Shape shifting predicts ontogenetic changes in metabolic scaling in diverse aquatic invertebrates

Metabolism fuels all biological activities, and thus understanding its variation is fundamentally important. Much of this variation is related to body size, which is commonly believed to follow a 3/4-power scaling law. However, during ontogeny, many kinds of animals and plants show marked shifts in metabolic scaling that deviate from 3/4-power scaling predicted by general models. Here, we show that in diverse aquatic invertebrates, ontogenetic shifts in the scaling of routine metabolic rate from near isometry (bR = scaling exponent approx. 1) to negative allometry (bR < 1), or the reverse, are associated with significant changes in body shape (indexed by bL = the scaling exponent of the relationship between body mass and body length). The observed inverse correlations between bR and bL are predicted by metabolic scaling theory that emphasizes resource/waste fluxes across external body surfaces, but contradict theory that emphasizes resource transport through internal networks. Geometric estimates of the scaling of surface area (SA) with body mass (bA) further show that ontogenetic shifts in bR and bA are positively correlated. These results support new metabolic scaling theory based on SA influences that may be applied to ontogenetic shifts in bR shown by many kinds of animals and plants.

[1]  H. Satoh,et al.  Oral and integumental uptake of free exogenous glycine by the Japanese spiny lobster Panulirus japonicus phyllosoma larvae , 2010, Journal of Experimental Biology.

[2]  J. Wilkens,et al.  Invertebrate Circulatory Systems , 2011 .

[3]  Peter Sheridan Dodds,et al.  Optimal form of branching supply and collection networks. , 2009, Physical review letters.

[4]  I. McGaw,et al.  A Review of the “Open” and “Closed” Circulatory Systems: New Terminology for Complex Invertebrate Circulatory Systems in Light of Current Findings , 2009 .

[5]  H. U. Riisgård,et al.  Size, oxygen consumption and growth in the mussel Mytilus edulis , 1983 .

[6]  D. S. Glazier,et al.  The 3/4-Power Law Is Not Universal: Evolution of Isometric, Ontogenetic Metabolic Scaling in Pelagic Animals , 2006 .

[7]  Q. Fitzgibbon,et al.  Effect of body mass and activity on the metabolic rate and ammonia-N excretion of the spiny lobster Sagmariasus verreauxi during ontogeny. , 2013, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[8]  D. S. Glazier Log-transformation is useful for examining proportional relationships in allometric scaling. , 2013, Journal of theoretical biology.

[9]  Sara A. Lombardi,et al.  Ecological effects on metabolic scaling: amphipod responses to fish predators in freshwater springs , 2011 .

[10]  M. Rubner,et al.  Ueber den Einfluss der Körpergrösse auf Stoff- und Kraftwechsel , 1883 .

[11]  David Atkinson,et al.  The intraspecific scaling of metabolic rate with body mass in fishes depends on lifestyle and temperature. , 2010, Ecology letters.

[12]  J. Hiromi,et al.  Do respiratory metabolic rates of the scyphomedusa Aurelia aurita scale isometrically throughout ontogeny in a sexual generation? , 1997, Hydrobiologia.

[13]  Q. Fitzgibbon,et al.  The effect of stocking density on growth, metabolism and ammonia–N excretion during larval ontogeny of the spiny lobster Sagmariasus verreauxi , 2013 .

[14]  J. Rohwer,et al.  Supply-demand analysis a framework for exploring the regulatory design of metabolism. , 2011, Methods in enzymology.

[15]  Craig R. White,et al.  Testing Metabolic Theories , 2012, The American Naturalist.

[16]  B. Seibel On the depth and scale of metabolic rate variation: scaling of oxygen consumption rates and enzymatic activity in the Class Cephalopoda (Mollusca) , 2007, Journal of Experimental Biology.

[17]  A. Kideys,et al.  Respiration rates of Beroe ovata in the Black Sea , 2004 .

[18]  D. Manahan Adaptations by Invertebrate Larvae for Nutrient Acquisition from Seawater , 1990 .

[19]  A. Hirst Intraspecific scaling of mass to length in pelagic animals: Ontogenetic shape change and its implications , 2012 .

[20]  Melanie E. Moses,et al.  Shifts in metabolic scaling, production, and efficiency across major evolutionary transitions of life , 2010, Proceedings of the National Academy of Sciences.

[21]  Viviane Callier,et al.  Supply-Side Constraints Are Insufficient to Explain the Ontogenetic Scaling of Metabolic Rate in the Tobacco Hornworm, Manduca sexta , 2012, PloS one.

[22]  F. Bokma Evidence against universal metabolic allometry , 2004 .

