuals using residual plots and the Shapiro-Wilk normality test respectively, to test if the data meet the linear mixed effect model assumptions. If data failed to meet the model assumptions, data were log (SMR) or square transformed (aerobic scope). Relations between escape metrics and EPOC or maximum metabolic rate were tested separately for each species using Pearson correlation, if data passed the Shapiro-Wilk normality test. All values in the manuscript are expressed as mean and the 95% confidence interval in squared brackets. Full model details and formulae are available as R Markdown files in the Supplementary Files S2. The complete data set can be found in Supplementary Table S1.

Acknowledgements

We would like to thank all staff at IMAS Taroona for their technical and logistical assistance, particularly Greg Smith, Larnie Linton, Ross Goldsmid, Karl van Drunen, Craig Thomas, Alan Beech, Matthew Allen, Karen Watson, Johnny Waters and Lisette Robertson. We further thank Alistair Hobday for providing regional warming forecasts for Eastern Tasmania as well as Dover Seafoods, Leale Fising and an anonymous Triabunna fishermen for providing wild caught S. verreauxi. We acknowledge the palawa, traditional custodians of lutruwita who have extensive knowledge of nubeena.

Funding

Open Access funding enabled and organized by Projekt DEAL. This work was supported by the German Research Foundation (DFG) fellowships [OE 658/1 and OE 658/2 to M.O.] and an Australian Research Council (ARC) Future Fellowship to G.T.P.

Data Availability

The dataset generated and analysed during the current study and all supplementary information are available in the figshare repository, (Private link till peer review is completed: https://figshare.com/s/cbed7c33a3c57c3950b3).

Competing interests

The authors declare no competing interests.

Author contributions

M.O, Q.P.F and G.T.P. conceptualized the study and provided instrumentation, laboratory resources and funding. M.O. developed instrumental software and hardware; set up, validated, and performed experiments; collected, curated, analysed, and visualised data; wrote the main manuscript text as well as supervised and managed the project. All authors developed the methodology as well as reviewed and edited the manuscript.

