Inferring the temperature dependence of population parameters: The effects of experimental design and inference algorithm

Ecology and Evolution

Volumn 4, Issue 24, 2014, Pages 4736-4750

  Palamara, Gian Marco ^a,c   Childs, Dylan Z ^b   Clements, Christopher F ^a   Petchey, Owen L ^a   Plebani, Marco ^a   Smith, Matthew J ^c  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

^c MICROSOFT RESEARCH   (United Kingdom)

Author keywords

MCMC; Activation energy; Arrhenius equation; Maximum likelihood; Metabolic theory; Microcosm experiments; State space models; Stochastic simulations

Indexed keywords

PARAMECIUM CAUDATUM;

EID: 84919866028     PISSN: None     EISSN: 20457758     Source Type: Journal    
DOI: 10.1002/ece3.1309     Document Type: Article

References (86)

1. *Allen, L. J. S., and E. J. Allen. 2003. A comparison of three different stochastic population models with regard to persistence time. Theor. Popul. Biol. 64:439-449.
2. Allen, A. P., J. F. Gillooly, and J. H. Brown. 2005. Linking the global carbon cycle to individual metabolism. Funct. Ecol. 19:202-213.
3. Amarasekare, P., and V. M. Savage. 2012. Elucidating the temperature dependence of fitness. Am. Nat. 179:178-191.
4. Amarasekare, P., and R. Sifuentes. 2012. Elucidating the temperature response of survivorship in insects. Funct. Ecol. 26:959-968.
5. Ananthasubramaniam, B., R. M. Nisbet, W. A. Nelson, E. McCauley, and W. S. C. Gurney. 2011. Stochastic growth reduces population fluctuations in Daphnia-algal systems. Ecology 92:362-372.
6. Angiletta, M. J. Jr. 2006. Estimating and comparing thermal performance curves. J. Therm. Biol. 31:541-545.
7. Arrhenius, S. 1889. Über die reaktionsgeschwindigkeit bei der inversion von rohrzucker durch säuren. Z. Phys. Chem. 4:226-248.
8. Beaumont, M. A. 2010. Approximate Bayesian Computation in evolution and ecology. Annu. Rev. Ecol. Evol. Syst. 41:379-406.
9. Beveridge, O. S., O. L. Petchey, and S. Humphries. 2010. Direct and indirect effects of temperature on the population dynamics and ecosystem functioning of aquatic microbial ecosystems. J. Anim. Ecol. 79:1324-1331.
10. Black, A. J., and A. J. McKane. 2012. Stochastic formulation of ecological models and their applications. Trends Ecol. Evol. 27:337-345.
11. *Bolker, B. 2013. Bbmle: Tools for general maximum likelihood estimation. R package version 1.0-13.
12. 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.
13. *Cappé, O., E. Moulines, and T. Ryden. 2005. Inference in hidden Markov models. Springer Series in Statistics XVIII. Springer, New York.
14. *Chib, S., and E. Greenberg. 1995. Understanding the Metropolis-Hasting algorithm. Am. Stat. 49:327-335.
15. Corkrey, R., J. Olley, D. Ratkowsky, T. McMeekin, T. Ross T. Ross. 2012 Universality of Thermodynamic Constants Governing Biological Growth Rates. PLoS One 7(2):e32003. doi: 10.1371/journal.pone.0032003.
16. De Valpine, P., and A. Hastings. 2002. Fitting population models incorporating process noise and observation error. Ecol. Monogr. 72:57-76.
17. De'ath, G., and K. E. Fabricius. 2000. Classification and regression trees: a powerful yet simple technique for ecological data analysis. Ecology 81:3178-3192.
18. Dell, A. I., S. Pawar, and V. M. Savage. 2010. Systematic variation in the temperature dependence of physiological and ecological traits. Proc. Natl Acad. Sci. USA 108:10591-10596.
19. Dell, A. I., S. Pawar, and V. M. Savage. 2014. Temperature dependence of trophic interactions are driven by asymmetry of species responses and foraging strategy. J. Anim. Ecol. 83:70-84.
