Abstract
The surface area (SA) of organs and cells may vary with temperature, which changes the SA exchange limitation on metabolic flows as well as the influence of temperature on metabolic scaling. The effect of SA change can intensify (when the effect is the same as that of temperature) or compensate for (when the effect is the opposite of that of temperature) the negative effects of temperature on metabolic scaling, which can result in multiple patterns of metabolic scaling with temperature among species. The present study aimed to examine whether metabolic scaling in black carp changes with temperature and to identify the link between metabolic scaling and SA at the organ and cellular levels at different temperatures. The resting metabolic rate (RMR), gill surface area (GSA) and red blood cell (RBC) size of black carp with different body masses were measured at 10 °C and 25 °C, and the scaling exponents of these parameters were compared. The results showed that both body mass and temperature independently affected the RMR, GSA and RBC size of black carp. A consistent scaling exponent of RMR (0.764, 95% CI [0.718–0.809]) was obtained for both temperatures. The RMR at 25 °C was 2.7 times higher than that at 10 °C. At both temperatures, the GSA scaled consistently with body mass by an exponent of 0.802 (95% CI [0.759–0.846]), while RBC size scaled consistently with body mass by an exponent of 0.042 (95% CI [0.010–0.075]). The constant GSA scaling can explain the constant metabolic scaling as temperature increases, as metabolism may be constrained by fluxes across surfaces. The GSA at 10 °C was 1.2 times higher than that at 25 °C, which suggests that the constraints of GSA on the metabolism of black carp is induced by the higher temperature. The RBC size at 10 °C was 1.1 times higher than that at 25 °C. The smaller RBC size (a larger surface-to-volume ratio) at higher temperature suggests an enhanced oxygen supply and a reduced surface boundary limit on bR, which offset the negative effect of temperature on bR.
Highlights
IntroductionThe mechanisms of metabolic scaling have been attributed to the ontogenetic changes in the components of active organs (the organ size theory)
The relationship between the metabolic rate (MR) and body mass (M) of organisms can be expressed as a power-law function, MR = aMb, where a is a constant and b is the scaling exponent
The results showed that both body mass (F = 1,021.04, P < 0.001) and temperature (F = 648.44, P < 0.001) affected the resting metabolic rate (RMR) of black carp, with no significant interaction between body mass and temperature (F = 1.02, P = 0.317)
Summary
The mechanisms of metabolic scaling have been attributed to the ontogenetic changes in the components of active organs (the organ size theory). (Itazawa & Oikawa, 1983; Oikawa, Takemori & Itazawa, 1992), the fractal patterns of resource distributions (the metabolic theory of ecology) (West, Brown & Enquist, 1997; Brown et al, 2004), the limitations on surfaces for mass and/or energy exchange (the surface area (SA) hypothesis) (Rubner, 1883; Okie, 2013), the ontogenetic change in the ratio of cell SA to volume (cell metabolic hypothesis) (Davison, 1955; Kozłowski, Konarzewski & Gawelczyk, 2003; Starostová et al, 2009), and the effects of SA vs the volume-related metabolic processes of organisms mediated by metabolic level (the metabolic level boundaries hypothesis) (Glazier, 2005, 2008, 2009, 2010). It is of interest to investigate whether the changes in SA at the organ and cellular levels affect the metabolic scaling of the whole body of an organism
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