Kwiatkowski, L. et al. Twenty-first century ocean warming, acidification, deoxygenation, and upper-ocean nutrient and primary production decline from CMIP6 model projections. Biogeosciences 17, 3439–3470, http://doi.org/10.5194/bg-17-3439-2020 (2020).
Yeruham, E., Shpigel, M., Abelson, A. & Rilov, G. Ocean warming and tropical invaders erode the performance of a key herbivore., 101, e02925 https://doi.org/10.1002/ecy.2925 (2020).
Groner, M. L., Shields, J. D., Landers, D. F. Jr., Swenarton, J. & Hoenig, J. M. Rising temperatures, molting phenology, and epizootic shell disease in the American lobster. Am. Nat, 192, E163–E177 https://doi.org/10.1086/699478 (2018).
Behringer, D. C. & Hart, J. E. Competition with stone crabs drives juvenile spiny lobster abundance and distribution., 184, 205–218 https://doi.org/10.1007/s00442-017-3844-1 (2017).
Rossong, M. A., Williams, P. J., Comeau, M., Mitchell, S. C. & Apaloo, J. Agonistic interactions between the invasive green crab, Carcinus maenas (Linnaeus) and juvenile American lobster, Homarus americanus (Milne Edwards). J. Exp. Mar. Biol. Ecol, 329, 281–288 https://doi.org/10.1016/j.jembe.2005.09.007 (2006).
Fitzgibbon, Q. P., Simon, C. J., Smith, G. G., Carter, C. G. & Battaglene, S. C. Temperature dependent growth, feeding, nutritional condition and aerobic metabolism of juvenile spiny lobster, Sagmariasus verreauxi. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol, 207, 13–20 https://doi.org/10.1016/j.cbpa.2017.02.003 (2017).
Boyle, K. L., Dillaman, R. M. & Kinsey, S. T. Mitochondrial distribution and glycogen dynamics suggest diffusion constraints in muscle fibers of the blue crab, Callinectes sapidus. J. Exp. Zool, 297, 1–16 https://doi.org/10.1002/jez.a.10227 (2003).
Lee, C. G., Farrell, A. P., Lotto, A., Hinch, S. G. & Healey, M. C. Excess post-exercise oxygen consumption in adult sockeye (Oncorhynchus nerka) and coho (O. kisutch) salmon following critical speed swimming. J. Exp. Biol, 206, 3253–3260 https://doi.org/10.1242/jeb.00548 (2003).
Briceno, F. A., Fitzgibbon, Q. P., Polymeropoulos, E. T., Hinojosa, I. A. & Pecl, G. T. Temperature alters the physiological response of spiny lobsters under predation risk. Conserv. Physiol, 8, coaa065 https://doi.org/10.1093/conphys/coaa065 (2020).
Powell, M. L. & Watts, S. A. Effect of temperature acclimation on metabolism and hemocyanin binding affinities in two crayfish, Procambarus clarkii and Procambarus zonangulus. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol, 144, 211–217 https://doi.org/10.1016/j.cbpa.2006.02.032 (2006).
Sandblom, E. et al. Physiological constraints to climate warming in fish follow principles of plastic floors and concrete ceilings. Nat. Commun, 7, 11447 https://doi.org/10.1038/ncomms11447 (2016).
Rodgers, E. M. & Franklin, C. E. Aerobic scope and climate warming: Testing the "plastic floors and concrete ceilings" hypothesis in the estuarine crocodile (Crocodylus porosus). J. Exp. Zool. Part A, 335, 108–117 https://doi.org/10.1002/jez.2412 (2021).
Farrell, A. P. Environment, antecedents and climate change: lessons from the study of temperature physiology and river migration of salmonids. J. Exp. Biol, 212, 3771–3780 https://doi.org/10.1242/jeb.023671 (2009).
Hedrick, M. S., Hancock, T. V. & Hillman, S. S. inCompr. Physiol.1677–1703(2015).
Frederich, M. & Pörtner, H. O. Oxygen limitation of thermal tolerance defined by cardiac and ventilatory performance in spider crab, Maja squinado. Am. J. Physiol. Regul. Integr. Comp. Physiol, 279, R1531–R1538 https://doi.org/10.1152/ajpregu.2000.279.5.R1531 (2000).
Verberk, W. C. E. P. et al. Does oxygen limit thermal tolerance in arthropods? A critical review of current evidence. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol, 192, 64–78 https://doi.org/10.1016/j.cbpa.2015.10.020 (2016).
Boldsen, M. M., Norin, T. & Malte, H. Temporal repeatability of metabolic rate and the effect of organ mass and enzyme activity on metabolism in European eel (Anguilla anguilla). Comp. Biochem. Physiol. Part A Mol. Integr. Physiol, 165, 22–29 https://doi.org/10.1016/j.cbpa.2013.01.027 (2013).