20. Dennis, B., and J. M. Ponciano. 2014. Density-dependent-state space model for population-abundance with unequal time intervals. Ecology 95:2069-2076.
21. Dennis, B., J. M. Ponciano, S. R. Lele, M. L. Taper, and D. F. Staples. 2006. Estimating density dependence, process noise, and observation error. Ecol. Monogr. 76:323-341.
22. Deutsch, C. A., J. J. Tewksbury, R. B. Huey, K. S. Sheldon, C. K. Ghalambor, D. C. Haak, et al. 2008. Impacts of climate warming on terrestrial ectotherms across latitude. Proc. Natl Acad. Sci. USA 105:6668-6672.
23. Ebenman, B., R. Law, and C. Borrvall. 2004. Community viability analysis: the response of ecological communities to species loss. Ecology 85:2591-2600.
24. Englund, G., G. Ohlund, C. L. Hein, and S. Diehl. 2011. Temperature dependence of the functional response. Ecol. Lett. 14:914-921.
25. Ernest, S. K. M., B. J. Enquist, J. H. Brown, E. L. Charnov, J. F. Gillooly, V. M. Savage, et al. 2003. Thermodynamic and metabolic effects on the scaling of production and population energy use. Ecol. Lett. 6:990-995.
26. *Filzbach, Microsoft Research Cambridge. 2013. Available via http://research.microsoft.com/en-us/um/cambridge/groups/science/tools/filzbach/filzbach.htm
27. Fussmann, K. E., F. Schwarzmüller, U. Brose, A. Jousset, and B. C. Rall. 2014. Ecological stability in response to warming. Nat. Clim. Chang. 4:206-210.
28. Gardinier, C. 2009. Stochastic methods: a handbook for the natural and social sciences. Springer, Berlin.
29. Gillespie, D. T. 1976. A general method for numerically simulating the stochastic time evolution of coupled chemical reactions. J. Comput. Phys. 22:403-434.
30. *Gillespie, D. T. 1977. Exact stochastic simulation of coupled chemical reactions. J. Phys. Chem. 81:2340-2361.
31. 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.
32. Gillooly, J. F., E. L. Charnov, G. B. West, V. M. Savage, and J. H. Brown. 2002. Effects of size and temperature on developmental time. Nature 417:70-73.
33. Glazier, D. S. 2006. The 3/4-power law is not universal: evolution of isometric, ontogenetic metabolic scaling in pelagic animals. Bioscience 56:325-332.
34. Grimm, V., E. Revilla, U. Berger, F. Jeltsch, W. M. Mooij, S. F. Railsback, et al. 2005. Pattern-oriented modeling of agent-based complex systems: lessons from ecology. Science 310:987-991.
35. Hall, A. S. C., J. A. Stanford, and F. R. Hauer. 1992. The distribution of abundance of organisms as a consequence of energy balances along multiple environmental gradients. Oikos 65:377-390.
36. Hartig, F., J. M. Calabrese, B. Reineking, T. Wiegand, and A. Huth. 2011. Statistical inference for stochastic simulation models - theory and application. Ecol. Lett. 14:86-827.
37. Hilborn, R. 1997. The ecological detective: confronting models with data. Princeton Univ. Press, Princeton, New Jersey.
38. Huang, L., A. Hwang, and J. Phillips. 2011. Effect of temperature on microbial growth rate-mathematical analysis: the Arrhenius and Eyring-Polany corrections. J. Food Sci. 76:553-560.
39. Huey, R. B., and J. G. Kingsolver. 2011. Variation in universal dependence of biological rates. Proc. Natl Acad. Sci. USA 108:10377-10378.
40. Ionides, E. L. 2003. Inference and filtering for partially observed diffusion processes via sequential Monte Carlo. Department of Statistics Technical Report, The University of Michigan, Ann Arbor.
41. Ionides, E. L., C. Bretó, and A. A. King. 2006. Inference for nonlinear dynamical systems. Proc. Natl Acad. Sci. USA 103:18438-18443.
42. Irlich, U. M., J. S. Terblanche, T. M. Blackburn, and S. L. Chown. 2009. Insect rate-temperature relationships: environmental variation and the metabolic theory of ecology. Am. Nat. 174:819-835.
