Feeding provides the necessary energy to fuel all fitness-related processes including activity, growth and reproduction. Nevertheless, prey consumption and digestive processes can have physical and ...physiological trade-offs with other critical functions, many of which are not clearly understood. Using an ambush predator, barramundi (Lates calcarifer), fed meals ranging 0.6–3.4% of body mass, we examined interrelations between meal size, growth efficiency and surplus aerobic metabolic capacity (aerobic scope, AS). Large meals required a greater absolute investment of energy to process (a larger so-called specific dynamic action, SDA), but the percentage of digestible meal energy required in the SDA response (SDA coefficient) decreased with increasing meal size. Combined with the findings that growth rate and growth efficiency also increased with food intake, our results demonstrate that it is energetically advantageous for fish to select large prey. However, following a large meal, SDA processes occupied up to 77% of the available AS, indicating that other oxygen-demanding activities like swimming may be compromised while large meals are processed. This trade-off between meal size and AS suggests that fishes like barramundi would benefit from regulating prey size based on imminent requirements and threats.
Temperature has a dramatic effect on the physiology of ectothermic animals, impacting most of their biology. When temperatures increase above optimal for an animal, their growth gradually decreases. ...The main mechanism behind this growth rate reduction is unknown.
Here, we suggest the ‘aerobic scope protection’ hypothesis as a mechanistic explanation for the reduction in growth.
After a meal, metabolic rate, and hence oxygen consumption rate, transiently increase in a process called specific dynamic action (SDA). At warmer temperatures, the SDA response usually becomes temporally compressed, leading to a higher peak oxygen consumption rate. This peak in oxygen consumption rate risks taking up much of the animal's aerobic scope (the difference between resting and maximum rates of oxygen consumption), which would leave little residual aerobic scope for other aerobic functions.
We propose that water‐breathing ectothermic animals will protect their postprandial residual aerobic scope by reducing meal sizes in order to regulate the peak SDA response during times of warming, leading to reductions in growth.
This hypothesis is consistent with the published literature on fishes, and we provide predictions that can be tested.
A free Plain Language Summary can be found within the Supporting Information of this article.
A free Plain Language Summary can be found within the Supporting Information of this article.
Aerobic scope represents an animal’s capacity to increase its aerobic metabolic rate above maintenance levels (i.e. the difference between standard (SMR) and maximum (MMR) metabolic rates). Aerobic ...scope data can be presented in absolute or factorial terms (AAS or FAS, respectively). However, the robustness of these calculations to noise or variability in measures of metabolic rate can influence subsequent interpretations of patterns in the data. We explored this issue using simple models and we compared the predictions from these models to experimental data from the literature. First, we investigated the robustness of aerobic scope calculations as a function of varying SMR when MMR is fixed, and vice versa. While FAS is unexpectedly robust to variability in SMR, even in species with low aerobic scopes, AAS is less sensitive to variation in SMR than is FAS. However, where variation in MMR is the main concern, FAS is more robust than AAS. Our findings highlight the equal importance of minimising variability in MMR, rather than just the variability in SMR, to obtain robust aerobic scope estimates. Second, we analysed metabolic rate accounting for locomotor speed and body mass for swimming fish. The interactions among these factors in relation to AAS and FAS are complex and the appropriate metric is dependent on the specific eco-physiological context of the research question. We conclude with qualified recommendations for using and interpreting AAS and FAS.