Klymasz-Swartz, A. K. et al. Impact of climate change on the American lobster (Homarus americanus): Physiological responses to combined exposure of elevated temperature and pCO2. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol, 235, 202–210 https://doi.org/10.1016/j.cbpa.2019.06.005 (2019).
Seebacher, F. & Wilson, R. S. Fighting fit: thermal plasticity of metabolic function and fighting success in the crayfish Cherax destructor. Funct. Ecol, 20, 1045–1053 https://doi.org/10.1111/j.1365-2435.2006.01194.x (2006).
Jimenez, A. G., Dasika, S. K., Locke, B. R. & Kinsey, S. T. An evaluation of muscle maintenance costs during fiber hypertrophy in the lobster Homarus americanus: are larger muscle fibers cheaper to maintain? J. Exp. Biol, 214, 3688–3697 https://doi.org/10.1242/jeb.060301 (2011).
Jimenez, A. G., Locke, B. R. & Kinsey, S. T. The influence of oxygen and high-energy phosphate diffusion on metabolic scaling in three species of tail-flipping crustaceans. J. Exp. Biol, 211, 3214–3225 https://doi.org/10.1242/jeb.020677 (2008).
Johnson, L. K., Dillaman, R. M., Gay, D. M., Blum, J. E. & Kinsey, S. T. Metabolic influences of fiber size in aerobic and anaerobic locomotor muscles of the blue crab, Callinectes sapidus. J. Exp. Biol, 207, 4045–4056 https://doi.org/10.1242/jeb.01224 (2004).
Speed, S. R., Baldwin, J., Wong, R. J. & Wells, R. M. G. Metabolic characteristics of muscles in the spiny lobster, Jasus edwardsii, and responses to emersion during simulated live transport. Comp. Biochem. Phys. B, 128, 435–444 https://doi.org/10.1016/S1096-4959(00)00340-7 (2001).
England, W. & Baldwin, J. Anaerobic energy metabolism in the tail musculature of the Australian yabby Cherax destructor (Crustacea, Decapoda, Parastacidae): role of phosphagens and anaerobic glycolysis during escape behavior. Physiol. Zool, 56, 614–622 https://doi.org/10.1086/physzool.56.4.30155884 (1983).
Head, G. & Baldwin, J. Energy metabolism and the fate of lactate during recovery from exercise in the Australian freshwater crayfish Cherax destructor. Mar. Freshw. Res, 37, 641–646 https://doi.org/10.1071/MF9860641 (1986).
Goncalves, R., Lund, I. & Gesto, M. Interactions of temperature and dietary composition on juvenile European lobster (Homarus gammarus, L.) energy metabolism and performance. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol, 260, 111019 https://doi.org/10.1016/j.cbpa.2021.111019 (2021).
Baldwin, J., Gupta, A. & Iglesias, X. Scaling of anaerobic energy metabolism during tail flipping behaviour in the freshwater crayfish, Cherax destructor. Mar. Freshw. Res, 50, 183–187 https://doi.org/10.1071/MF98110 (1999).
Sabino, M. A. et al. Habitat degradation increases interspecific trophic competition between three spiny lobster species in Seychelles. Estuarine, Coastal and Shelf Science, 256, 107368 https://doi.org/10.1016/j.ecss.2021.107368 (2021).
Twiname, S. et al. Resident lobsters dominate food competition with range-shifting lobsters in an ocean warming hotspot. Mar. Ecol. Prog. Ser. submitted(2021).
Briones-Fourzan, P., Lozano-Alvarez, E., Negrete-Soto, F. & Barradas-Ortiz, C. Enhancement of juvenile Caribbean spiny lobsters: an evaluation of changes in multiple response variables with the addition of large artificial shelters., 151, 401–416 https://doi.org/10.1007/s00442-006-0595-9 (2007).
Ling, S. et al. Global regime shift dynamics of catastrophic sea urchin overgrazing. Philos. Trans. R. Soc. Lond. B, Biol. Sci, 370, 20130269 https://doi.org/10.1098/rstb.2013.0269 (2015).
Norin, T. & Clark, T. D. Measurement and relevance of maximum metabolic rate in fishes. J. Fish Biol, 88, 122–151 https://doi.org/10.1111/jfb.12796 (2016).
Marzloff, M. P. et al. Modelling marine community responses to climate-driven species redistribution to guide monitoring and adaptive ecosystem-based management. Glob. Change Biol, 22, 2462–2474 https://doi.org/10.1111/gcb.13285 (2016).
