Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-21T12:31:34.718Z Has data issue: false hasContentIssue false
  • English
  • Français

Body size and meta-community structure: the allometric scaling of parasitic worm communities in their mammalian hosts

Published online by Cambridge University Press:  22 March 2016

GIULIO A. DE LEO ,
ANDREW P. DOBSON  and
MARINO GATTO
GIULIO A. DE LEO
Affiliation:
Woods Institute for the Environment and Hopkins Marine Station, Stanford University, Pacific Grove, California 93950, USA
ANDREW P. DOBSON*
Affiliation:
Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey 08544-1003, USA
MARINO GATTO
Affiliation:
Dipartimento di Elettronica e Informazione, Politecnico di Milano, Via Ponzio 34/5, 23100 Milano, Italy
*
*Corresponding author: Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey 08544-1003, USA. E-mail: dobson@princeton.edu
Get access Rights & Permissions [Opens in a new window]

Summary

In this paper we derive from first principles the expected body sizes of the parasite communities that can coexist in a mammal of given body size. We use a mixture of mathematical models and known allometric relationships to examine whether host and parasite life histories constrain the diversity of parasite species that can coexist in the population of any host species. The model consists of one differential equation for each parasite species and a single density-dependent nonlinear equation for the affected host under the assumption of exploitation competition. We derive threshold conditions for the coexistence and competitive exclusion of parasite species using invasion criteria and stability analysis of the resulting equilibria. These results are then used to evaluate the range of parasites species that can invade and establish in a target host and identify the ‘optimal’ size of a parasite species for a host of a given body size; ‘optimal’ is defined as the body size of a parasite species that cannot be outcompeted by any other parasite species. The expected distributions of parasites body sizes in hosts of different sizes are then compared with those observed in empirical studies. Our analysis predicts the relative abundance of parasites of different size that establish in the host and suggests that increasing the ratio of parasite body size to host body size above a minimum threshold increases the persistence of the parasite population.

