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From Lotka–Volterra to Arditi–Ginzburg: 90 Years of Evolving Trophic Functions

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Abstract

The trophic function, often called a “functional response,” determines qualitative properties in models of predator–prey dynamics. Many of the theoretical and empirical studies have demonstrated the problem of choosing and fitting a trophic function to experimental data. Notably the publication by Arditi and Ginzburg (1989) has stimulated a lively debate in scientific literature regarding the application of trophic functions. The authors highlighted contradictions between the observed dynamics of natural ecosystems and the qualitative properties of predator–prey models using Holling-type trophic functions. They suggested revising the theoretical models by means of the trophic functions that depend on the ratio of prey to predator abundances. By comparing this and other proposed trophic functions, we demonstrate that the Arditi–Ginzburg function offers the simplest way of accounting for mutual interference in predator–prey models. This trophic function effectively resolves contradictions between theoretical models and natural systems, including the paradox of enrichment, paradox of biological control, and the paradoxical enrichment response mediated by trophic cascades. We review the debate regarding the Arditi–Ginzburg model and present recent results obtained with continuous and individual-based models of animal foraging behaviour in predator–prey systems, which explain predator interference as an emerging property.

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REFERENCES

  1. Abrams, P.A., The fallacies of “ratio-dependent” predation, Ecology, 1994, vol. 75, no. 6, pp. 1842–1850.

    Article  Google Scholar 

  2. Abrams, P.A., Why ratio dependence is (still) a bad model of predation, Biol. Rev., 2015, vol. 90, no. 3, pp. 794–814.

    Article  PubMed  Google Scholar 

  3. Abrams P.A. and Ginzburg, L.R., The nature of predation: prey dependent, ratio dependent or neither? Trends Ecol. Evol., 2000, vol. 15, no. 8, pp. 337–341.

    Article  CAS  PubMed  Google Scholar 

  4. Akçakaya, H.R., Population cycles of mammals: evidence for a ratio-dependent predation hypothesis, Ecol. Monogr., 1992, vol. 62, no. 1, pp. 119–142.

    Article  Google Scholar 

  5. Akçakaya, H.R., Arditi, R., and Ginzburg, L.R., Ratio-dependent predation: an abstraction that works, Ecology, 1995, vol. 76, no. 3, pp. 995–1004.

    Article  Google Scholar 

  6. Alexander, M.E., Dick, J.T., and O’Connor, N.E., Trait-mediated indirect interactions in a marine intertidal system as quantified by functional responses, Oikos, 2013, vol. 122, no. 11, pp. 1521–1531.

    Article  Google Scholar 

  7. Arditi, R., Relation of the Canadian lynx cycle to a combination of weather variables: a stepwise multiple regression analysis, Oecologia, 1979, vol. 41, no. 2, pp. 219–233.

    Article  CAS  PubMed  Google Scholar 

  8. Arditi, R., A unified model of the functional response of predators and parasitoids, J. Anim. Ecol., 1983, vol. 52, pp. 293–303.

    Article  Google Scholar 

  9. Arditi, R. and Akçakaya, H.R., Underestimation of mutual interference of predators, Oecologia, 1990, vol. 83, no. 3, pp. 358–361.

    Article  CAS  PubMed  Google Scholar 

  10. Arditi, R. and Berryman, A.A., The biological control paradox, Trends Ecol. Evol., 1991, vol. 6, no. 1, p. 32.

    Article  CAS  PubMed  Google Scholar 

  11. Arditi, R. and Ginzburg, L.R., Coupling in predator–prey dynamics: ratio-dependence, J. Theor. Biol., 1989, vol. 139, no. 3, pp. 311–326.

    Article  Google Scholar 

  12. Arditi, R. and Ginzburg, L.R., How Species Interact: Altering the Standard View on Trophic Ecology, New York: Oxford Univ. Press, 2012.

    Book  Google Scholar 

  13. Arditi, R. and Saïah, H., Empirical evidence of the role of heterogeneity in ratio–dependent consumption, Ecology, 1992, vol. 73, no. 5, pp. 1544–1551.

    Article  Google Scholar 

  14. Arditi, R., Abillon, J.M., and Vieira da Silva, J., A predator–prey model with satiation and intraspecific competition, Ecol. Model., 1978, vol. 5, no. 3, pp. 173–191.

    Article  Google Scholar 

  15. Arditi, R., Ginzburg, L.R., and Akcakaya, H.R., Variation in plankton densities among lakes: a case for ratio-dependent predation models, Am. Nat., 1991, vol. 138, no. 5, pp. 1287–1296.

    Article  Google Scholar 

  16. Arditi, R., Tyutyunov, Yu., Morgulis, A., Govorukhin, V., and Senina, I., Directed movement of predators and the emergence of density dependence in predator–prey models, Theor. Popul. Biol., 2001, vol. 59, no. 3, pp. 207–221.