Taylor, N. G. & Dunn, A. M. Predatory impacts of alien decapod Crustacea are predicted by functional responses and explained by differences in metabolic rate. Biol. Invasions, 20, 2821–2837 https://doi.org/10.1007/s10530-018-1735-y (2018).
Seth, H. et al. Metabolic scope and interspecific competition in sculpins of Greenland are influenced by increased temperatures due to climate change., 8, e62859 https://doi.org/10.1371/journal.pone.0062859 (2013).
Stoffels, R. J., Richardson, A. J., Vogel, M. T., Coates, S. P. & Muller, W. J. What do metabolic rates tell us about thermal niches? Mechanisms driving crayfish distributions along an altitudinal gradient., 180, 45–54 https://doi.org/10.1007/s00442-015-3463-7 (2016).
Mazur, M. D., Friedland, K. D., McManus, M. C. & Goode, A. G. Dynamic changes in American lobster suitable habitat distribution on the Northeast U.S. Shelf linked to oceanographic conditions. Fish. Oceanogr, 29, 349–365 https://doi.org/10.1111/fog.12476 (2020).
Stobart, B., Mayfield, S., Mundy, C., Hobday, A. J. & Hartog, J. R. Comparison of in situ and satellite sea surface-temperature data from South Australia and Tasmania: how reliable are satellite data as a proxy for coastal temperatures in temperate southern Australia? Mar. Freshw. Res, 67, https://doi.org/10.1071/mf14340 (2016).
Montgomery, S. S., Liggins, G. W., Craig, J. R. & McLeod, J. R. Growth of the spiny lobster Jasus verreauxi (Decapoda: Palinuridae) off the east coast of Australia. N. Z. J. Mar. Freshw. Res, 43, 113–123 https://doi.org/10.1080/00288330909509986 (2009).
Oellermann, M. et al. Harnessing the benefits of open electronics in science.arXiv preprint, http://doi.org/https://arxiv.org/abs/2106.15852 (2021).
Jensen, M. A., Fitzgibbon, Q. P., Carter, C. G. & Adams, L. R. Effect of body mass and activity on the metabolic rate and ammonia-N excretion of the spiny lobster Sagmariasus verreauxi during ontogeny. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol, 166, 191–198 https://doi.org/10.1016/j.cbpa.2013.06.003 (2013).
Briceño, F. A., Polymeropoulos, E. T., Fitzgibbon, Q. P., Dambacher, J. M. & Pecl, G. T. Changes in metabolic rate of spiny lobster under predation risk. Mar. Ecol. Prog. Ser, 598, 71–84 https://doi.org/10.3354/meps12644 (2018).
Svendsen, M. B. S., Bushnell, P. G. & Steffensen, J. F. Design and setup of intermittent-flow respirometry system for aquatic organisms. J. Fish Biol, 88, 26–50 https://doi.org/10.1111/jfb.12797 (2016).
Clark, T. D., Sandblom, E. & Jutfelt, F. Aerobic scope measurements of fishes in an era of climate change: respirometry, relevance and recommendations. J. Exp. Biol, 216, 2771–2782 https://doi.org/10.1242/jeb.084251 (2013).
R. A language and environment for statistical computing (Vienna, Austria, 2021).
Rstudio Integrated development environment for R(Boston, MA, USA, 2021).
Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw, 67, https://doi.org/10.18637/jss.v067.i01 (2015). http://doi.org/http://hdl.handle.net/
Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. lmerTest package: tests in linear mixed effects models. J. Stat. Softw, 82, 1–26 https://doi.org/10.18637/jss.v082.i13 (2017).
emmeans: Estimated Marginal Means, aka Least-Squares Means. v. 1.6.2-1 (2021).
Oellermann, M., Hickey, A. J. R., Fitzgibbon, Q. P. & Smith, G. Thermal sensitivity links to cellular cardiac decline in three spiny lobsters. Sci. Rep. 10, 202, http://doi.org/10.1038/s41598-019-56794-0 (2020).
Hooker, S. H., Jeffs, A. G., Creese, R. G. & Sivaguru, K. Growth of captive < emph type="2">Jasus edwardsii</emph> (Hutton) (Crustacea:Palinuridae) in north-eastern New Zealand. Mar. Freshw. Res. 48, 903–910, http://doi.org/10.1071/MF97156 (1998).
Yeruham, E., Shpigel, M., Abelson, A. & Rilov, G. Ocean warming and tropical invaders erode the performance of a key herbivore. Ecology 101, e02925, http://doi.org/10.1002/ecy.2925 (2020).