Keywords

intestinal nematodeswild mammal pathologybody sizeparasite communityinterspecific competitionlife-history strategiesallometric scalingbioenergetic requirements
Type
Special Issue Article
Information
Parasitology , Volume 143 , Special Issue 7: Mathematical modelling of infectious diseases , June 2016 , pp. 880 - 893
Check for updates
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Anderson, R. M. (1978). The regulation of host population growth by parasite species. Parasitology 76, 119–157.Google Scholar
Anderson, R. M. (1986). The population dynamics and epidemiology of intestinal nematode infections. Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 686–696.Google Scholar
Anderson, R. M. and May, R. M. (1978). Regulation and stability of host-parasite population interaction. I. Regulatory processes. Journal of Animal Ecology 47, 219–247.Google Scholar
Anderson, R. M. and May, R. M. (1991). Infectious Diseases of Humans: Dynamics and Control. Oxford University Press, Oxford.Google Scholar
Bailey, G. N. A. (1975). Energetics of a host parasite system: a preliminary report. International Journal for Parasitology: Parasites 5, 609–613.Google Scholar
Banavar, J. R., Damuth, J., Maritan, A. and Rinaldo, A. (2002 a). Supply-demand balance and metabolic scaling. Proceedings of the National Academy of Sciences of the United States of America 99, 10506–10509.Google Scholar
Banavar, J. R., Damuth, J., Maritan, A. and Rinaldo, A. (2002 b). Modelling universality and scaling. Nature 420, 626.Google Scholar
Berding, C., Keymer, A. E., Murray, J. D. and Slater, A. F. G. (1986). The population dynamics of acquired immunity to helminth infection. Journal of Theoretical Biology 122, 459–471.Google Scholar
Bolzoni, L., Gatto, M., Dobson, A. P. and De Leo, G. A. (2008 a). Body-size scaling in an SEI model of wildlife diseases. Theoretical Population Biology 73, 374–382.Google Scholar
Bolzoni, L., Gatto, M., Dobson, A. P. and De Leo, G. A. (2008 b). Allometric scaling and seasonality in the epidemics of wildlife diseases. The American Naturalist 172, 818–828.Google Scholar
Booth, D. T., Clayton, D. H. and Block, B. A. (1993). Experimental demonstration of the energetic cost of parasitism in free ranging hosts. Proceedings of the Royal Society of London B 253, 125–129.Google Scholar
Brose, U., Williams, R. J. and Martinez, N. D. (2006). Allometric scaling enhances stability in complex food webs. Ecology Letters 9, 1228–1236.Google Scholar
Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M. and West, G. B. (2004). Toward a metabolic theory of ecology. Ecology 77, 1771–1789.Google Scholar
Cable, J. M., Enquist, B. J. and Moses, M. E. (2007). The allometry of host pathogen interactions. PLoS ONE 2, e1130.Google Scholar
Calder, W. A. (1984). Size, Function and Life History. Harvard University Press, Cambridge.Google Scholar
Cattadori, I. M., Boag, B., Bjørnstad, O. N., Cornell, S. J. and Hudson, P. J. (2005). Peak shift and epidemiology in a seasonal host-nematode system. Proceedings of the Royal Society B: Biological Sciences 272, 1163–1169.Google Scholar
Charnov, E. L. (1992). Allometric aspects of population dynamics: a symmetry approach. Evolutionary Ecology 6, 307–311.Google Scholar
Charnov, E. L. (1993). Life History Invariants. Oxford University Press, Oxford.Google Scholar
Cohen, J. E., Jonsson, T. and Carpenter, S. R. (2003). Ecological community description using the food web, species abundance, and body size. Proceedings of the National Academy of Sciences of the United States of America 100, 1781–1786.Google Scholar
Cohen, J. E., Jonsson, T., Mƒuller, C. B., Godfray, H. C. J. and Savage, V. M. (2005). Body sizes of hosts and parasitoids in individual feeding relationships. Proceedings of the National Academy of Sciences of the United States of America 102, 684–689.Google Scholar
Cornell, S. J., Bjornstad, O. N., Cattadori, I. M., Boag, B. and Hudson, P. J. (2008). Seasonality, cohort-dependence and the development of immunity in a natural host-nematode system. Proceedings of the Royal Society B: Biological Sciences 275, 511–518.Google Scholar
Damuth, J. (1981). Population density and body size in mammals. Nature (Lond.) 290, 699–700.Google Scholar
De Leo, G. A. and Dobson, A. P. (1996). Allometry and simple epidemic models for macroparasites. Nature 379, 720–722.Google Scholar
Diekmann, O. and Kretzschmar, M. (1991). Patterns in the effects of infectious diseases on population growth. Journal of Mathematical Biology 29, 539–570.Google Scholar
Diekmann, O., Heesterbeek, J. A. P. and Metz, J. A. J. (1990). On the definition of the basic reproduction ratio R0 in models for infectious diseases in heterogeneous populations. Journal of Mathematical Biology 28, 365–382.Google Scholar
Dobson, A. P. (1985). The population dynamics of competition between parasites. Parasitology 91, 317–347.Google Scholar
Dobson, A. P. (1990). Models for multi-species parasite-host communities. In The Structure of Parasite Communities (ed. Esch, G., Kennedy, C. R. and Aho, J.), pp. 261–288. Chapman and Hall, London.Google Scholar
Dobson, A. P. and Roberts, M. (1994). The population dynamics of parasitic helminth communities. Parasitology 109 (Suppl.), 97–108.Google Scholar