Metabolic rate (MR) usually changes (scales) out of proportion to body mass (BM) as MR = aBMb, where a is a normalisation constant and b is the scaling exponent that reflects how steep this change ...is. This scaling relationship is fundamental to biology, but over a century of research has provided little consensus on the value of b, and why it appears to vary among taxa and taxonomic levels. By analysing published data on fish and taking an individual-based approach to metabolic scaling, I show that variation in growth of fish under naturally restricted food availability can explain variation in within-individual (ontogenetic) b for standard (maintenance) metabolic rate (SMR) of brown trout (Salmo trutta), with the fastest growers having the steepest metabolic scaling (b ≈ 1). Moreover, I show that within-individual b can vary much more widely than previously assumed from work on different individuals or different species, from -1 to 1 for SMR among individual brown trout. The negative scaling of SMR for some individuals was caused by reductions in metabolic rate in a food limited environment, likely to maintain positive growth. This resulted in a mean within-individual b for SMR that was significantly lower than the across-individual ("static") b, a difference that also existed for another species, cunner (Tautogolabrus adspersus). Interestingly, the wide variation in ontogenetic b for SMR among individual brown trout did not exist for maximum (active) metabolic rate (MMR) of the same fish, showing that these two key metabolic traits (SMR and MMR) can scale independently of one another. I also show that across-species ("evolutionary") b for SMR of 134 fishes is significantly steeper (b approaching 1) than the mean ontogenetic b for the brown trout and cunner. Based on these interesting findings, I hypothesise that evolutionary and static metabolic scaling can be systematically different from ontogenetic scaling, and that the steeper evolutionary than ontogenetic scaling for fishes arises as a by-product of natural selection for fast-growing individuals with steep metabolic scaling (b ≈ 1) early in life, where size-selective mortality is high for fishes. I support this by showing that b for SMR tends to increase with natural mortality rates of fish larvae within taxa.
Increased ocean temperatures are causing mass bleaching of anemones and corals in the tropics worldwide. While such heat-induced loss of algal symbionts (zooxanthellae) directly affects anemones and ...corals physiologically, this damage may also cascade on to other animal symbionts. Metabolic rate is an integrative physiological trait shown to relate to various aspects of organismal performance, behaviour and locomotor capacity, and also shows plasticity during exposure to acute and chronic stressors. As climate warming is expected to affect the physiology, behaviour and life history of animals, including ectotherms such as fish, we measured if residing in bleached versus unbleached sea anemones (Heteractis magnifica) affected the standard (i.e. baseline) metabolic rate and behaviour (activity) of juvenile orange-fin anemonefish (Amphiprion chrysopterus). Metabolic rate was estimated from rates of oxygen uptake , and the standard metabolic rate of anemonefish from bleached anemones was significantly higher by 8.2% compared with that of fish residing in unbleached anemones, possibly due to increased stress levels. Activity levels did not differ between fish from bleached and unbleached anemones. As reflects the minimum cost of living, the increased metabolic demands may contribute to the negative impacts of bleaching on important anemonefish life history and fitness traits observed previously (e.g. reduced spawning frequency and lower fecundity).
Environmentally-induced changes in fitness are mediated by direct effects on physiology and behaviour, which are tightly linked. We investigated how predicted ocean warming (OW) and acidification ...(OA) affect key ecological behaviours (locomotion speed and foraging success) and metabolic rate of a keystone marine mollusc, the sea hare Stylocheilus striatus, a specialist grazer of the toxic cyanobacterium Lyngbya majuscula. We acclimated sea hares to OW and/or OA across three developmental stages (metamorphic, juvenile, and adult) or as adults only, and compare these to sea hares maintained under current-day conditions. Generally, locomotion speed and time to locate food were reduced ~1.5- to 2-fold when the stressors (OW or OA) were experienced in isolation, but reduced ~3-fold when combined. Decision-making was also severely altered, with correct foraging choice nearly 40% lower under combined stressors. Metabolic rate appeared to acclimate to the stressors in isolation, but was significantly elevated under combined stressors. Overall, sea hares that developed under OW and/or OA exhibited a less severe impact, indicating beneficial phenotypic plasticity. Reduced foraging success coupled with increased metabolic demands may impact fitness in this species and highlight potentially large ecological consequences under unabated OW and OA, namely in regulating toxic cyanobacteria blooms on coral reefs.