Groner, M. L., Shields, J. D., Landers, D. F., Jr., Swenarton, J. & Hoenig, J. M. Rising temperatures, molting phenology, and epizootic shell disease in the American lobster. The American Naturalist 192, E163-E177, http://doi.org/10.1086/699478 (2018).
Behringer, D. C. & Hart, J. E. Competition with stone crabs drives juvenile spiny lobster abundance and distribution. Oecologia 184, 205–218, http://doi.org/10.1007/s00442-017-3844-1 (2017).
Rossong, M. A., Williams, P. J., Comeau, M., Mitchell, S. C. & Apaloo, J. Agonistic interactions between the invasive green crab, Carcinus maenas (Linnaeus) and juvenile American lobster, Homarus americanus (Milne Edwards). J. Exp. Mar. Biol. Ecol. 329, 281–288, http://doi.org/10.1016/j.jembe.2005.09.007 (2006).
Fitzgibbon, Q. P., Simon, C. J., Smith, G. G., Carter, C. G. & Battaglene, S. C. Temperature dependent growth, feeding, nutritional condition and aerobic metabolism of juvenile spiny lobster, Sagmariasus verreauxi. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 207, 13–20, http://doi.org/10.1016/j.cbpa.2017.02.003 (2017).
Boyle, K. L., Dillaman, R. M. & Kinsey, S. T. Mitochondrial distribution and glycogen dynamics suggest diffusion constraints in muscle fibers of the blue crab, Callinectes sapidus. J. Exp. Zool. 297, 1–16, http://doi.org/10.1002/jez.a.10227 (2003).
Lee, C. G., Farrell, A. P., Lotto, A., Hinch, S. G. & Healey, M. C. Excess post-exercise oxygen consumption in adult sockeye (Oncorhynchus nerka) and coho (O. kisutch) salmon following critical speed swimming. J. Exp. Biol. 206, 3253–3260, http://doi.org/10.1242/jeb.00548 (2003).
Briceno, F. A., Fitzgibbon, Q. P., Polymeropoulos, E. T., Hinojosa, I. A. & Pecl, G. T. Temperature alters the physiological response of spiny lobsters under predation risk. Conserv. Physiol. 8, coaa065, http://doi.org/10.1093/conphys/coaa065 (2020).
Powell, M. L. & Watts, S. A. Effect of temperature acclimation on metabolism and hemocyanin binding affinities in two crayfish, Procambarus clarkii and Procambarus zonangulus. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 144, 211–217, http://doi.org/10.1016/j.cbpa.2006.02.032 (2006).
Sandblom, E. et al. Physiological constraints to climate warming in fish follow principles of plastic floors and concrete ceilings. Nat. Commun. 7, 11447, http://doi.org/10.1038/ncomms11447 (2016).
Rodgers, E. M. & Franklin, C. E. Aerobic scope and climate warming: Testing the "plastic floors and concrete ceilings" hypothesis in the estuarine crocodile (Crocodylus porosus). J. Exp. Zool. Part A 335, 108–117, http://doi.org/10.1002/jez.2412 (2021).
Farrell, A. P. Environment, antecedents and climate change: lessons from the study of temperature physiology and river migration of salmonids. J. Exp. Biol. 212, 3771–3780, http://doi.org/10.1242/jeb.023671 (2009).
Hedrick, M. S., Hancock, T. V. & Hillman, S. S. in Compr. Physiol. 1677–1703 (2015).
Frederich, M. & Pörtner, H. O. Oxygen limitation of thermal tolerance defined by cardiac and ventilatory performance in spider crab, Maja squinado. Am. J. Physiol. Regul. Integr. Comp. Physiol. 279, R1531-R1538 http://doi.org/10.1152/ajpregu.2000.279.5.R1531 (2000).
Verberk, W. C. E. P. et al. Does oxygen limit thermal tolerance in arthropods? A critical review of current evidence. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 192, 64–78, http://doi.org/10.1016/j.cbpa.2015.10.020 (2016).
Boldsen, M. M., Norin, T. & Malte, H. Temporal repeatability of metabolic rate and the effect of organ mass and enzyme activity on metabolism in European eel (Anguilla anguilla). Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 165, 22–29, http://doi.org/10.1016/j.cbpa.2013.01.027 (2013).
Klymasz-Swartz, A. K. et al. Impact of climate change on the American lobster (Homarus americanus): Physiological responses to combined exposure of elevated temperature and pCO2. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 235, 202–210, http://doi.org/10.1016/j.cbpa.2019.06.005 (2019).
