Gill surface area allometry does not constrain the body mass scaling of maximum oxygen uptake rate in the tidepool sculpin, Oligocottus maculosus

Somo, Derek A.; Chu, Ken H.; Richards, Jeffrey G.

doi:10.1007/s00360-023-01490-9

Cited by 8 publications

(2 citation statements)

References 75 publications

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“…However, for G. maculatus reared in each temperature and oxygen treatment, the scaling exponent for S MMR did not statistically differ from zero, revealing that GSA grows to meet the maximal oxygen requirements of fish independent of their environment. Equivalent results for the tidepool sculpin Oligocottus maculosus across a smaller size range have been reported (Somo et al, 2023). These findings, combined with a significant decrease of MMR scaling exponents in aquatic ectotherms with warming (Rubalcaba et al, 2020), suggest that factors other than the gills may be responsible for any reduction in MMR of larger fish in warmer settings.…”

Section: Does Gsa Meet Metabolic Requirements Through Ontogeny?mentioning

confidence: 67%

Fish gill surface area can keep pace with metabolic oxygen requirements across body mass and temperature

Skeeles,

Clark

2024

Functional Ecology

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Climate warming is driving the maximum attainable size of many fish species to decrease, yet the mechanisms underlying this ‘shrinking’ phenomenon are not well understood. The gill oxygen limitation (GOL) hypothesis is perhaps the most prominent mechanistic proposition, asserting that, as fish grow, the two‐dimensional gill surface area (GSA) progressively fails to supply enough oxygen to support the continued growth of the three‐dimensional body—a process exacerbated by increased metabolism associated with warming. However, these ideas have been hotly debated owing to limited empirical understanding of how GSA develops with respect to a fish's body mass and oxygen requirements. For the first time, we addressed this knowledge gap by rearing Galaxias maculatus for 5 months at normal (15°C) and elevated (20°C) summer temperatures, with (hyperoxia) or without (normoxia) supplementary oxygen. Quantifying individual metabolic rate and GSA traits across body sizes encompassing most of the species' ontogeny, we found little evidence for a change in the proportion of GSA available per unit of metabolic rate (termed the S metric) and no improvements under hyperoxia. Importantly, at the elevated temperature where gill oxygen limitation should be most pronounced, the S metric did not change across body mass in either oxygen treatment (allometric exponents were no different from 0). These results indicate that the gills can grow in ways that support an individual's oxygen requirements, contrasting with the suggestion that size reductions of fish in response to climate warming are driven by an insurmountable geometric constraint at the gills. Read the free Plain Language Summary for this article on the Journal blog.

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Section: Does Gsa Meet Metabolic Requirements Through Ontogeny?mentioning

confidence: 67%

Fish gill surface area can keep pace with metabolic oxygen requirements across body mass and temperature

Skeeles,

Clark

2024

Functional Ecology

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“…For example, GOL assumes that the scaling of GSA is constrained by surface area to volume ratios, which ultimately constrain metabolic rate and growth. In contrast, critics argue that there is substantial evidence that GSA scales proportional to metabolic rate in order to meet metabolic demands ( Lefevre et al, 2017 , 2018 ; Somo et al, 2023 ; Prinzing et al, 2023 ) and that gills can be highly plastic and dynamic structures such that GSA can acclimate to changes in oxygen demand such as those induced by climate warming ( Wegner and Farrell, 2023 ). Despite such concerns, estimates of climate impacts on fisheries have been generated by models based on GOL assumptions ( Cheung et al, 2013 ) as well as integrated into International Union for Conservation of Nature (IUCN) climate change biological impact assessments ( Cheung and Pauly, 2016 ).…”

Section: Introductionmentioning

confidence: 99%

Smaller body size under warming is not due to gill-oxygen limitation in a cold-water salmonid

Lonthair,

Wegner,

Cheng

et al. 2024

Journal of Experimental Biology

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Declining body size in fishes and other aquatic ectotherms associated with anthropogenic climate warming has significant implications for future fisheries yields, stock assessments and aquatic ecosystem stability. One proposed mechanism seeking to explain such body-size reductions, known as the gill oxygen limitation (GOL) hypothesis, has recently been used to model future impacts of climate warming on fisheries but has not been robustly empirically tested. We used brook trout (Salvelinus fontinalis), a fast-growing, cold-water salmonid species of broad economic, conservation and ecological value, to examine the GOL hypothesis in a long-term experiment quantifying effects of temperature on growth, resting metabolic rate (RMR), maximum metabolic rate (MMR) and gill surface area (GSA). Despite significantly reduced growth and body size at an elevated temperature, allometric slopes of GSA were not significantly different than 1.0 and were above those for RMR and MMR at both temperature treatments (15°C and 20°C), contrary to GOL expectations. We also found that the effect of temperature on RMR was time-dependent, contradicting the prediction that heightened temperatures increase metabolic rates and reinforcing the importance of longer-term exposures (e.g. >6 months) to fully understand the influence of acclimation on temperature–metabolic rate relationships. Our results indicate that although oxygen limitation may be important in some aspects of temperature–body size relationships and constraints on metabolic supply may contribute to reduced growth in some cases, it is unlikely that GOL is a universal mechanism explaining temperature–body size relationships in aquatic ectotherms. We suggest future research focus on alternative mechanisms underlying temperature–body size relationships, and that projections of climate change impacts on fisheries yields using models based on GOL assumptions be interpreted with caution.

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Whether hypoxia tolerance improved after short-term fasting is closely related to phylogeny but not to foraging mode in freshwater fish species

Huang,

Liu,

Zhang

et al. 2024

J Comp Physiol B

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Gill surface area allometry does not constrain the body mass scaling of maximum oxygen uptake rate in the tidepool sculpin, Oligocottus maculosus

Cited by 8 publications

References 75 publications

Fish gill surface area can keep pace with metabolic oxygen requirements across body mass and temperature

Fish gill surface area can keep pace with metabolic oxygen requirements across body mass and temperature

Smaller body size under warming is not due to gill-oxygen limitation in a cold-water salmonid

Whether hypoxia tolerance improved after short-term fasting is closely related to phylogeny but not to foraging mode in freshwater fish species

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