Standard metabolic rate (SMR) and active metabolic rate (AMR) are two fundamental physiological parameters providing the floor and ceiling in aerobic energy metabolism. The total amount of energy ...available within these two parameters confines constitutes the absolute aerobic scope (AAS). Previous studies on fish have found SMR to closely correlate with dominance and position in the social hierarchy, and to be highly repeatable over time when fish were provided an ad libitum diet. In this study we tested the temporal repeatability of individual SMR, AMR and AAS, as well as repeatability of body mass, in young brown trout (Salmo trutta L.) fed a moderately restricted diet (0.5-0.7% fish mass day⁻¹). Metabolism was estimated from measurements of oxygen consumption rate (M(.)(O₂)) and repeatability was evaluated four times across a 15-week period. Individual body mass was highly repeatable across the entire 15 week experimental period whereas residual body-mass-corrected SMR, AMR and AAS showed a gradual loss of repeatability over time. Individual residual SMR, AMR and AAS were significantly repeatable in the short term (5 weeks), gradually declined across the medium term (10 weeks) and completely disappeared in the long term (15 weeks). We suggest that this gradual decline in repeatability was due to the slightly restricted feeding regime. This is discussed in the context of phenotypic plasticity, natural selection and ecology.
Indirect effects of predators can manifest themselves as changes in prey behaviour and physiology. Given that digestion requires energy, it has been suggested that prey will choose to eat smaller ...meals under predation risk to reserve a larger portion of the aerobic metabolic scope they have available for energetically demanding tasks more critical than digestion, such as escape. To test this prediction, we quantified food consumption and growth of juvenile corkwing wrasses (
Symphodus melops
) over 11 days in the presence or absence of a predator (Atlantic cod,
Gadus morhua
). We then quantified behaviour and food consumption of the same wrasses in behavioural arenas with a predator. All food consumption was examined in the context of the aerobic scope that would have been available during the digestive period. Overall, there was no effect of predator exposure on food consumption or growth, yet predator-exposed wrasses were more consistent in their daily food consumption, lending some support to our prediction of prey bet-hedging on meal size under predation risk. The lack of a clear pattern may have resulted from a relatively low percentage of aerobic scope (~ 20–27%) being occupied by digestion, such that fish retained ample capacity for activities other than digestion. In the subsequent behavioural trials, predator-exposed wrasses were more active and spent more time near the cod than predator-naïve wrasses, suggesting the former had habituated to predation threat and were more risk-taking. Our results highlight the complex and often counter-intuitive effects that predator presence can have on prey populations beyond direct consumption.
Significance statement
Predators affect the behaviour of prey species by simply being present in the environment. Such intimidation by predators can change activity patterns of prey and be as important as direct predation for ecosystem dynamics. However, compared to behavioural changes, we know little about how predators indirectly affect prey physiology. We investigated if fish deliberately eat less food when a predator is present, in order to retain sufficient physiological capacity for avoiding a potential attack, on top of the energetically costly process of digesting. While our study confirms that predator encounters reduce prey activity, prey fish appeared to rapidly habituate to predator presence and we did not see reduced food consumption in predator-exposed fish; these were, however, more consistent than unexposed fish in their daily food consumption, suggesting that fish may still be mindful about protecting their aerobic capacity under predation risk.
Organismal metabolic rates (MRs) are the basis of energy and nutrient fluxes through ecosystems. In the marine realm, fishes are some of the most prominent consumers. However, their metabolic demand ...in the wild (field MR FMR) is poorly documented, because it is challenging to measure directly. Here, we introduce a novel approach to estimating the component of FMR associated with voluntary activity (i.e., the field active MR AMRfield). Our approach combines laboratory‐based respirometry, swimming speeds, and field‐based stereo‐video systems to estimate the activity of individuals. We exemplify our approach by focusing on six coral reef fish species, for which we quantified standard MR and maximum MR (SMR and MMR, respectively) in the laboratory, and body sizes and swimming speeds in the field. Based on the relationships between MR, body size, and swimming speeds, we estimate that the activity scope (i.e., the ratio between AMRfield and SMR) varies from 1.2 to 3.2 across species and body sizes. Furthermore, we illustrate that the scaling exponent for AMRfield varies across species and can substantially exceed the widely assumed value of 0.75 for SMR. Finally, by scaling organismal AMRfield estimates to the assemblage level, we show the potential effect of this variability on community metabolic demand. Our approach may improve our ability to estimate elemental fluxes mediated by a critically important group of aquatic animals through a non‐destructive, widely applicable technique.
We know little about the metabolic demand of fishes in the wild. We propose a new approach to estimate active field metabolic rates by combining laboratory‐based respirometry and field‐based stereo‐video systems.
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