Dobson, A. P., Lafferty, K. D., Kuris, A. M., Hechinger, R. and Jetz, W. (2008). Homage to Linnaeus: How many parasites? How many hosts? Proceedings of the National Academy of Sciences of the United States of America 105 (Suppl. 1), 11482–11489.Google Scholar
Dodds, P. S., Rothman, D. H. and Weitz, J. S. (2001). Re-examination of the 3/4-law of metabolism. Journal of Theoretical Biology 209, 9–27.Google Scholar
Dwyer, G., Levin, S. A. and Buttel, L. (1990). Simulation model of the population dynamics and evolution of myxomatosis. Ecological Monographs 60, 423–447.Google Scholar
Economo, E. P., Kerkhoff, A. J. and Enquist, B. J. (2005). Allometric growth, life-history invariants and population energetics. Ecology Letters 8, 353–360.Google Scholar
Esch, G. W., Bush, A. O. and Aho, J. M. (1990). Parasite Communities: Patterns and Processes. Chapman and Hall, London.Google Scholar
Fenner, F. (1983). Biological control, as exemplified by smallpox eradication and myxomatosis. Proceedings of the Royal Society of London B 218, 259–285.Google Scholar
Gatto, M. and De Leo, G. A. (1998). Interspecific competition among macroparasites in a density-dependent host population. Journal of Mathematical Biology 37, 467–490.Google Scholar
Gillooly, J. F., Brown, J. H., West, G. B. and Savage, V. M. (2001). Effects of size and temperature on metabolic rate. Science 293, 2248–2251.Google Scholar
Grenfell, B. T. and Dobson, A. P. (1995). Ecology of Infectious Diseases in Natural Populations. Cambridge University Press, Cambridge.Google Scholar
Harvey, P. H. and Keymer, A. E. (1991). Comparing life histories using phylogenies. Philosophical Transactions of the Royal Society B. 332, 31–39.Google Scholar
Hechinger, R. F. (2013). A metabolic and body-size scaling framework for parasite within-host abundance, biomass, and energy flux. The American Naturalist 182, 234–248.Google Scholar
Hechinger, R. F. (2015). Parasites help find universal ecological rules. Proceedings of the National Academy of Sciences 112, 1656–1657.Google Scholar
Hechinger, R. F., Lafferty, K. D., Dobson, A. P., Brown, J. H. and Kuris, A. M. (2011). A common scaling rule for abundance, energetics, and production of parasitic and free-living species. Science 333, 445–448.Google Scholar
Hechinger, R. F., Lafferty, K. D. and Kuris, A. M. (2012). Parasites. In Metabolic Ecology: a Scaling Approach (ed. Sibly, R. M., Brown, J. H. Kodric-Brown, A.), pp. 234–247, 392 p. Wiley-Blackwell, Oxford.Google Scholar
Hudson, P. J. and Dobson, A. P. (1994). Microparasites, observed patterns. In Infectious Diseases in Natural Populations (ed. Grenfell, B. T. and Dobson, A. P.), pp. 144–76. Cambridge University Press, Cambridge.Google Scholar
Janovy, J. Jr., Ferdig, M. T. and McDowell, M. A. (1990). A model of dynamic behavior of a parasite species assemblage. Journal of Theoretical Biology 142, 517–529.Google Scholar
Jetz, W., Carbone, C., Fulford, J. and Brown, J. H. (2005). The scaling of animal space use. Science 306, 266–268.Google Scholar
Kozlowksi, J. and Konarzewski, M. (2004). Is West, Brown and Enquist's model of allometric scaling mathematically correct and biologically relevant? Functional Ecology 18, 283–289.Google Scholar
Lafferty, K. D., DeLeo, G., Briggs, C. J., Dobson, A. P., Gross, T. and Kuris, A. M. (2015). A general consumer-resource population model. Science 349, 854–857.Google Scholar
Loeuille, N. and Loreau, M. (2005). Evolutionary emergence of size-structured food webs. Proceedings of the National Academy of Sciences of the United States of America 102, 5761–5766.Google Scholar
MacArthur, R. H. (1970). Species packing and competitive equilibrium for many species. Theoretical Population Biology 1, 1–11.Google Scholar
MacArthur, R. H. and Levins, R. (1967). The limiting similarity, convergence and divergence of coexisting species. American Naturalist 101, 377–385.Google Scholar
Marquet, P. A., Labra, F. A. and Maurer, B. A. (2004). Metabolic ecology: linking individuals to ecosystems. Ecology 85, 1794–1796.Google Scholar
May, R. M. and Anderson, R. M. (1978). Regulation and stability of host-parasite population interaction. II. Destabilizing processes. Journal of Animal Ecology 47, 249–267.Google Scholar
May, R. M. and Anderson, R. M. (1983). Epidemiology and genetics in the coevolution of parasites and hosts. Proceedings of the Royal Society of London, Series B 219, 281–313.Google Scholar
Molnar, P. K., Dobson, A. P. and Kutz, S. J. (2013 a). Gimme shelter – the relative sensitivity of parasitic nematodes with direct and indirect life cycles to climate change. Global Change Biology 19, 3291–3305.Google Scholar
Molnar, P. K., Kutz, S. J., Hoar, B. M. and Dobson, A. P. (2013 b). Metabolic approaches to understanding climate change impacts on seasonal host-macroparasite dynamics. Ecology Letters 16, 9–21.Google Scholar
Morand, S. (1996). Life-history traits in parasitic nematodes: a comparative approach for the search of invariants. Functional Ecology 10, 210–218.Google Scholar
Morand, S. and Poulin, R. (1998). Density, body mass and parasite species richness of terrestrial mammals. Evolutionary Ecology 12, 717–727.Google Scholar
Morand, S. and Poulin, R. (2002). Body size–density relationships and species diversity in parasitic nematodes: patterns and likely processes. Evolutionary Ecology Research 4, 951–961.Google Scholar
