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

Proceedings of the Royal Society B: Biological Sciences

Volumn 282, Issue 1802, 2015, Pages

  Glazier, Douglas S ^a   Hirst, Andrew G ^b,c   Atkinson, David ^d  

^a JUNIATA COLLEGE   (United States)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^d UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Aquatic invertebrates; Body shape; Metabolic scaling; Ontogeny; Resource transport networks; Surface area

Indexed keywords

AQUATIC ORGANISM; BODY MASS; BODY SHAPE; BODY SIZE; INVERTEBRATE; METABOLISM; ONTOGENY;

ANIMALIA; INVERTEBRATA;

ANIMAL; AQUATIC SPECIES; BODY SIZE; BODY WEIGHT; ENERGY METABOLISM; GROWTH, DEVELOPMENT AND AGING; INVERTEBRATE; METABOLISM;

ANIMALS; AQUATIC ORGANISMS; BODY SIZE; BODY WEIGHT; ENERGY METABOLISM; INVERTEBRATES;

EID: 84922363304     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2014.2302     Document Type: Article

References (54)

1. West GB, Brown JH, Enquist BJ. 1997 A general model for the origin of allometric scaling laws in biology. Science 276, 122-126. (doi:10.1126/ science.276.5309.122)
2. Banavar JR, Moses ME, Brown JH, Damuth J, Rinaldo A, Sibly RM, Maritan A. 2010 A general basis for quarter-power scaling in animals. Proc. Natl Acad. Sci. USA 107, 15 816-15 820. (doi:10. 1073/pnas.1009974107)
3. Riisgård HU. 1998 No foundation of a '3/4 power scaling law' for respiration in biology. Ecol. Lett. 1, 71-73. (doi:10.1046/j.1461-0248.1998.00020.x)
4. Glazier DS. 2005 Beyond the '3/4-power law': variation in the intra- and interspecific scaling of metabolic rate in animals. Biol. Rev. 80, 611-662. (doi:10.1017/S1464793105006834)
5. Czarnołeski M, Kozłowski J, Dumiot G, Bonnet J-C, Mallard J, DuPont-Nivet M. 2008 Scaling of metabolism in Helix aspersa snails: changes through ontogeny and response to selection for increased size. J. Exp. Biol. 211, 391-399. (doi:10.1242/jeb.013169)
6. Peng Y, Niklas KJ, Reich PB, Sun S. 2010 Ontogenetic shift in the scaling of dark respiration with whole-plant mass in seven shrub species. Funct. Ecol. 24. 502-512. (doi:10.1111/j.1365- 2435.2009.01667.x)
7. Kutschera U, Niklas KJ. 2011 Ontogenetic changes in the scaling of cellular respiration with respect to size among sunflower seedlings. Plant Signal. Behav. 6, 72-76. (doi:10.4161/psb.6.1.14001)
8. Hirst AG, Glazier DS, Atkinson D. 2014 Body shape shifting during growth permits tests that distinguish between competing geometric theories of metabolic scaling. Ecol. Lett. 17, 1274-1281. (doi:10.1111/ele.12334)
9. Darveau C-A, Suarez RK, Andrews RD, Hochachka PW. 2002 Allometric cascade as a unifying principle of body mass effects on metabolism. Nature 417, 166-170. (doi:10.1038/417166a)
10. Hofmeyr JHS, Rohwer JM. 2011 Supply-demand analysis: a framework for exploring the regulatory design of metabolism. Methods Enzymol. 500, 533-554. (doi:10.1016/B978-0-12-385118-5. 00025-6)
11. Glazier DS. In press. Is metabolic rate a universal 'pacemaker' for biological processes? Biol. Rev. (doi:10.1111/brv.12115)
12. Glazier DS. 2010 A unifying explanation for diverse metabolic scaling in animals and plants. Biol. Rev. 85, 111-138. (doi:10.1111/j.1469-185X.2009. 00095.x)
13. Callier V, Nijhout HF. 2012 Supply-side constraints are insufficient to explain the ontogenetic scaling of metabolic rate in the tobacco hornworm, Manduca sexta. PLoS ONE 7, e45455. (doi:10.1371/journal. pone.0045455)
14. Rubner M. 1883 Über den Einfluss der Körpergrösse auf Stoff- und Kraftwechsel. Zeit. Biol. 19, 535-562.