43. Ives, A. R. 1995. Predicting the response of populations to environmental change. Ecology 76:926-941.
44. Jang, L., and P. J. Morin. 2004. Temperature-dependent interactions explain unexpected responses to environmental warming in communities of competitors. J. Anim. Ecol. 73:569-576.
45. *Kirkpatrick, S., C. D. Gelatt, and M. P. Vecchi. 1983. Optimization by simulated annealing. Science 220:671-680.
46. Knape, J., and P. De Valpine. 2012. Fitting complex population models by combining particle filters with Markov chain Monte Carlo. Ecology 93:256-263.
47. Knies, L., and J. G. Kingsolver. 2010. Erroneus Arrhenius: modified Arrhenius model best explains the temperature dependence of ectotherm fitness. Am. Nat. 176:227-233.
48. Krenek, S., T. U. Berendonk, and T. Petzoldt. 2011. Thermal performance curves of Paramecium caudatum: a model selection approach. Eur. J. Protistol. 47:124-137.
49. Krenek, S., T. Petzoldt, and T. U. Berendonk. 2012. Coping with temperature at the warm edge - patterns of thermal adaptation in the microbial eukaryote Paramecium caudatum. PLoS One, 7. Available via http://dx.doi.org/10.1371/journal.pone.0030598
50. Leary, D. J., and O. L. Petchey. 2009. Testing a biological mechanism of the insurance hypothesis in experimental aquatic communities. J. Anim. Ecol. 78:1143-1151.
51. Leary, D. J., J. M. K. Rip, and O. L. Petchey. 2012. The impact of environmental variability and species composition on the stability of experimental microbial populations and communities. Oikos 121:327-336.
52. Malthus, T. 1798. An essay on the principle of population. J. Johnson, London.
53. McInerny, G. J., and D. W. Purves. 2011. Fine-scale environmental variation in species distribution modelling: regression dilution, latent variables and neighbourly advice. Methods Ecol. Evol. 2:248-257.
54. McKane, A. J., and T. J. Newman. 2004. Stochastic models in population biology and their deterministic analogs. Phys. Rev. E 70:1-19.
55. McKane, A. J., and T. J. Newman. 2005. Predator-prey cycles from resonant amplification of demographic stochasticity. Phys. Rev. Lett. 94:1-4.
56. Monod, J. 1942. Recherches sur la croissance des cultures bacteriennes. Hermann, Paris.
57. Montagnes, D. J. S., and D. J. Franklin. 2001. Effect of temperature on diatom volume, growth rate, and carbon and nitrogen content: reconsidering some paradigms. Limnol. Oceanogr. 46:2008-2018.
58. Montagnes, D. J. S., S. A. Kimmance, G. Tsounis, and J. C. Gumbs. 2001. Combined effect of temperature and food concentration on the grazing rate of the rotifer Brachionus plicatilis. Mar. Biol. 139:975-979.
59. Nåsell, I. 2001. Extinction and quasi-stationarity in the Verhulst logistic model. J. Theor. Biol. 211:11-27.
60. Novak, M., J. T. Wootton, D. F. Doak, M. Emmerson, J. A. Estes, and M. T. Tinker. 2011. Predicting community responses to perturbations in the face of imperfect knowledge and network complexity. Ecology 92:836-846.
61. O'Connor, M. I., B. Gilbert, and C. J. Brown. 2011. Theoretical predictions for how temperature affects the dynamics of interacting herbivores and plants. Am. Nat. 178:626-638.
62. Pascual, M. A., and P. Kareiva. 1996. Predicting the outcome of competition using experimental data: Maximum Likelihood and Bayesian approaches. Ecology 77:337-349.
63. Petchey, O. L., U. Brose, and B. C. Rall. 2010. Predicting the effects of temperature on food web connectance. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365:2081-2091.