Morand, S., Legendre, P., Gardner, S. L. and Hugot, J. P. (1996). Body size evolution of oxyurid (Nematoda) parasites: the role of hosts. Oecologia 107, 274–282.Google Scholar
Osnas, E. E. and Dobson, A. P. (2010). Evolution of virulence when transmission occurs before disease. Biology Letters 6, 505–508.Google Scholar
Osnas, E. E. and Dobson, A. P. (2012). Evolution of virulence in heterogeneous host communities under multiple trade-offs. Evolution 66, 391–401.Google Scholar
Otto, S. B., Rall, B. C. and Brose, U. (2007). Allometric degree distributions facilitate food-web stability. Nature 450, 1226–1229.Google Scholar
Owen-Smith, R. N. (1988). Megaherbivores. The Influence of Very Large Body Size on Ecology. Cambridge University Press, Cambridge.Google Scholar
Peters, R. H. (1983). The Ecological Implications of Body Size. Cambridge University Press, Cambridge.Google Scholar
Poulin, R. (1995 a). Phylogeny, ecology, and the richness of parasite communities in vertebrates. Ecological Monographs 65, 283–302.Google Scholar
Poulin, R. and Morand, S. (2000). Parasite body size and interspecific variation in levels of aggregation among nematodes. Journal of Parasitology 86, 642–647.Google Scholar
Poulin, R. W. (1995 b). Evolution of parasite life history traits: myths and reality. Parasitology Today 11, 342–345.Google Scholar
Price, C. A., Weitz, J. S., Savage, V. M., Stegen, J., Clarke, A., Coomes, D. A., Dodds, P. S., Etienne, R. S., Kerkhoff, A. J., McCulloh, K., Niklas, K. J., Olff, H. and Swenson, N. G. (2012). Testing the metabolic theory of ecology. Ecology Letters 15, 1465–1474.Google Scholar
Roberts, M. G. and Dobson, A. P. (1995). The population-dynamics of communities of parasitic helminths. Mathematical Biosciences 126, 191–215.Google Scholar
Roberts, M. G., Smith, G. and Grenfell, B. T. (1993). Mathematical models for macroparasites of wildlife. In Ecology of Infectious Diseases in Natural Populations. Newton Workshop (ed. Dobson, A. P. and Grenfell, B. T.), pp. 177–208. Cambridge University Press, Cambridge.Google Scholar
Roughgarden, J. (1979). Theory of Population Genetics and Evolutionary Ecology: an Introduction. Macmillan Publishing Company Co., Inc., New York.Google Scholar
Savage, V. M., Gillooly, J. F., Brown, J. H., West, G. B. and Charnov, E. L. (2004 a). Effects of body size and temperature on population growth. The American Naturalist 163, E429–E441.Google Scholar
Savage, V. M., Gillooly, J. F., WoodruÆ, W. H., West, G. B., Allen, A. P., Enquist, B. J. and Brown, J. H. (2004 b). The predominance of quarterpower scaling in biology. Functional Ecology 18, 257–282.Google Scholar
Schmidt-Nielsen, K. (1984). Scaling: Why is Animal Body Size so Important? Cambridge University Press, Cambridge.Google Scholar
Shaw, D. J., Grenfell, B. T. and Dobson, A. P. (1998). Patterns of parasite aggregation and the negative binomial distribution. Parasitology 117, 597–610.Google Scholar
Silva, M. and Downing, J. A. (1995). The allometric scaling of density and body mass: a nonlinear relationship for terrestrial mammals. The American Naturalist 145, 704–727.Google Scholar
Skorping, A., Read, A. F. and Keymer, A. E. (1991). Life history covariation in intestinal nematodes of mammals. Oikos 60, 365–372.Google Scholar
Stearns, S. C. (1992). The Evolution of Life Histories. Oxford University Press, London.Google Scholar
Tilman, D., Lehman, C., HilleRisLambers, J., Harpole, W. S., Dybzinski, R., Fargione, J., Clark, C. and Lehman, C. (2004). Does metabolic theory apply to community ecology? It's a matter of scale. Ecology 85, 1797–1799.Google Scholar
Vance, R. R. (1985). The stable coexistence of two competitors for one resource. The American Naturalist 126, 72–86.Google Scholar
Wakelin, D. (1984). Evasion of the immune response: survival within low responder individuals of the host population. Parasitology 88, 639–657.Google Scholar
Weibel, E. R., Bacigalupe, L. D., Schmitt, B. and Hoppeler, H. (2004). Allometric scaling of maximal metabolic rate in mammals: muscle aerobic capacity as determinant factor. Respiratory Physiology & Neurobiology. 140, 115–132.Google Scholar
Weitz, J. S. and Levin, S. A. (2006). Size and scaling in predator-prey dynamics. Ecology Letters 9, 548–557.Google Scholar
West, G. B. and Brown, J. H. (2005). The origin of allometric scaling laws in biology from genomes to ecosystems: towards a quantitative unifying theory of biological structure and organization. Journal of Experimental Biology 208, 1575–1592.Google Scholar
West, G. B., Brown, J. H. and Enquist, B. J. (1997). A general model for the origin of allometric scaling laws in biology. Science 276, 122–126.Google Scholar
West, G. B., Brown, J. H. and Enquist, B. J. (1999). The fourth dimension of life: fractal geometry and allometry scaling of organisms. Science 284, 1677–1679.Google Scholar
White, C. R. and Seymour, R. S. (2003). Mammalian basal metabolic rate is proportional to body mass 2/3. Proceedings of the National Academy of Sciences of the United States of America 100, 4046–4049.Google Scholar
Yodzis, P. and Innes, S. (1992). Body size and consumer-resource dynamics. The American Naturalist 139, 1151–1175.Google Scholar