15. Okie JG. 2013 General models for the spectra of surface area scaling strategies of cells and organisms: fractality, geometric dissimilitude, and internalization. Am. Nat. 181, 421-439. (doi:10. 1086/669150)
16. West GB, Brown JH, Enquist BJ. 1999 The fourth dimension of life: fractal geometry and allometric scaling of organisms. Science 284, 1677-1679. (doi:10.1126/science.284.5420.1677)
17. Dodds PS. 2010 Optimal form of branching supply and collection networks. Phys. Rev. Lett. 104, 048702. (doi:10.1103/PhysRevLett.104.048702)
18. Kooijman SALM. 2010 Dynamic energy budget theory for metabolic organization. Cambridge, UK: Cambridge University Press.
19. Maino JL, Kearney MR, Nisbet RM, Kooijman SALM. 2014 Reconciling theories of metabolic scaling. J. Anim. Ecol. 83, 20-29. (doi:10.1111/1365-2656. 12085)
20. Savage VM, Deeds EJ, Fontana W. 2008 Sizing up allometric scaling theory. PLoS Comp. Biol. 4, e1000171. (doi:10.1371/journal.pcbi.1000171)
21. Price CA et al. 2012 Testing the metabolic theory of ecology. Ecol. Lett. 15, 1465-1474. (doi:10.1111/j. 1461-0248.2012.01860.x)
22. Kleiber M. 1932 Body size and metabolism. Hilgardia 6, 315-353. (doi:10.3733/hilg. v06n11p315)
23. Glazier DS, Butler EM, Lombardi SA, Deptola TJ, Reese AJ, Satterthwaite EV. 2011 Ecological effects on metabolic scaling: amphipod responses to fish predators in freshwater springs. Ecol. Monogr. 81, 599-618. (doi:10.1890/11-0264.1)
24. Kearney MR, White CR. 2012 Testing metabolic theories. Am. Nat. 180, 546-565. (doi:10.1086/ 667860)
25. Zeuthen E. 1953 Oxygen uptake as related to body size in organisms. Q. Rev. Biol. 28, 1-12. (http:// www.jstor.org/stable/2810299)
26. Kinoshita J, Hiromi J, Kadota S. 1997 Do respiratory metabolic rates of the scyphomedusa Aurelia aurita scale isometrically throughout ontogeny in a sexual generation? Hydrobiologia 347, 51-55. (doi:10. 1023/A:1002942806113)
27. Svetlichny LS, Abolmasova GI, Hubareva ES, Finenko GA, Bat L, Kideys AE. 2004 Respiration rates of Beroe ovata in the Black Sea. Mar. Biol. 145, 585-593. (doi:10.1007/s00227-004-1336-4)
28. Hirst AG. 2012 Intra-specific scaling of mass to length in pelagic animals: ontogenetic shape change and its implications. Limnol. Oceanogr. 57, 1579-1590. (doi:10.4319/lo.2012.57.5.1579)
29. Glazier DS. 2013 Log-transformation is useful for examining proportional relationships in allometric scaling. J. Theor. Biol. 334, 200-203. (doi:10.1016/ j.jtbi.2013.06.017)
30. Jensen MA, Fitzgibbon QP, Carter CG, Adams LR. 2013 Effect of body mass and activity on the metabolic rate and ammonia-N excretion of the spiny lobster Sagmariasus verreauxi during ontogeny. Comp. Biochem. Physiol. A 166, 191-198. (doi:10.1016/j.cbpa.2013.06.003)
31. Jensen MA, Fitzgibbon QP, Carter CG, Adams LR. 2013 The effect of stocking density on growth, metabolism and ammonia-N excretion during larval ontogeny of the spiny lobster Sagmariasus verreauxi. Aquaculture 376-379, 45-53. (doi:10. 1016/j.aquaculture.2012.10.033)
32. Cumming G. 2008 Inference by eye: reading the overlap of independent confidence intervals. Stat. Med. 28, 205-220. (doi:10.1002/ sim.3471)
33. DeLong JP, Okie JG, Moses ME, Sibly RM, Brown JH. 2010 Shifts in metabolic scaling, production and efficiency across major evolutionary transitions of life. Proc. Natl Acad. Sci. USA 107, 12 941-12 945. (doi:10.1073/pnas.1007783107)
34. Reiber CL, McGaw IJ. 2009 A review of the 'open' and 'closed' circulatory systems: new terminology for complex invertebrate circulatory systems in light of current findings. Int. J. Zool. 2009, 301284. (doi:10.1155/2009/301284)
