A metabolic and body-size scaling framework for parasite within-host abundance, biomass, and energy flux

American Naturalist

Volumn 182, Issue 2, 2013, Pages 234-248

  Hechinger, Ryan F ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Infracommunity; Infrapopulation; Metabolic theory of ecology; Parasite communities; Pathology; Virulence

Indexed keywords

ABUNDANCE; BIOENERGETICS; BIOMASS; BODY SIZE; ENERGY FLUX; HOST-PARASITE INTERACTION; METABOLISM; PARASITISM; PARASITOLOGY; PATHOLOGY; VIRULENCE;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; BIOMASS; BODY SIZE; ENERGY METABOLISM; HOST PARASITE INTERACTION;

ANIMALS; BIOMASS; BODY SIZE; ENERGY METABOLISM; HOST-PARASITE INTERACTIONS; MODELS, BIOLOGICAL;

EID: 84880130031     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/670820     Document Type: Article

References (77)

1. Anderson, R. M., and R. M. May. 1978. Regulation and stability of host-parasite population interactions. 1. Regulatory processes. Journal of Animal Ecology 47:219-247.
2. Arneberg, P., A. Skorping, and A. F. Read. 1998. Parasite abundance, body size, life histories, and the energetic equivalence rule. American Naturalist 151:497-513.
3. Bailey, G. N. A. 1975. Energetics of a host-parasite system: preliminary report. International Journal for Parasitology 5:609-613.
4. Brown, J. H., J. F. Gillooly, A. P. Allen, V. M. Savage, and G. B. West. 2004. Toward a metabolic theory of ecology. Ecology 85:1771-1789.
5. Brown, J. H., R. M. Sibly, and A. Kodric-Brown. 2012. Introduction: metabolism as the basis for a theoretical unification of ecology. Pages 1-6 in R. M. Sibly, J. H. Brown, and A. Kodric-Brown, eds. Metabolic ecology: a scaling approach. Wiley-Blackwell, Chichester.
6. Bush, A. O., and J. C. Holmes. 1986. Intestinal helminths of lesser scaup ducks: an interactive community. Canadian Journal of Zoology 64:142-152.
7. Bush, A. O., K. D. Lafferty, J. M. Lotz, and A. W. Shostak. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83:575-583.
8. Calder, W. A. 1984. Size, function, and life history. Harvard University Press, Cambridge, MA.
9. Carbone, C., and J. L. Gittleman. 2002. A common rule for the scaling of carnivore density. Science 295:2273-2276.
10. Cox, F. E. G. 2001. Concomitant infections, parasites and immune responses. Parasitology 122:S23-S38.
11. Crompton, D. W., and R. R. Whitehead. 1993. Hookworm infections and human iron metabolism. Parasitology 107:S137-S145.
12. Damuth, J. 1981. Population-density and body size in mammals. Nature 290:699-700.
13. Damuth, J. 1987. Interspecific allometry of population-density in mammals and other animals: the independence of body-mass and population energy-use. Biological Journal of the Linnean Society 31: 193-246.
14. De Leo, G. A., and A. P. Dobson. 1996. Allometry and simple epidemic models for microparasites. Nature 379:720-722.
15. DeLong, J. P., J. G. Okie, M. E. Moses, R. M. Sibly, and J. H. Brown. 2010. Shifts in metabolic scaling, production, and efficiency across major evolutionary transitions of life. Proceedings of the National Academy of Sciences of the USA 107:12,941-12,945.
16. DeLong, J. P., and D. A. Vasseur. 2011. A dynamic explanation of size-density scaling in carnivores. Ecology 93:470-476.
17. DeLong, J. P., and D. A. Vasseur. 2012. Size-density scaling in protists and the links between consumer-resource interaction parameters. Journal of Animal Ecology 81:1193-1201.
18. Dobson, A. P. 1985. The population dynamics of competition between parasites. Parasitology 91:317-347.
19. Ernest, S. K. M., B. J. Enquist, J. H. Brown, E. L. Charnov, J. F. Gillooly, V. Savage, E. P. White, et al. 2003. Thermodynamic and metabolic effects on the scaling of production and population energy use. Ecology Letters 6:990-995.
20. Esch, G. W., A. O. Bush, and J. M. Aho, eds. 1990. Parasite communities: patterns and processes. Pages xi, 335. Chapman & Hall, London.
21. George-Nascimento, M., G. Munoz, P. A. Marquet, and R. Poulin. 2004. Testing the energetic equivalence rule with helminth endoparasites of vertebrates. Ecology Letters 7:527-531.
22. Gillooly, J. F., A. P. Allen, and J. H. Brown. 2006. Food-web structure and dynamics: reconciling alternative ecological currencies. Pages 209-222 in M. Pascual and J. A. Dunne, eds. Ecological networks: linking structure to dynamics in food webs. Oxford University Press, Oxford.
23. Gillooly, J. F., J. H. Brown, G. B. West, V. M. Savage, and E. L. Charnov. 2001. Effects of size and temperature on metabolic rate. Science 293:2248-2251.