    Article  CAS  PubMed  Google Scholar 

  17. Arditi, R., Callois, J.-M., Tyutyunov, Yu., and Jost, C., Does mutual interference always stabilize predator–prey dynamics? A comparison of models, C. R. Biol., 2004, vol. 327, pp. 1037–1057.

    Article  PubMed  Google Scholar 

  18. Arditi, R., Bersier, L.F., and Rohr, R.P., The perfect mixing paradox and the logistic equation: Verhulst vs. Lotka, Ecosphere, 2016, vol. 7, no. 11, p. e01599.

    Article  Google Scholar 

  19. Bakaeva, E.N., Ekologo-biologicheskie osnovy zhiznedeyatel’nosti kolovratok v kul’ture (Ecological and Biological Principles of Activity of Rotifers in Culture), Rostov-on-Don: Sev.-Kavk. Nauchn. Tsentr, Vyssh. Shk., 1999.

  20. Bazykin, A.D., Matematicheskaya biofizika vzaimodeistvuyushchikh populyatsii (Mathematical Biophysics of Interacting Populations), Moscow: Nauka, 1985.

  21. Bazykin, A.D., Nonlinear Dynamics of Interacting Populations, World Scientific Series on Nonlinear Science Series A, vol. 11, Singapore: World Scientific, 1989. https://doi.org/10.1142/2284.

  22. Bazykin, A.D., Berezovskaya, F.S., Denisov, G.A., and Kuznetzov, Yu.A., The influence of predator saturation effect and competition among predators on predator–prey system dynamics, Ecol. Model., 1981, vol. 14, nos. 1–2, pp. 39–57.

    Article  Google Scholar 

  23. Beddington, J.R., Mutual interference between parasites or predators and its effect on searching efficiency, J. Anim. Ecol., 1975, vol. 44, no. 1, pp. 331–340.

    Article  Google Scholar 

  24. Begon, M., Harper, J.L., and Townsend, C.R., Ecology: Individuals, Populations and Communities, Oxford: Blackwell, 1986.

    Google Scholar 

  25. Berdnikov, S.V., Selyutin, V.V., Vasilchenko, V.V., and Caddy, J.F., Trophodynamic model of the Black and Azov seas pelagic ecosystem: consequences of the comb jelly, Mnemiopsis leydei, invasion, Fish. Res., 1999, vol. 42, no. 3, pp. 261–289.

    Article  Google Scholar 

  26. Berezovskaya, F., Karev, G., and Arditi, R., Parametric analysis of the ratio-dependent predator–prey model, J. Math. Biol., 2001, vol. 43, no. 3, pp. 221–246.

    Article  CAS  PubMed  Google Scholar 

  27. Berezovskaya, F.S., Novozhilov, A.S., and Karev, G.P., Population models with singular equilibrium, Math. Biosci., 2007, vol. 208, no. 1, pp. 270–299.

    Article  PubMed  Google Scholar 

  28. Berezovskya, F., Karev, G., Song, B., and Castillo-Chavez, C., A simple epidemic model with surprising dynamics, Math. Biosci. Eng., 2005, vol. 2, no. 1, pp. 133–152.

    Article  Google Scholar 

  29. Berlow, E.L., Neutel, A.M., Cohen, J.E., De Ruiter, P.C., Ebenman, B.O., Emmerson, M., Fox, J.W., Jansen, V.A.A., Jones, J.I., Kokkoris, G.D., Logofet, D.O., McKane, A. J., Montoya, J.M., and Petchey, O., Interaction strengths in food webs: issues and opportunities, J. Anim. Ecol., 2004, vol. 73, no. 3, pp. 585–598.

    Article  Google Scholar 

  30. Berryman, A.A., The theoretical foundations of biological control, in Theoretical Approaches to Biological Control, Hawkins, B.A. and Cornell, H.V., Eds., Cambridge: Cambridge Univ. Press, 1999, pp. 3–21.

    Google Scholar 

  31. Bohannan, B.J. and Lenski, R.E., Effect of resource enrichment on a chemostat community of bacteria and bacteriophage, Ecology, 1997, vol. 78, no. 8, pp. 2303–2315.

    Article  Google Scholar 

  32. Borrelli, J.J., Allesina, S., Amarasekare, P., Arditi, R., Chase, I., Damuth, J., Holt, R.D., Logofet, D.O., et al., Selection on stability across ecological scales, Trends Ecol. Evol., 2015, vol. 30, no. 7, pp. 417–425.

    Article  PubMed  Google Scholar 

  33. Bratus’, A.S., Novozhilov, A.S., and Platonov, A.P., Dinamicheskie sistemy i modeli biologii (Dynamic Systems and Models in Biology), Moscow: Fizmatlit, 2010.

  34. Contois, D.E., Kinetic of bacterial growth relationship between population density and specific growth rate of continuous culture, J. Gen. Microbiol., 1959, vol. 21, no. 1, pp. 40–50.

