Ecological pressures and the contrasting scaling of metabolism and body shape in coexisting taxa: cephalopods versus teleost fish

Abstract

Metabolic rates are fundamental to many biological processes, and commonly scale with body size with an exponent ( b R ) between 2/3 and 1 for reasons still debated. According to the ‘metabolic-level boundaries hypothesis', b R depends on the metabolic level ( L R ). We test this prediction and show that across cephalopod species intraspecific b R correlates positively with not only L R but also the scaling of body surface area with body mass. Cephalopod species with high L R maintain near constant mass-specific metabolic rates, growth and probably inner-mantle surface area for exchange of respiratory gases or wastes throughout their lives. By contrast, teleost fish show a negative correlation between b R and L R . We hypothesize that this striking taxonomic difference arises because both resource supply and demand scale differently in fish and cephalopods, as a result of contrasting mortality and energetic pressures, likely related to different locomotion costs and predation pressure. Cephalopods with high L R exhibit relatively steep scaling of growth, locomotion, and resource-exchange surface area, made possible by body-shape shifting. We suggest that differences in lifestyle, growth and body shape with changing water depth may be useful for predicting contrasting metabolic scaling for coexisting animals of similar sizes. This article is part of the theme issue ‘Physiological diversity, biodiversity patterns and global climate change: testing key hypotheses involving temperature and oxygen’.

Can shifts in metabolic scaling predict coevolution between diet quality and body size?

“…2017), but current research suggests it may reflect the scaling of selective pressures on life‐history traits (Harrison 2017; Tan et al. 2019). Likewise, it has been suggested that the dimensionality of foraging space (2D or 3D) drives the scaling of consumption rate (Pawar et al.…”

A new framework for growth curve fitting based on the von Bertalanffy Growth Function

“…A 1 12) of O.dioica during ontogenetic growth prompts suggestions about the selective effects on growth of mortality risk in an open-water environment. With no refuges from predators, rapid sustained uptake of resources may be required to reach maturity fast before being consumed 79,80 . The scyphozoan Pelagia noctiluca also exists within a high-mortality pelagic environment but instead exhibits a shallower mass-scaling of biosynthesis potential ( = .…”

“…predation) that exist between benthic and pelagic habitats of aquatic invertebrates may affect the mass-scaling of an organism's uptake of resources. For example, high predation risk throughout ontogeny in the sunlit epipelagic zone, which lacks refuges from predators, may lead to the evolution of steeper mass-scaling of resource uptake, compared with more benthic conditions where invertebrates can reduce predation risk by finding refuge [78][79][80] . The diversity in the mass-scaling of biosynthesis potential makes benthic and pelagic invertebrate species two ideal groups to explore variation in the mass-scaling exponent of biosynthesis potential A ( ) when fitting the VBGF.…”

Effects of gill excision and food deprivation on metabolic scaling in the goldfish Carassius auratus

“…For most teleosts, the scaling exponent of RMR (b R ) ranges between 0.65 and 0.95 (Bokma, 2004;Clarke & Johnston, 1999;Killen, Atkinson, & Glazier, 2010;Luo et al, 2015). Many hypotheses have been proposed to explain allometric scaling and whether the scaling exponent b has a constant value, including the surface area hypothesis (Glazier, Hirst, & Atkinson, 2015;Hirst, Glazier, & Atkinson, 2014;Okie, 2013;Rubner, 1883;Tan, Hirst, Glazier, & Atkinson, 2019), the organ size hypothesis (Itazawa & Oikawa, 1983;Oikawa, Takemori, & Itazawa, 1992), the metabolic theory of ecology (Brown, Gillooly, Allen, Savage, & West, 2004;West, Brown, & Enquist, 1997), the cell metabolism hypothesis (Davison, 1955;Kozłowski, Konarzewski, & Gawelczyk, 2003;Shestopaloff, 2016;Starostová, Konarzewski, Kozłowski, & Kratochvíl, 2013), and the metabolic-level boundaries hypothesis (Glazier, 2005(Glazier, , 2008(Glazier, , 2009(Glazier, , 2010. These hypotheses can partially explain the allometric scaling of MR, but multiple causes may play a role (Glazier, 2014a(Glazier, , 2014b.…”