24. Glazier, D. S. 2005. Beyond the "3/4-power law": variation in the intra-and interspecific scaling of metabolic rate in animals. Biological Reviews 80:611-662.
25. Gotelli, N. J., and G. R. Graves. 1996. Null models in ecology. Smithsonian Institution, Washington, DC.
26. Hechinger, R. 2013. Data from: A metabolic and body-size scaling framework for parasite within-host abundance, biomass, and energy flux. American Naturalist, Dryad Digital Repository, http://dx.doi.org/10.5061/dryad.14nn1.
27. Hechinger, R. F., K. D. Lafferty, A. P. Dobson, J. H. Brown, and A. M. Kuris. 2011. A common scaling rule for the abundance, energetics, and productivity of parasitic and free-living species. Science 333:445-448.
28. Hechinger, R. F., K. D. Lafferty, and A. M. Kuris. 2012. Parasites. Pages 234-247 in R. M. Sibly, J. H. Brown, and A. Kodric-Brown, eds. Metabolic ecology: a scaling approach. Wiley-Blackwell, Chichester.
29. Hemmingsen, A. M. 1960. Energy metabolism as related to body size and respiratory surfaces and its evolution. Reports of the Steno Memorial Hospital and the Nordisk Insulinlaboratorium 9:7-110.
30. Holmes, J. C. 1961. Effects of concurrent infections on Hymenolepis diminuta (Cestoda) and Moniliformis dubius (Acanthocephala). 1.
31. General effects and comparison with crowding. Journal of Parasitology 47:209-216.
32. Holmes, J. C. 1962. Effects of concurrent infections on Hymenolepis dim- inuta (Cestoda) and Moniliformis dubius (Acanthocephala). 2. Effects on growth. Journal of Parasitology 48:87-96.
33. Holmes, J. C., and P.W. Price. 1986. Communities of parasites. Pages 187-213 in J. Kikkawa and D. J. Anderson, eds. Community ecology: pattern and process. Blackwell Scientific, Palo Alto, CA.
34. Isaac, N. J. B., C. Carbone, and B. McGill. 2012. Population and community ecology, Pages 77-85 in R. M. Sibly, J. H. Brown, and A. Kodric-Brown, eds. Metabolic ecology: a scaling approach. Wiley-Blackwell, Chichester.
35. Jackson, D. A., and K. M. Somers. 1991. The spectre of "spurious" correlations. Oecologia (Berlin) 86:147-151.
36. Kleiber, M. 1932. Body size and metabolism. Hilgardia 6:315-353.
37. Krebs, C. J. 1999. Ecological methodology. Addison-Wesley, Menlo Park, CA.
38. Kuris, A. M., and K. D. Lafferty. 2000. Parasite-host modeling meets reality: adaptive peaks and their ecological attributes. Pages 9-26 in R. Poulin, S. Morand, and A. Skorping, eds. Evolutionary biology of host-parasite relationships: theory meets reality. Developments in Animal and Veterinary Sciences. Elsevier, Amsterdam.
39. Lafferty, K. D., and A. M. Kuris. 2002. Trophic strategies, animal diversity and body size. Trends in Ecology and Evolution 17:507-513.
40. Lafferty, K. D., and A. K. Morris. 1996. Altered behavior of parasitized killifish increases susceptibility to predation by bird final hosts. Ecology 77:1390-1397.
41. Lochmiller, R. L., and C. Deerenberg. 2000. Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88:87-98.
42. Makarieva, A. M., V. G. Gorshkov, B.-L. Li, S. L. Chown, P. B. Reich, and V. M. Gavrilov. 2008. Mean mass-specific metabolic rates are strikingly similar across life's major domains: evidence for life's metabolic optimum. Proceedings of the National Academy of Sciences of the USA 105:16,994-16,999.
43. Marquet, P. A., F. A. Labra, and B. A. Maurer. 2004. Metabolic ecology: linking individuals to ecosystems. Ecology 85:1794-1796.
44. Marquet, P. A., R. A. Quinones, S. Abades, F. Labra, M. Tognelli, M. Arim, and M. Rivadeneira. 2005. Scaling and power-laws in ecological systems. Journal of Experimental Biology 208:1749-1769.
45. May, R. M., and R. M. Anderson. 1979. Population biology of infectious diseases: pt. II. Nature 280:455-461.
46. Molnár, P. K., S. J. Kutz, B. M. Hoar, and A. P. Dobson. 2013. Metabolic approaches to understanding climate change impacts on seasonal host-macroparasite dynamics. Ecology Letters 16:9-21.
47. Morand, S., and R. Poulin. 2002. Body size-density relationships and species diversity in parasitic nematodes: patterns and likely processes. Evolutionary Ecology Research 4:951-961.
48. Munger, J. C., and W. H. Karasov. 1994. Costs of bot fly infection in white-footed mice: energy and mass flow. Canadian Journal of Zoology 72:166-173.
49. Muñoz, G., and T. H. Cribb. 2005. Infracommunity structure of parasites of Hemigymnus melapterus (Pisces: Labridae) fromLizard Island, Australia: the importance of habitat and parasite body size. Journal of Parasitology 91:38-44.