    Article  CAS  PubMed  Google Scholar 

  35. Cordoleani, F., Nerini, D., Morozov, A., Gauduchon, M., and Poggiale, J.C., Scaling up the predator functional response in heterogeneous environment: When Holling type III can emerge? J. Theor. Biol., 2013, vol. 336, pp. 200–208.

    Article  PubMed  Google Scholar 

  36. Cosner, C., DeAngelis, D.L., Ault, J.S., and Olson, D.B., Effect of spatial grouping on the functional response of predators, Theor. Popul. Biol., 1999, vol. 56, no. 1, pp. 65–75.

    Article  CAS  PubMed  Google Scholar 

  37. Courchamp, F. and Bradshaw, C.J., 100 articles every ecologist should read, Nat. Ecol. Evol., 2018, vol. 2, no. 2, p. 395.

    Article  PubMed  Google Scholar 

  38. Crowley, P.H. and Martin, E.K., Functional responses and interference within and between year classes of a dragonfly population, J. North Am. Benthol. Soc., 1989, vol. 8, no. 3, pp. 211–221.

    Article  Google Scholar 

  39. Dawes, J.H.P. and Souza, M.O., A derivation of Holling’s type I, II and III functional responses in predator–prey systems, J. Theor. Biol., 2013, vol. 327, pp. 11–22.

    Article  CAS  PubMed  Google Scholar 

  40. DeAngelis, D.L., Goldstein, R.A., and O’Neill, R.V., A model for trophic interaction, Ecology, 1975, vol. 56, no. 4, P. 881–892.

    Article  Google Scholar 

  41. Elton C., Animal Ecology, New York: Macmillan, 1927.

    Google Scholar 

  42. Food Webs: From Connectivity to Energetics, Caswell, H., Ed., London: Elsevier, 2005.

    Google Scholar 

  43. Free, C.A., Beddington, J.R., and Lawton, J.H., On the inadequacy of simple models of mutual interference for parasitism and predation, J. Anim. Ecol., 1977, vol. 46, no. 2, pp. 543–554.

    Article  Google Scholar 

  44. Freedman, H.I. and Mathsen, R.M., Persistence in predator–prey systems with ratio-dependent predator influence, Bull. Math. Biol., 1993, vol. 55, no. 4, pp. 817–827.

    Article  Google Scholar 

  45. Fussmann, G.F., Weithoff, G., and Yoshida, T., A direct, experimental test of resource vs. consumer dependence, Ecology, 2005, vol. 86, no. 11, pp. 2924–2930.

    Article  Google Scholar 

  46. Gabriel, J.P., Saucy, F., and Bersier, L.F., Paradoxes in the logistic equation? Ecol. Model., 2005, vol. 185, no. 1, pp. 147–151.

    Article  Google Scholar 

  47. Gause, G.F., The Struggle for Existence, Baltimore: Williams and Wilkins, 1934.

    Book  Google Scholar 

  48. Ginzburg, L.R., Equations of the theory of biological communities, in Matematicheskoe modelirovanie v biologii (Mathematical Models in Biology), Moscow: Nauka, 1975, pp. 53–91.

  49. Ginzburg, L.R., The theory of population dynamics: I. Back to first principles, J. Theor. Biol., 1986, vol. 122, no. 4, pp. 385–399.

    Article  Google Scholar 

  50. Ginzburg, L.R., Recollections of unforgettable encounters with Aleksei Andreevich Lyapunov, in Aleksei Andreevich Lyapunov. 100 let so dnya rozhdeniya (Aleksey Andreevich Lyapunov: To the 100th Anniversary), Fedotov, A.M. and Fet, Ya.I., Eds., Novosibirsk: GEO, 2011, pp. 322–323.

  51. Ginzburg, L.R., Assuming reproduction to be a function of consumption raises doubts about some popular predator–prey models, J. Anim. Ecol., 1998, vol. 67, no. 2, pp. 325–327.

    Article  Google Scholar 

  52. Ginzburg, L.R. and Akcakaya, H.R., Consequences of ratio-dependent predation for steady-state properties of ecosystems, Ecology, 1992, vol. 73, no. 5, pp. 1536–1543.

    Article  Google Scholar 

  53. Ginzburg, L.R. and Colyvan, M., Ecological Orbits: How Planets Move and Populations Grow, New York: Oxford Univ. Press, 2004.

    Google Scholar 

  54. Ginzburg, L.R. and Jensen, C.X., Rules of thumb for judging ecological theories, Trends Ecol. Evol., 2004, vol. 19, no. 3, pp. 121–126.

    Article  PubMed  Google Scholar 

  55. Ginzburg, L.R. and Jensen, C.X., From controversy to consensus: the indirect interference functional response, Verh.-Int. Ver. Theor. Angew. Limnol., 2008, vol. 30, no. 2, pp. 297–301.