Seebacher, F. & Wilson, R. S. Fighting fit: thermal plasticity of metabolic function and fighting success in the crayfish Cherax destructor. Funct. Ecol. 20, 1045–1053, http://doi.org/10.1111/j.1365-2435.2006.01194.x (2006).
Jimenez, A. G., Dasika, S. K., Locke, B. R. & Kinsey, S. T. An evaluation of muscle maintenance costs during fiber hypertrophy in the lobster Homarus americanus: are larger muscle fibers cheaper to maintain? J. Exp. Biol. 214, 3688–3697, http://doi.org/10.1242/jeb.060301 (2011).
Jimenez, A. G., Locke, B. R. & Kinsey, S. T. The influence of oxygen and high-energy phosphate diffusion on metabolic scaling in three species of tail-flipping crustaceans. J. Exp. Biol. 211, 3214–3225, http://doi.org/10.1242/jeb.020677 (2008).
Johnson, L. K., Dillaman, R. M., Gay, D. M., Blum, J. E. & Kinsey, S. T. Metabolic influences of fiber size in aerobic and anaerobic locomotor muscles of the blue crab, Callinectes sapidus. J. Exp. Biol. 207, 4045–4056, http://doi.org/10.1242/jeb.01224 (2004).
Speed, S. R., Baldwin, J., Wong, R. J. & Wells, R. M. G. Metabolic characteristics of muscles in the spiny lobster, Jasus edwardsii, and responses to emersion during simulated live transport. Comp. Biochem. Phys. B 128, 435–444, http://doi.org/10.1016/S1096-4959(00)00340-7 (2001).
England, W. & Baldwin, J. Anaerobic energy metabolism in the tail musculature of the Australian yabby Cherax destructor (Crustacea, Decapoda, Parastacidae): role of phosphagens and anaerobic glycolysis during escape behavior. Physiol. Zool. 56, 614–622, http://doi.org/10.1086/physzool.56.4.30155884 (1983).
Head, G. & Baldwin, J. Energy metabolism and the fate of lactate during recovery from exercise in the Australian freshwater crayfish Cherax destructor. Mar. Freshw. Res. 37, 641–646, http://doi.org/10.1071/MF9860641 (1986).
Goncalves, R., Lund, I. & Gesto, M. Interactions of temperature and dietary composition on juvenile European lobster (Homarus gammarus, L.) energy metabolism and performance. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 260, 111019, http://doi.org/10.1016/j.cbpa.2021.111019 (2021).
Baldwin, J., Gupta, A. & Iglesias, X. Scaling of anaerobic energy metabolism during tail flipping behaviour in the freshwater crayfish, Cherax destructor. Mar. Freshw. Res. 50, 183–187, http://doi.org/10.1071/MF98110 (1999).
Sabino, M. A. et al. Habitat degradation increases interspecific trophic competition between three spiny lobster species in Seychelles. Estuarine, Coastal and Shelf Science 256, 107368, http://doi.org/10.1016/j.ecss.2021.107368 (2021).
Twiname, S. et al. Resident lobsters dominate food competition with range-shifting lobsters in an ocean warming hotspot. Mar. Ecol. Prog. Ser. submitted (2021).
Briones-Fourzan, P., Lozano-Alvarez, E., Negrete-Soto, F. & Barradas-Ortiz, C. Enhancement of juvenile Caribbean spiny lobsters: an evaluation of changes in multiple response variables with the addition of large artificial shelters. Oecologia 151, 401–416, http://doi.org/10.1007/s00442-006-0595-9 (2007).
Ling, S. et al. Global regime shift dynamics of catastrophic sea urchin overgrazing. Philos. Trans. R. Soc. Lond. B, Biol. Sci. 370, 20130269, http://doi.org/10.1098/rstb.2013.0269 (2015).
Norin, T. & Clark, T. D. Measurement and relevance of maximum metabolic rate in fishes. J. Fish Biol. 88, 122–151, http://doi.org/10.1111/jfb.12796 (2016).
Marzloff, M. P. et al. Modelling marine community responses to climate-driven species redistribution to guide monitoring and adaptive ecosystem-based management. Glob. Change Biol. 22, 2462–2474, http://doi.org/10.1111/gcb.13285 (2016).
Taylor, N. G. & Dunn, A. M. Predatory impacts of alien decapod Crustacea are predicted by functional responses and explained by differences in metabolic rate. Biol. Invasions 20, 2821–2837, http://doi.org/10.1007/s10530-018-1735-y (2018).
Seth, H. et al. Metabolic scope and interspecific competition in sculpins of Greenland are influenced by increased temperatures due to climate change. Plos One 8, e62859, http://doi.org/10.1371/journal.pone.0062859 (2013).