64. Price, P. B., and T. Sowers. 2004. Temperature dependence of metabolic rates for microbial growth, maintenance, and survival. Proc. Natl Acad. Sci. USA 101:4631-4636.
65. Rall, B. C., O. Vucic-Pestic, R. B. Ehnes, M. Emmerson, and U. Brose. 2009. Temperature, predator-prey interaction strength and population stability. Glob. Change Biol. 16:2145-2157.
66. Ripley, B. 2007. Tree: classification and regression trees. R package version 1.0-26.
67. Ross, J. V. 2012. On parameter estimation in population models III: time-inhomogeneous processes and observation error. Theor. Popul. Biol. 82:1-17.
68. Ross, J. V., T. Taimre, and P. K. Pollett. 2006. On parameter estimation in population models. Theor. Popul. Biol. 70:498-510.
69. Ross, J. V., D. E. Pagendam, and P. K. Pollett. 2009. On parameter estimation in population models II: multi-dimensional processes and transient dynamics. Theor. Popul. Biol. 75:123-132.
70. Savage, V. M., J. F. Gillooly, J. H. Brown, G. B. West, and E. L. Charnov. 2004. Effects of body size and temperature on population growth. Am. Nat. 3:429-441.
71. 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. J. Theor. Biol. 88:719-731.
72. Sibly, R. M., V. Grimm, B. T. Martin, A. S. A. Johnston, K. Kulakowska, C. J. Topping, et al. 2013. Representing the acquisition and use of energy by individuals in agent-based models of animal populations. Methods Ecol. Evol. 4:151-161.
73. Smith, M. J., D. W. Purves, M. C. Vanderwel, V. Lyutsarev, and S. Emmott. 2013. The climate dependence of the terrestrial carbon cycle, including parameter and structural uncertainties. Biogeosciences 10:583-606.
74. Thomas, C. D., A. Cameron, R. E. Green, M. Bakkenes, L. J. Beaumont, Y. C. Collingham, et al. 2004. Extinction risk from climate change. Nature 427:145-148.
75. Turchin, P. 2003. Complex population dynamics: a theoretical/empirical synthesis. Princeton Univ. Press, Princeton, New Jersey.
76. Van't Hoff, J. H. 1884. Etudes de dynamique chimique F. Muller & Co., Amsterdam.
77. Vasseur, D. A., and K. S. McCann. 2005. A mechanistic approach for modeling temperature-dependent consumer-resource dynamics. Am. Nat. 166:184-198.
78. Vasseur, D. A., J. P. DeLong, B. Gilbert, H. S. Greig, C. D. G. Harley, K. S. McKann, et al. 2014. Increased temperature variation poses a greater risk to species than climate warming. Proc. R. Soc. B Biol. Sci. 281:20132612.
79. Volkov, I., J. R. Banavar, S. P. Hubbell, and A. Maritan. 2003. Neutral theory and relative species abundance in ecology. Nature 424:1035-1037.
80. Weisse, T., and D. J. S. Montagnes. 1998. Effect of temperature on inter- and intraspecific isolates of Urotricha (Prostomatida, Ciliophora). Aquat. Microb. Ecol. 15:285-291.
81. Weisse, T., P. Stadler, E. S. Lindström, S. A. Kimmance, and D. J. S. Montagnes. 2002. Interactive effect of temperature and food concentration on growth rate: A test case using the small freshwater ciliate Urotricha farcta. Limnol. Oceanogr. 47:1447-1455.
82. Wells, K., H. Feldhaar, and R. B. O'Hara. 2014. Population fluctuations affect inference in ecological networks of multi-species interactions. Oikos 123:589-598.
83. *Wilkinson, D. 2006. Stochastic modelling for systems biology. Chapman & Hall/CRC, London.
84. Yodzis, P. 1988. The Indeterminacy of Ecological Interactions as Perceived Through Perturbation Experiments. Ecology 69:508-515.
85. Yodzis, P., and S. Innes. 1992. Body size and consumer-resource dynamics. Am. Nat. 139:1151-1175.
86. Yvon-Durocher, G., J. M. Caffrey, A. Cescatti, M. Dossena, P. Del Giorgio, J. M. Gasol, et al. 2012. Reconciling the temperature dependence of respiration across timescales and ecosystem types. Nature 487:472-476.