    Google Scholar 

  56. Ginzburg, L.R. and Krebs, C.J., Mammalian cycles: internally defined periods and interaction-driven amplitudes, PeerJ, 2015, vol. 3, p. e1180.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Ginzburg, L.R., Goldman, Yu.I., and Railkin, A.I., A mathematical model of interaction between two populations—predator–prey, Zh. Obshch. Biol., 1971, vol. 32, no. 6, pp. 724–730.

    Google Scholar 

  58. Ginzburg, L.R., Konovalov, N.Yu., and Epelman, G.S., A mathematical model of interaction between two populations, Zh. Obshch. Biol., 1974, vol. 35, no. 4, pp. 613–619.

    CAS  PubMed  Google Scholar 

  59. Hanski, I., Hansson, L., and Henttonen, H., Specialist predators, generalist predators, and the microtine rodent cycle, J. Anim. Ecol., 1991, vol. 60, no. 1, pp. 353–367.

    Article  Google Scholar 

  60. Harrison, G.W., Comparing predator–prey models to Luckinbill’s experiment with Didinium and Paramecium, Ecology, 1995, vol. 76, no. 2, pp. 357–374.

    Article  Google Scholar 

  61. Hassell, M.P., The Dynamics of Arthopod Predator-Prey Systems, Princeton, NY: Princeton Univ. Press, 1978.

    Google Scholar 

  62. Hassell, M.P. and Varley, G.C., New inductive population model for insect parasites and its bearing on biological control, Nature, 1969, vol. 223, pp. 1133–1137.

    Article  CAS  PubMed  Google Scholar 

  63. Haydon, D.T. and Lloyd, A.L., On the origins of the Lotka–Volterra equations, Bull. Ecol. Soc. Am., 1999, vol. 80, no. 3, pp. 205–206.

    Article  Google Scholar 

  64. Holling, C.S., The components of predation as revealed by a study of small-mammal predation of the European sawfly, Can. Entomol., 1959a, vol. 91, pp. 293–320.

    Article  Google Scholar 

  65. Holling, C.S., Some characteristics of simple types of predation and parasitism, Can. Entomol., 1959b, vol. 91, pp. 385–398.

    Article  Google Scholar 

  66. Il’ichev, V.G., The structure of a family of feedbacks and the stability of ecological systems, Autom. Remote Control, 1986. 1986, vol. 47, no. 12, pp. 1664–1673.

  67. Il’ichev, V.G., Structure of feedbacks with delay and stability of ecological systems, Zh. Obshch. Biol., 2009a, vol. 70, no. 4, pp. 341–348.

    PubMed  Google Scholar 

  68. Il’ichev, V.G., Ustoichivost’, adaptatsiya i upravlenie v ekologicheskikh sistemakh (Stability, Adaptation and Control in Ecological Systems), Moscow: Fizmatlit, 2009b.

  69. It Must be Beautiful: Great Equations of Modern Science, Farmelo, G., Ed., London: Granta, 2003.

    Google Scholar 

  70. Ivlev, V.S., Some questions of fed animals’ competitions, Usp. Sovrem. Biol., 1947, vol. 24, no. 6, pp. 417–432.

    Google Scholar 

  71. Ivlev, V.S., Eksperimental’naya ekologiya pitaniya ryb (Experimental Ecology of the Feeding of Fishes), Moscow: Pishchepromizdat, 1955.

  72. Ivlev, V.S., Experimental Ecology of the Feeding of Fishes, New Haven, CT: Yale Univ. Press, 1961.

    Google Scholar 

  73. Jensen, C.X.J. and Ginzburg, L.R., Paradoxes or theoretical failures? The jury is still out, Ecol. Model., 2005, vol. 188, no. 1, pp. 3–14.

    Article  Google Scholar 

  74. Jeschke, J.M. and Tollrian, R., Effects of predator confusion on functional responses, Oikos, 2005, vol. 111, no. 3, pp. 547–555.

    Article  Google Scholar 

  75. Jeschke, J.M., Kopp, M., and Tollrian, R., Consumer–food systems: why type I functional responses are exclusive to filter feeders, Biol. Rev., 2004, vol. 79, no. 2, pp. 337–349.

    Article  PubMed  Google Scholar 

  76. Jost, C., Comparing predator–prey models qualitatively and quantitatively with ecological time-series data, PhD Thesis, Paris: Inst. Natl. Agron., 1998.

  77. Jost, C. and Arditi, R., Identifying predator–prey processes from time-series, Theor. Popul. Biol., 2000, vol. 57, no. 4, pp. 325–337.

    Article  CAS  PubMed  Google Scholar 

  78. Jost, C. and Ellner, S.P., Testing for predator dependence in predator–prey dynamics: a non-parametric approach, Proc. R. Soc. B, 2000, vol. 267, no. 1453, pp. 1611–1620.