50. Munoz, S. A., and M. George-Nascimento. 2008. The effect of Anonchocephalus chilensis Riggenbach (Eucestoda: Bothriocephalidea) on infracommunity patterns in Genypterus maculatus Tschudi (Osteichthyes: Ophidiidae). Journal of Helminthology 82:221-226.
51. Nee, S., A. F. Read, J. J. D. Greenwood, and P. H. Harvey. 1991. The relationship between abundance and body size in British birds. Nature 351:312-313.
52. Noble, E. R. 1974. Three avenues to ecologic research on parasitic protozoa. Journal of Protozoology 21:1-4.
53. Pearson, K. 1897. Mathematical contributions to the theory of evolution: on a form of spurious correlation which may arise when indices are used in the measurement of organs. Proceedings of the Royal Society of London 60:489-498.
54. Peters, R. H. 1983. The ecological implications of body size. Cambridge Studies in Ecology. Cambridge, Cambridge University Press.
55. Petney, T. N., and R. H. Andrews. 1998. Multiparasite communities in animals and humans: frequency, structure and pathogenic significance. International Journal for Parasitology 28:377-393.
56. Pichyangkul, S., P. Saengkrai, and H. K. Webster. 1994. Plasmodium falciparum pigment induces monocytes to release high levels of tumor necrosis factor-a and interleukin-1b. American Journal of Tropical Medicine and Hygiene 51:430-435.
57. Poulin, R. 1998. Evolutionary ecology of parasites: from individuals to communities. Chapman & Hall, London.
58. Poulin, R., and M. George-Nascimento. 2007. The scaling of total parasite biomass with host body mass. International Journal for Parasitology 37:359-364.
59. Poulin, R., and S. Morand. 2000. Parasite body size and interspecific variation in levels of aggregation among nematodes. Journal of Parasitology 86:642-647.
60. Price, P. W. 1990. Host populations as resources defining parasite community organization. Pages 21-40 in G. W. Esch, A. O. Bush, and J. M. Aho, eds. Parasite communities: patterns and processes. Chapman & Hall, London.
61. Quinn, G. P., and M. J. Keough. 2002. Experimental design and data analysis for biologists. Cambridge University Press, Cambridge.
62. Robar, N., D. L. Murray, and G. Burness. 2011. Effects of parasites on host energy expenditure: the resting metabolic rate stalemate. Canadian Journal of Zoology 89:1146-1155.
63. Roberts, L. S. 2000. The crowding effect revisited. Journal of Parasitology 86:209-211.
64. Robinson, W. R., R. H. Peters, and J. Zimmermann. 1983. The effects of body size and temperature on metabolic rate of organisms. Canadian Journal of Zoology 61:281-288.
65. Rohde, K. 2005. Nonequilibrium ecology: ecology, biodiversity, and conservation. Cambridge; New York, Cambridge University Press.
66. Rohde, K., C. Hayward, M. Heap, and D. Gosper. 1994. A tropical assemblage of ectoparasites: gill and head parasites of Lethrinus miniatus (Teleostei, Lethrinidae). International Journal for Parasitology 24:1031-1053.
67. Sall, J. 1990. Leverage plots for general linear hypotheses. American Statistician 44:308-315.
68. Savage, V. M., J. F. Gillooly, W. H. Woodruff, G. B. West, A. P. Allen, B. J. Enquist, and J. H. Brown. 2004. The predominance of quarterpower scaling in biology. Functional Ecology 18:257-282.
69. Schmidt-Nielsen, K. 1984. Scaling: why is animal size so important? Cambridge University Press, Cambridge.
70. Schoolfield, R. M., P. J. H. Sharpe, and C. E. Magnuson. 1981. Nonlinear regression of biological temperature-dependent rate models based on absolute reaction-rate theory. Journal of Theoretical Biology 88:719-731.
71. Shaw, D. J., and A. P. Dobson. 1995. Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology 111:S111-S133.
72. Sibly, R. M., J. H. Brown, and A. Kodric-Brown, eds. 2012. Metabolic ecology: a scaling approach. Wiley-Blackwell, Chichester.
73. Stock, T. M., and J. C. Holmes. 1988. Functional relationships and microhabitat distributions of enteric helminths of grebes (Podicipedidae): the evidence for interactive communities. Journal of Parasitology 74:214-227.
74. Taylor, J. R. 1982. An introduction to error analysis: the study of uncertainties in physical measurements. University Science, Mill Valley, CA.
75. Walkey, M., and R. H. Meakins. 1970. An attempt to balance the energy budget of a host-parasite system. Journal of Fish Biology 2:361-372.
76. White, E. P., X. Xiao, N. J. B. Isaac, and R. M. Sibly. 2012. Methodological tools. Pages 7-20 in R. M. Sibly, J. H. Brown, and A. Kodric-Brown, eds. Metabolic ecology: a scaling approach. Wiley- Blackwell, Chichester.
77. Wiegel, F. W., and A. S. Perelson. 2004. Some scaling principles for the immune system. Immunology and Cell Biology 82:127-131.