[23]  R. Peters The Ecological Implications of Body Size , 1983 .

[24]  J. Okie General Models for the Spectra of Surface Area Scaling Strategies of Cells and Organisms: Fractality, Geometric Dissimilitude, and Internalization , 2013, The American Naturalist.

[25]  M. Kleiber Body size and metabolism , 1932 .

[26]  C. R. White,et al.  Sample size and mass range effects on the allometric exponent of basal metabolic rate. , 2005, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[27]  D. S. Glazier,et al.  Body shape shifting during growth permits tests that distinguish between competing geometric theories of metabolic scaling. , 2014, Ecology letters.

[28]  J. Lee,et al.  Metabolic ontogeny of teleost fishes , 1996 .

[29]  C. Wood,et al.  The skin of fish as a transport epithelium: a review , 2013, Journal of Comparative Physiology B.

[30]  D. S. Glazier Is metabolic rate a universal ‘pacemaker’ for biological processes? , 2015, Biological reviews of the Cambridge Philosophical Society.

[31]  James H. Brown,et al.  The fourth dimension of life: fractal geometry and allometric scaling of organisms. , 1999, Science.

[32]  Eric J. Deeds,et al.  Sizing Up Allometric Scaling Theory , 2008, PLoS Comput. Biol..

[33]  Rampal S Etienne,et al.  Testing the metabolic theory of ecology. , 2012, Ecology letters.

[34]  Michael R Kearney,et al.  Reconciling theories for metabolic scaling. , 2014, The Journal of animal ecology.

[35]  E. Zeuthen Oxygen Uptake as Related to Body Size in Organisms , 1953, The Quarterly Review of Biology.

[36]  Riisgård No foundation of a “3/4 power scaling law” for respiration in biology , 1998 .

[37]  K. Niklas,et al.  Ontogenetic changes in the scaling of cellular respiration with respect to size among sunflower seedlings , 2011, Plant signaling & behavior.

[38]  P. Reich,et al.  Ontogenetic shift in the scaling of dark respiration with whole-plant mass in seven shrub species , 2010 .

[39]  Geoff Cumming,et al.  Inference by eye: Reading the overlap of independent confidence intervals , 2009, Statistics in medicine.

[40]  Raul K. Suarez,et al.  Allometric cascade as a unifying principle of body mass effects on metabolism , 2002, Nature.

[41]  James H. Brown,et al.  A General Model for the Origin of Allometric Scaling Laws in Biology , 1997, Science.

[42]  D. S. Glazier Effects of metabolic level on the body size scaling of metabolic rate in birds and mammals , 2008, Proceedings of the Royal Society B: Biological Sciences.

[43]  Wenyun Zuo,et al.  Revisiting a Model of Ontogenetic Growth: Estimating Model Parameters from Theory and Data , 2008, The American Naturalist.

[44]  A. Hirst,et al.  When growth models are not universal: evidence from marine invertebrates , 2013, Proceedings of the Royal Society B: Biological Sciences.

[45]  Transport of exogenous organic substances by invertebrate integuments: the field revisited. , 2001 .

[46]  M. Peck,et al.  Respiration rates of the polyps of four jellyfish species: Potential thermal triggers and limits , 2014 .

[47]  Douglas S. Glazier,et al.  Metabolic Scaling in Complex Living Systems , 2014, Syst..

[48]  D. S. Glazier,et al.  Beyond the ‘3/4‐power law’: variation in the intra‐and interspecific scaling of metabolic rate in animals , 2005, Biological reviews of the Cambridge Philosophical Society.

[49]  M. Czarnoleski,et al.  Scaling of metabolism in Helix aspersa snails: changes through ontogeny and response to selection for increased size , 2008, Journal of Experimental Biology.

[50]  C. R. White,et al.  The scaling and temperature dependence of vertebrate metabolism , 2006, Biology Letters.

[51]  Bas Kooijman,et al.  Dynamic Energy Budget Theory for Metabolic Organisation , 2005 .

[52]  D. S. Glazier A unifying explanation for diverse metabolic scaling in animals and plants , 2010, Biological reviews of the Cambridge Philosophical Society.

[53]  L. Mcedward Morphometric and metabolic analysis of the growth and form of an echinopluteus , 1984 .

[54]  James H. Brown,et al.  A general basis for quarter-power scaling in animals , 2010, Proceedings of the National Academy of Sciences.

[55]  G. Flik,et al.  Identification of respiratory and ion-transporting epithelia in the phyllosoma larvae of the slipper lobster Scyllarus arctus , 2001, Cell and Tissue Research.