    Article  CAS  PubMed  Google Scholar 

  79. Jost, C., Arino, O., and Arditi, R., About deterministic extinction in ratio-dependent predator–prey models, Bull. Math. Biol., 1999, vol. 61, no. 1, pp. 19–32.

    Article  Google Scholar 

  80. Jost, C., Devulder, G., Vucetich, J.A., Peterson, R.O., and Arditi, R., The wolves of Isle Royale display scale-invariant satiation and ratio-dependent predation on moose, J. Anim. Ecol., 2005, vol. 74, no. 5, pp. 809–816.

    Article  Google Scholar 

  81. Kaçar, G., Wang, X.G., Biondi, A., and Daane, K.M., Linear functional response by two pupal Drosophila parasitoids foraging within single or multiple patch environments, PLoS One, 2017, vol. 12, no. 8, p. e0183525.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  82. Kolmogorov, A.N., Qualitative analysis of mathematical models of populations, in Problemy kibernetiki (Problems of Cybernetics), Moscow: Nauka, 1972, no. 25. p. 100–106.

  83. Kostitzin, V.A., Biologie Mathématique, Paris: Armand Colin, 1937.

    Google Scholar 

  84. Kovalev, O.V. and Tyutyunov, Yu.V., The role of solitary population waves in efficient suppression of adventive weeds by introduced phytophagous insects, Entomol. Rev., 2014, vol. 94, no. 3, pp. 310–319.

    Article  Google Scholar 

  85. Kratina, P., Vos, M., Bateman, A., and Anholt, B.R., Functional responses modified by predator density, Oecologia, 2009, vol. 159, no. 2, pp. 425–433.

    Article  PubMed  Google Scholar 

  86. Kuang, Y. and Freedman, H.I., Uniqueness of limit cycles in Gause-type models of predator–prey systems, Math. Biosci., 1988, vol. 88, no. 1, pp. 67–84.

    Article  Google Scholar 

  87. Lyapunov, A.A., Biogeocenoses and mathematical modelling, Priroda (Moscow), 1971, no. 10, pp. 38–41.

  88. Lyapunov, A.A. and Bagrinovskaya, G.P., On methodological problems of mathematical biology, in Matematicheskoe modelirovanie v biologii (Mathematical Modeling in Biology), Moscow: Nauka, 1975, pp. 5–18.

  89. Leslie, P.H., Some further notes on the use of matrices in population mathematics, Biometrika, 1948, vol. 35, nos. 3–4, pp. 213–245.

    Article  Google Scholar 

  90. Leslie, P.H. and Gower, J.C., The properties of a stochastic model for the predator–prey type of interaction between two species, Biometrika, 1960, vol. 47, no. 3/4, pp. 219–234.

    Article  Google Scholar 

  91. Logofet, D.O., Matrices and Graphs. Stability Problems in Mathematical Ecology, Boca Raton, FL: CRC Press, 1993.

    Google Scholar 

  92. Lotka, A.J., Elements of Physical Biology, Baltimore: Williams and Wilkins, 1925.

    Google Scholar 

  93. Luck, R.F., Evaluation of natural enemies for biological control: a behavioral approach, Trends Ecol. Evol., 1990, vol. 5, no. 4, pp. 196–199.

    Article  Google Scholar 

  94. Luckinbill, L.S., Coexistence in laboratory populations of Paramecium aurelia and its predator Didinium nasutum,Ecology, 1973, vol. 54, pp. 1320–1327.

    Article  Google Scholar 

  95. Mallet, J., The struggle for existence: how the notion of carrying capacity, K, obscures the links between demography, Darwinian evolution, and speciation, Evol. Ecol. Res., 2012, vol. 14, pp. 627–665.

    Google Scholar 

  96. Malthus, T.R., An Essay on the Principle of Population or a View of Its Past and Present Effects on Human Happiness; with an Inquiry into Our Prospects Respecting the Future Removal or Mitigation of the Evils which It Occasions, London: Reeves and Turner, 1872.

    Google Scholar 

  97. May R.M., Stability and Complexity in Model Ecosystems, Princeton: Princeton Univ. Press, 1973.

    Google Scholar 

  98. Medvinsky, A.B., Petrovskii, S.V., Tikhonov, D.A., Tikhonova, I.A., Ivanitsky, G.R., Venturino, E., and Malchow, H., Biological factors underlying regularity and chaos in aquatic ecosystems: simple models of complex dynamics, J. Biosci., 2001, vol. 26, no. 1, pp. 77–108.

    Article  CAS  PubMed  Google Scholar 

  99. Menshutkin, V.V., Matematicheskoe modelirovanie populyatsii i soobshchestv vodnykh zhivotnykh (Mathematical Modeling of Populations and Communities of Aquatic Animals), Leningrad: Nauka, 1971.