Stoffels, R. J., Richardson, A. J., Vogel, M. T., Coates, S. P. & Muller, W. J. What do metabolic rates tell us about thermal niches? Mechanisms driving crayfish distributions along an altitudinal gradient. Oecologia 180, 45–54, http://doi.org/10.1007/s00442-015-3463-7 (2016).
Mazur, M. D., Friedland, K. D., McManus, M. C. & Goode, A. G. Dynamic changes in American lobster suitable habitat distribution on the Northeast U.S. Shelf linked to oceanographic conditions. Fish. Oceanogr. 29, 349–365, http://doi.org/10.1111/fog.12476 (2020).
Stobart, B., Mayfield, S., Mundy, C., Hobday, A. J. & Hartog, J. R. Comparison of in situ and satellite sea surface-temperature data from South Australia and Tasmania: how reliable are satellite data as a proxy for coastal temperatures in temperate southern Australia? Mar. Freshw. Res. 67, http://doi.org/10.1071/mf14340 (2016).
Montgomery, S. S., Liggins, G. W., Craig, J. R. & McLeod, J. R. Growth of the spiny lobster Jasus verreauxi (Decapoda: Palinuridae) off the east coast of Australia. N. Z. J. Mar. Freshw. Res. 43, 113–123, http://doi.org/10.1080/00288330909509986 (2009).
Oellermann, M. et al. Harnessing the benefits of open electronics in science. arXiv preprint, http://doi.org/https://arxiv.org/abs/2106.15852 (2021).
Jensen, M. A., Fitzgibbon, Q. P., Carter, C. G. & Adams, L. R. Effect of body mass and activity on the metabolic rate and ammonia-N excretion of the spiny lobster Sagmariasus verreauxi during ontogeny. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 166, 191–198, http://doi.org/10.1016/j.cbpa.2013.06.003 (2013).
Briceño, F. A., Polymeropoulos, E. T., Fitzgibbon, Q. P., Dambacher, J. M. & Pecl, G. T. Changes in metabolic rate of spiny lobster under predation risk. Mar. Ecol. Prog. Ser. 598, 71–84, http://doi.org/10.3354/meps12644 (2018).
Svendsen, M. B. S., Bushnell, P. G. & Steffensen, J. F. Design and setup of intermittent-flow respirometry system for aquatic organisms. J. Fish Biol. 88, 26–50, http://doi.org/10.1111/jfb.12797 (2016).
Clark, T. D., Sandblom, E. & Jutfelt, F. Aerobic scope measurements of fishes in an era of climate change: respirometry, relevance and recommendations. J. Exp. Biol. 216, 2771–2782, http://doi.org/10.1242/jeb.084251 (2013).
R: A language and environment for statistical computing. (Vienna, Austria, 2021).
Rstudio: Integrated development environment for R. (Boston, MA, USA, 2021).
Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, http://doi.org/http://hdl.handle.net/10.18637/jss.v067.i01 (2015).
Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. lmerTest package: tests in linear mixed effects models. J. Stat. Softw. 82, 1–26, http://doi.org/10.18637/jss.v082.i13 (2017).
emmeans: Estimated Marginal Means, aka Least-Squares Means. v. 1.6.2-1 (2021).

No competing interests reported.

Download PDF

Editorial decision: Major revision
10 Nov, 2021
Reviews received at journal
25 Sep, 2021
Reviewers agreed at journal
15 Sep, 2021
Reviewers invited by journal
15 Sep, 2021
Editor assigned by journal
15 Sep, 2021
Editor invited by journal
27 Aug, 2021
Submission checks completed at journal
26 Aug, 2021
First submitted to journal
20 Aug, 2021

You are reading this latest preprint version

Metabolic Plasticity Improves Lobster´s Resilience to Ocean Warming but Not to Climate-driven Novel Species Interactions

Status:

Version 1

Abstract

Figures

Introduction

Lobsters in a warming and range-shift hotspot

Results

Thermal plasticity of aerobic metabolism

Anaerobic escape performance

Resident versus range-shifting lobster

Discussion

Metabolic plasticity

Anaerobic escape performance

Resident versus range shifting lobsters

Conclusion

Methods

Animals

Temperature acclimation

Metabolic rate measurements

Data and statistical analysis

Declarations

Acknowledgements

Funding

Data Availability

Competing interests

Author contributions

References

Additional Declarations

Supplementary Files

Status:

Version 1