35. McMahon BR, Wilkens JL, Smith PJS. 2011 Invertebrate circulatory systems. Compr. Physiol. 2011, 931-1008. (doi:10.1002/cphy. cp130213)
36. Bokma F. 2004 Evidence against universal metabolic allometry. Funct. Ecol. 18, 184-187. (doi:10.1111/j. 0269-8463.2004.00817.x)
37. White CR, Phillips NF, Seymour RS. 2006 The scaling and temperature dependence of vertebrate metabolism. Biol. Lett. 2, 125-127. (doi:10.1098/rsbl.2005.0378)
38. Glazier DS. 2008 Effects of metabolic level on the body-size scaling of metabolic rate in birds and mammals. Proc. R. Soc. B 275, 1405-1410. (doi:10. 1098/rspb.2008.0118)
39. Killen SS, Atkinson D, Glazier DS. 2010 The intraspecific scaling of metabolic rate with body mass in fishes depends on lifestyle and temperature. Ecol. Lett. 13, 184-193. (doi:10.1111/ j.1461-0248.2009.01415.x)
40. Manahan DT. 1990 Adaptations by invertebrate larvae for nutrient acquisition from seawater. Am. Zool. 30, 147-160. (doi:10.1093/icb/30.1.147)
41. Haond C, Charmantier G, Flik G, Bonga SE. 2001 Identification of respiratory and ion-transporting epithelia in the phyllosoma larvae of the slipper lobster Scyllarus arctus. Cell Tissue Res. 305, 445-455. (doi:10.1007/s004410100405)
42. Rodriguez Souza JC, Strüssmann CA, Takashima F, Satoh H, Sekine S, Shima Y, Matsuda H. 2010 Oral and integumental uptake of free exogenous glycine by the Japanese spiny lobster Panulirus japonicas phyllosoma larvae. J. Exp. Biol. 213, 1859-1867. (doi:10.1242/jeb.040030)
43. Gomme J. 2001 Transport of exogenous organic substances by invertebrate integuments: the field revisited. J. Exp. Zool. 289, 254-265. (doi:10.1002/ 1097-010X(20010401/30)289:4,254::AID-JEZ6.3. 0.CO;2-F)
44. White CR, Seymour RS. 2005 Sample size and mass range effects on the allometric exponent of basal metabolic rate. Comp. Biochem. Physiol. A 142, 74-78. (doi:10.1016/j.cbpa.2005.07.013)
45. Moses ME, Hou C, Woodruff WH, West GB, Nekola JC, Zuo W, Brown JH. 2008 Revisiting a model of ontogenetic growth: estimating model parameters from theory and data. Am. Nat. 171, 632-645. (http://www.jstor.org/stable/10.1086/587073)
46. Gambill M, Peck MA. 2014 Respiration rates of the polyps of four jellyfish species: potential thermal triggers and limits. J. Exp. Mar. Biol. Ecol. 459, 17-22. (doi:10.1016/j.jembe.2014.05.005)
47. Hamburger K, Mohlenberg F, Randlov A, Riisgård HU. 1983 Size, oxygen consumption and growth in the mussel Mytilus edulis. Mar. Biol. 75, 303-306. (doi:10.1007/BF00406016)
48. Glazier DS. 2014 Metabolic scaling in complex living systems. Systems 2, 451-540. (doi:10.3390/ systems2040451)
49. Glazier DS. 2006 The 3/4-power law is not universal: evolution of isometric, ontogenetic metabolic scaling in pelagic animals. Bioscience 56, 325-332. (doi:10. 1641/0006-3568(2006)56[325:TPLINU]2.0.CO;2)
50. Hirst AG, Forster J. 2013 When growth models are not universal: evidence from marine invertebrates. Proc. R. Soc. B 280, 20131546. (doi:10.1098/rspb. 2013.1546)
51. McEdward LR. 1984 Morphometric and metabolic analysis of the growth and form of an echinopluteus. J. Exp. Mar. Biol. Ecol. 82, 259-287. (doi:10.1016/0022-0981(84)90109-6)
52. Seibel BA. 2007 On the depth and scale of metabolic rate variation: scaling of oxygen consumption rates and enzymatic activity in the Class Cephalopoda (Mollusca). J. Exp. Biol. 210, 1-11. (doi:10.1242/jeb.02588)
53. Post JR, Lee JA. 1996 Metabolic ontogeny of teleost fishes. Can. J. Fish. Aquat. Sci. 53, 910-923. (doi:10.1139/f95-278)
54. Glover CN, Bucking C, Wood CM. 2013 The skin of fish as a transport epithelium: a review. J. Comp. Physiol. B 183, 877-891. (doi:10.1007/s00360-013-0761-4)