  100. Michaelis, L. and Menten, M.L., Die kinetik der invertinwirkung, Biochem. Z., 1913, vol. 49, pp. 333–369.

    CAS  Google Scholar 

  101. Molles, M.C., Jr., Ecology: Concepts and Applications, New York: McGraw-Hill, 2016, 7th ed.

    Google Scholar 

  102. Monod, J., The growth of bacterial cultures, Annu. Rev. Microbiol., 1949, vol. 3, no. 1, pp. 371–394.

    Article  CAS  Google Scholar 

  103. Murdoch, W.W., Switching in general predators: experiments on predator specificity and stability of prey populations, Ecol. Monogr., 1969, vol. 39, no. 4, pp. 335–354.

    Article  Google Scholar 

  104. Myers, J.H., Population cycles: generalities, exceptions and remaining mysteries, Proc. R. Soc. B, 2018, vol. 285, no. 1875, art. ID 20172841.

  105. Nedorezov, L.V. and Utyupin, Yu.V., Nepreryvno-diskretnye modeli dinamiki chislennosti populyatsii: analiticheskii obzor (Continuous-Discrete Models of Population Dynamics: An Analytical Review), Novosibirsk: Sib. Otd., Ross. Akad. Nauk, 2011, no. 95.

  106. Nicholson, A.J., The balance of animal populations, J. Anim. Ecol., 1933. vol. 2, suppl. 1, pp. 132–178.

    Article  Google Scholar 

  107. Nicholson, A.J. and Bailey, V.A., The balance of animal populations—Part I, Proc. Zool. Soc. Lond., 1935, vol. 3, no. 1, pp. 551–598.

    Article  Google Scholar 

  108. Oksanen, L., Moen, J., and Lundberg, P.A., The time-scale problem in exploiter–victim models: does the solution lie in ratio–dependent exploitation? Am. Nat., 1992, vol. 140, no. 6, pp. 938–960.

    Article  Google Scholar 

  109. Park, T., Experimental studies of interspecific competition. II. Temperature, humidity and competition in two species of Tribolium,Physiol. Zool., 1954, vol. 27, pp. 177–238.

    Article  Google Scholar 

  110. Pearl, R., The Biology of Population Growth, New York: A.A. Knopf, 1925.

    Google Scholar 

  111. Petrovskii, S.V. and Li, B.L., Exactly Solvable Models of Biological Invasion, Boca Raton, FL: CRC Press, 2005.

    Book  Google Scholar 

  112. Pimm, S., Food Webs, Chicago: Univ. of Chicago Press, 2002, p. 258.

    Google Scholar 

  113. Poggiale, J.C., Michalski, J., and Arditi, R., Emergence of donor control in patchy predator–prey systems, Bull. Math. Biol., 1998, vol. 60, no. 6, pp. 1149–1166.

    Article  Google Scholar 

  114. Prokopenko, C.M., Turgeon, K., and Fryxell, J.M., Evaluation of alternative prey-, predator-, and ratio-dependent functional response models in a zooplankton microcosm, Can. J. Zool., 2017, vol. 95, no. 3, pp. 177–182.

    Article  Google Scholar 

  115. Real, L.A., The kinetics of the functional response, Am. Nat., 1977, vol. 111, no. 978, pp. 289–300.

    Article  Google Scholar 

  116. Rosenzweig, M.L., Paradox of enrichment: destabilization of exploitation ecosystem in ecological time, Science, 1971, vol. 171, no. 3969, pp. 385–387.

    Article  CAS  PubMed  Google Scholar 

  117. Rosenzweig, M.L. and MacArthur, R.H., Graphical representation and stability conditions of predator–prey interactions, Am. Nat., 1963, vol. 97, no. 895, pp. 217–223.

    Article  Google Scholar 

  118. Sapoukhina, N., Tyutyunov, Yu., and Arditi, R., The role of prey taxis in biological control: a spatial theoretical model, Am. Nat., 2003, vol. 162, no. 1, pp. 61–76.

    Article  PubMed  Google Scholar 

  119. Sarnelle, O. and Wilson, A.E., Type III functional response in Daphnia, Ecology, 2008, vol. 89, no. 6, pp. 1723–1732.

    Article  PubMed  Google Scholar 

  120. Shannon, R.E., Systems Simulation: The Art and Science, Englewood Cliffs, NJ: Prentice-Hall, 1975.

    Google Scholar 

  121. Skalski, G.T. and Gilliam, J.F., Functional responses with predator interference: viable alternatives to the Holling type II model, Ecology, 2001, vol. 82, no. 11, pp. 3083–3092.

    Article  Google Scholar 

  122. Sokol, W. and Howell, J.A., Kinetics of phenol oxidation by washed cells, Biotechnol. Bioeng., 1981, vol. 23, no. 9, pp. 2039–2049.

    Article  CAS  Google Scholar 

  123. Solomon, M.E., The natural control of animal populations, J. Anim. Ecol., 1949, vol. 18, pp. 1–35.

    Article  Google Scholar 

  124. Steele, J.H. and Henderson, E.W., A simple plankton model, Am. Nat., 1981, vol. 117, no. 5, pp. 676–691.

    Article  Google Scholar 

  125. Sushchenya, L.M., Kolichestvennye zakonomernosti pitaniya rakoobraznykh (Quantitative Aspects of Feeding of Crustacea), Minsk: Nauka i Technika, 1975.

  126. Sutherland, W.J., Aggregation and the ‘ideal free’ distribution, J. Anim. Ecol., 1983, vol. 52, no. 3, pp. 821–828.

    Article  Google Scholar 

  127. Svirezhev, Yu.M., Nonlinearities in mathematical ecology: phenomena and models. Would we live in Volterra’s world?, Ecol. Model., 2008, vol. 216, no. 2, pp. 89–101.

    Article  Google Scholar 

  128. Svirezhev, Yu.M. and Logofet, D.O., Ustoichivost’ biologicheskikh soobshchestv (Stability of Biological Communities), Moscow: Nauka, 1978.

  129. Svirezhev, Yu.M. and Logofet, D.O., Stability of Biological Communities, Moscow: Mir, 1983.

  130. Tanner, J.T., The stability and the intrinsic growth rates of prey and predator populations, Ecology, 1975, vol. 56, no. 4, pp. 855–867.

    Article  Google Scholar 

  131. Trân, J.K., A predator–prey functional response incorporating indirect interference and depletion, Proc. Int. Assoc. Theor. Appl. Limnol., 2008, vol. 30, no. 2, pp. 302–305.

    Google Scholar 

  132. Tully, T., Cassey, P., and Ferrière, R., Functional response: rigorous estimation and sensitivity to genetic variation in prey, Oikos, 2005, vol. 111, no. 3, pp. 479–487.

    Article  Google Scholar 

  133. Turchin, P., Complex Population Dynamics: A Theoretical/Empirical Synthesis, Princeton, Oxford: Princeton Univ. Press, 2003, vol. 35.

    Google Scholar 

  134. Turchin, P., and Hanski, I., An empirically based model for latitudinal gradient in vole population dynamics, Am. Nat., 1997, vol. 149, no. 5, pp. 842–874.

    Article  CAS  PubMed  Google Scholar 

  135. Tyutyunov, Yu.V. and Senina, I.N., Trophic function as a result of spatial behavior, in Problemy proektirovaniya i upravleniya ekonomicheskimi sistemami: investitsionnyi aspekt (Problems of Planning and Control of Economical Systems: Investment Aspect), Rostov-on-Don: Rostovsk. Gos. Ekon. Akad., 1998, pp. 132–135.

  136. Tyutyunov, Yu., Titova, L., and Arditi, R., Predator interference emerging from trophotaxis in predator–prey systems: an individual-based approach, Ecol. Complexity, 2008, vol. 5, no. 1, pp. 48–58.

    Article  Google Scholar 

  137. Tyutyunov, Yu.V., Titova, L.I., and Berdnikov, S.V., A mechanistic model for interference and Allee effect in the predator population, Biophysics, 2013, vol. 58, no. 2, pp. 258–264.

    Article  CAS  Google Scholar 

  138. Tyutyunov, Yu.V., Titova, L.I., and Senina, I.N., Prey–taxis destabilizes homogeneous stationary state in spatial Gause–Kolmogorov-type model for predator–prey system, Ecol. Complexity, 2017, vol. 31, pp. 170–180.

    Article  Google Scholar 

  139. Tyutyunov, Yu.V., Sapoukhina, N.Yu., Senina, I.N., and Arditi, R., Explicit model for searching behavior of predator, Zh. Obshch. Biol., 2002, vol. 63, no. 2, pp. 137–148.

    Google Scholar 

  140. Tyutyunov, Yu.V., Titova, L.I., Surkov, F.A., and Bakaeva, E.N., Trophic function of phytophagous rotifers (Rotatoria). Experiment and modeling, Zh. Obshch. Biol., 2010, vol. 71, no. 1, pp. 52–62.

    Google Scholar 

  141. Veilleux, B.G., An analysis of the predatory interaction between Paramecium and Didinium,J. Anim. Ecol., 1979, vol. 48, no. 3, pp. 787–803.

    Article  Google Scholar 

  142. Verhulst, P.-F., Notice sur la loi que la population suit dans son accroissement, Corresp. Math. Phys., 1838, vol. 10, pp. 113–121.

    Google Scholar 

  143. Volterra, V., Fluctuations in the abundance of a species considered mathematically, Nature, 1926, vol. 188, pp. 558–560.

    Article  Google Scholar 

  144. Volterra, V., Leçons sur la Théorie Mathématique de la Lutte pour la Vie, Paris: Gauthier–Villars, 1931.

    Google Scholar 

  145. Vucetich, J.A., Peterson, R.O., and Schaefer, C.L., The effect of prey and predator densities on wolf predation, Ecology, 2002, vol. 83, no. 11, pp. 3003–3013.

    Article  Google Scholar 

  146. White, T.C.R., The Inadequate Environment: Nitrogen and the Abundance of Animals, Berlin: Springer-Verlag, 1993.

    Book  Google Scholar 

  147. White, T.C.R., Why Does the World Stay Green?: Nutrition and Survival of Plant-Eaters? Collingwood: CSIRO, 2005.

    Book  Google Scholar 

  148. White, T.C.R., Experimental and observational evidence reveals that predators in natural environments do not regulate their prey: they are passengers, not drivers, Acta Oecol., 2013, vol. 53, pp. 73–87.

    Article  Google Scholar 

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ACKNOWLEDGMENTS

The authors are grateful to L.R. Ginzburg and D.O. Logofet for insightful comments and stimulating discussions. We also express our gratitude to Roger Arditi for his friendship, for the long-lasting fruitful collaboration, and for attracting our interest to studying of mechanisms causing emergence of the predator interference in natural trophic systems.

Funding

The research was funded by the project 0256-2019-0038 (state reg. no. 01201363188) of SSC RAS “Development of GIS-based methods of modelling marine and terrestrial ecosystems” (for Tyutyunov), by the basic part of the state assignment research, project 1.5169.2017/8.9 of the Southern Federal University “Fundamental and applied problems of mathematical modelling” (for Titova), and Russian Foundation for Basic Research, project no. 18-01-00453 A “Multistable spatiotemporal scenarios for population models” (for Tyutyunov).

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EDITOR’S AFTERWORD

EDITOR’S AFTERWORD

Term “trophic function” has naturally appeared in mathematical theory of trophic chains by Yu.M. Svirezhev (see Ch. 5 in Svirezhev and Logofet, 1978, 1983) as the designation of function \(g\) (\(V\) in the original notations) in system (1) of differential equations that describes how the predator/consumer consumption rate depends on the prey/resource abundance (\(N\)). In English literature of those years, this function had an already established name “functional response” of predator (to the prey population density, Solomon, 1949). The result of predator’s trophic activity in terms of predator population had a name “numerical response” (Solomon, 1949), designating, as it might seem, an independent process. According to the opinion of Ginzburg and Arditi (Ginzburg, 1998; Arditi and Ginzburg, 2012) and of the authors of this review, the difference of these principal attributes had later caused the models to appear that violated physical conservation laws.

In the theory of Yu.M. Svirezhev, whose background was physics, the conservation law holds by default: the same trophic function (with the conversion coefficient \(k\)) enters the consument equation so that quantity \(\left( {1 - k} \right)\) represents the energetic loss in consumption. However, it is not the conservation law that makes Svirezhev’s theory original—his innovation was rather in replacing the growth term in the primary resource (\(R\) in original notations) equation with a constant flux (\(Q\)) of nutrients entering the system of several trophic levels.

The existence and stability conditions for equilibria in the trophic chain model were then analysed as functions of \(Q\) and other parameters (Svirezhev and Logofet, 1978, 1983). It was found that if there existed a stable positive equilibrium \(\left( {R^{*},~N_{1}^{*},N_{2}^{*}, \ldots ,~N_{n}^{*}} \right)\) corresponding to a trophic chain of n levels, then all equilibria with the number of levels less than \(n\) became unstable. Furthermore, there are no partially positive equilibria with zero population densities below the nth level. Moreover, there are threshold values of parameter \(Q\): \(Q_{1}^{*},Q_{2}^{*},Q_{3}^{*}, \ldots ~\) subdividing the virtual Q-axis into a set of non-overlapping intervals within which there exist stable chains with one, two, three,… trophic levels (Fig. 7). In other words, if in a stably functioning trophic chain the flux of nutrients reduces for some reason to a value of \(Q\) from a neighboring interval, then the top trophic level loses its stability and goes to extinction; if the flux \(Q\) increases in similar manner, then the higher trophic level can be occupied by an appropriate top predator.

Fig. 7.
figure 7

Results of mathematical theory of trophic chains by Yu.M. Svirezhev. See text for details.

Thus, the mathematical results comply with biological understanding of trophic chain structures and functioning, and the theory of Yu.M. Svirezhev is an exempt from “trophic” paradoxes mentioned in this review. The theory was built for trophic functions depending on the prey/resource abundance or density, N. The question is whether the theory will retain its elegance with the RD trophic functions.

Dmitrii O. Logofet

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Tyutyunov, Y.V., Titova, L.I. From Lotka–Volterra to Arditi–Ginzburg: 90 Years of Evolving Trophic Functions. Biol Bull Rev 10, 167–185 (2020). https://doi.org/10.1134/S207908642003007X

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