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Tri-trophic plankton models revised: importance of space, food web structure and functional response parametrisation. (English) Zbl 06849692

Summary: Revealing mechanisms of efficient top-down control in eutrophic ecosystems remains a long term challenge in theoretical ecology. In this paper, we revisit the role of environmental heterogeneity, food web structure and shape of the predator functional response in persistence and stabilization of a planktonic system with high nutrient supply. We consider a 1D vertically resolved tri-trophic planktonic food web composed of a primary producer, an intermediate predator and a highly mobile top predator, such as a system of phytoplankton, microzooplankton and copepods. We explore the realistic scenario in which the top predator is omnivorous, i.e. when copepods can feed both on phytoplankton and microzooplankton. We show that the interplay between heterogeneity of the environment due to for instance, a light gradient in the water column, and trophic interaction between species can result in an efficient top-down control which would otherwise be impossible in the corresponding well-mixed system. We also find that allowing the top predator to feed on the primary producer may dramatically impede the coexistence of the three trophic levels, with only two levels generally surviving. The coexistence of all three trophic levels within a wide range of parameters becomes possible only when the top predator exhibits active food source switching behaviour. We also show the phenomenon of bistability in the considered tri-trophic food web: a small initial amount of the top predator should lead to its extinction whereas introduction of a supercritical initial amount will eventually result in establishment of the population. The demonstrated mechanism of top-down control seems to be rather generic and might be a good candidate to explain stability in some other non-planktonic tri-trophic ecosystems.

MSC:

47A75 Eigenvalue problems for linear operators
45K05 Integro-partial differential equations
92D40 Ecology
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[1] M.W. Adamson, A. Yu. Morozov. When can we trust our model predictions? Unearthing structural sensitivity in biological systems. Proc. R. Soc. A, 469 (2012), 20120500. · Zbl 1371.92057
[2] P.A. Abrams, C.J. Walters. Invulnerable prey and the paradox of enrichment. Ecology, 77 (1996), 1125-1133.
[3] A. Beckmann, I. Hense. Beneath the surface: characteristics of oceanic ecosystems under weak mixing conditions - a theoretical investigation. Prog. Oceanogr., 75 (2007), 771-796.
[4] M. N. Breckels, N. W. F. Bode, E. A. Codling, M. Steinke. The effect of grazing-mediated DMS production on the behaviour of the copepod Calanus helgolandicus. Mar. Drugs, 11 (2013), 2486-2500.
[5] P.W. Boyd. Environmental factors controlling phytoplankton processes in the Southern Ocean. J. Phycol., 38 (2002), 844-861.
[6] P.W. Boyd, S.M. Smith, T. Cowles. Grazing patterns of copepods in the upwelling system off Peru. Limnol. Oceanogr., 25 (1980), 583-596.
[7] A. Calbet, F. Carlotti, R. Gaudy. The feeding ecology of the copepod Centropages typicus (Kroyer). Prog. Oceanogr., 72 (2007), 137-150
[8] F. Carlotti, and S. Nival Moulting and mortality rates of copepods related to age within stage: Experimental results. Mar. Ecol. Prog. Ser., 84 (1992), 235-243.
[9] F.P. Chavez, K.R. Buck, R.T. Barber. Phytoplankton taxa in relation to primary production in the equatorial Pacific. Deep Sea Res. 37 (1990), 1733-1752.
[10] P. Chow-Fraser, W.G. Sprules. Type-3 functional response in limnetic suspension-feeders, as demonstrated by in situ grazing rates. Hydrobiologia, 232 (1992), 175-191.
[11] F. Cordoleani, D. Nerini, M. Gauduchon, A. Morozov, J-C. Poggiale. Structural sensitivity of biological models revisited. J. Theor. Biol. 283 (2011), 82-91 · Zbl 1397.92565
[12] F. Courchamp, L. Berec, J. Gascoigne. Allee Effects in Ecology and Conservation. Oxford Uni. Press, Oxford, 2006.
[13] J.J. Cullen, M.R. Lewis, C.O. Davis, R.T. Barber. Photosynthetic characteristics and estimated growth rates indicate that grazing is the proximate control of primary production in the equatorial Pacific. J. Geophys. Res., 97(1992), 639-654
[14] B. Dennis. Allee effect: population growth, critical density, and chance of extinction. Nat. Resour. Model., 3 (1989), 481-538. · Zbl 0850.92062
[15] E.G. Durbin, A.G. Durbin. Effects of temperature and food abundance on grazing and short-term weight change in the marine copepod Acartia hudsonica. Limnol. Oceanogr., 37 (1996), 361-378
[16] A. M. Edwards, J. Brindley. Zooplankton mortality and the dynamical behaviour of plankton population models. Bull. Math. Biol., 61 (1999), 303-339. · Zbl 1323.92162
[17] C. A. Edwards, H. P. Batchelder, T. M. Powell. Modeling microzooplankton and macrozooplankton dynamics within a coastal upwelling system. J. Plankton Res., 22 (2000a), 1619-1648.
[18] C. A. Edwards, T. A. Powell, H. P. Batchelder. The stability of an NPZ model subject to realistic levels of vertical mixing. J. Mar. Res., 58 (2000b), 37-60.
[19] A.M. Edwards, A Yool. The role of higher predation in plankton population models. J. Plankton Res., 22 (2000), 1085-1112
[20] K. F. Edwards, M. K. Thomas, C. A. Klausmeier, E. Litchman. Light and growth in marine phytoplankton: Allometric, taxonomic, and environmental variation. Limnol. Oceanogr., 60 (2015), 540-552
[21] J.Z. Farkas, A. Yu. Morozov, E.G. Arashkevich, A. Nikishina. Revisiting the stability of spatially heterogeneous predator-prey systems under eutrophication. Bull. Math. Biol., 77 (2015), 1886-1908. · Zbl 1339.92071
[22] B.W. Frost. Grazing control of phytoplankton stock in the open subarctic Pacific Ocean: a model assessing the role of mesozooplankton, particularly the large calanoid copepods Neocalanus spp. Mar. Ecol. Prog. Ser., 39 (1987), 49-68.
[23] G.F. Fussmann, B. Blasius. Community response to enrichment is highly sensitive to model structure. Biol. Lett., 1(2005), 9-12
[24] A. Gabric, N. Murray, L. Stone, M. Kohl. Modelling the production of dimethylsulfide during a phytoplankton bloom. J. Geophys. Res., 98 (1993), 22805-22816.
[25] M. Genkai-Kato, N. Yamamura. Unpalatable prey resolves the paradox of enrichment. P. Roy. Soc. Lond. B. Bio., 266, (1999), 1215-1219
[26] W. Gentleman, A. Leising, B. Frost, S. Storm, J. Murray. Functional responses for zooplankton feeding on multiple resources: a review of assumptions and biological dynamics. Deep-sea Res. Pt. II, 50 (2003), 2847-2875.
[27] I. Gismervik, Top-down impact by copepods on ciliate numbers and persistence depends on copepod and ciliate species composition. J. Plankton Res., 28 (2006), 499-507.
[28] I. Gismervik, T. Andersen. Prey switching by Acartia clausi: experimental evidence and implications of intraguild predation assessed by a model. Mar. Ecol. Prog. Ser., 157(1997), 247-259
[29] P. J. Hansen, P.K. Bjornsen, B.W Hansen. Zooplankton grazing and growth: Scaling within the 2-2000 μm body size range. Limnol. Oceanogr., 42 (1997), 687-704.
[30] F. C. Hansen, M. Reckermann, W. C. M. Klein Breteler. Phaeocystis blooming enhanced by copepod predation on protozoa: evidence from incubation experiments. Mar. Ecol. Prog. Ser., 102 (1993), 51-57.
[31] C.X.J. Jensen, L.R. Ginzburg. Paradoxes or theoretical failures? The jury is still out. Ecol. Model., 188 (2005), 3-14.
[32] A. Kharab, R. B. Guenther. An Introduction to Numerical Methods: A MATLAB Approach. Third edition. CRC Press, Boca Raton, 2012. · Zbl 1378.65003
[33] T. Kierboe, Saiz, M. Viitasalo. Prey switching behaviour in the planktonic copepod Acartia tonsa. Mar. Ecol. Prog. Ser., 143(1996), 65-75.
[34] W. Lampert. Vertical distribution of zooplankton: density dependence and evidence for an ideal free distribution with costs. BMC Biol., 3 (2005), 10.
[35] N. Lewis, A. Morozov, M. Breckels, M. Steinke, and E. Codling. Multitrophic interactions in the sea: assessing the effect of infochemical-mediated foraging in a 1-d spatial model. MMNP, 8(2013), 25-44. · Zbl 1321.92068
[36] K.M. Meyer, M. Vos, W. M. Mooij, W. H. G. Hol, A. J. Termorshuizen, W. H. van der Putten. Testing the paradox of enrichment along a land use gradient in a multitrophic aboveground and belowground community. PLoS ONE 7 (2012): e49034.
[37] A. Yu. Morozov, M. Sen, M. Banerje. Top-down control in a patchy environment: Revisiting the stabilizing role of food-dependent predator dispersal. Theor. Popul. Biol., 81 (2012), 9-19. · Zbl 1322.92060
[38] A. Yu. Morozov. Incorporating complex foraging of zooplankton in models: role of micro and mesoscale processes in macroscale patterns. In Dispersal, individual movement and spatial ecology: a mathematical perspective (eds M Lewis, P Maini & S Petrovskii), pp. 1-10. New York, NY: Springer, 2011. · Zbl 1347.92107
[39] A. Yu. Morozov, E.G. Arashkevich, A. Nikishina, K Solovyev. Nutrient-rich plankton communities stabilized via predator-prey interactions: revisiting the role of vertical heterogeneity. Math. Med. Biol., 28 (2011), 185-215 · Zbl 1216.92066
[40] A. Yu. Morozov, A. F. Pasternak, E. G. Arashkevich. Revisiting the role of individual variability in population persistence and stability. PLoS ONE, (8) (2013), e70576.
[41] A. Yu. Morozov, S.V. Petrovskii. Feeding on multiple sources: towards a universal parameterization of the functional response of a generalist predator allowing for switching. PLoS ONE, (8) (2013), e74586. doi: .
[42] A. Mougi, K. Nishimura. A resolution of the paradox of enrichment. J. Theor. Biol., 248, (2007), 194-201 · Zbl 1451.92263
[43] W.W. Murdoch. The functional response of predators. J. Appl. Ecol., 10 (1973), 335-342
[44] S. Petrovskii S, B. Li, H. Malchow. Transition to spatiotemporal chaos can resolve the paradox of enrichment. Ecol. Complex, 1 (2004), 37-47.
[45] G.A. Polis, R.D. Holt. 1992. Intraguild predation: the dynamics of complex trophic interactions. Trends. Ecol. Evol., 7 (1992), 151-155
[46] J.E.G. Raymont. Plankton and Productivity in the Oceans. Phytoplankton, Vol. 1 Pergamon. Oxford (1980)
[47] A. B. Ryabov, L. Rudolf, B. Blasius. Vertical distribution and composition of phytoplankton under the influence of an upper mixed layer. J. Theor. Biol., 263 (2010), 120-133. · Zbl 1406.92685
[48] A. B. Ryabov, A. Morozov, B. Blasius Imperfect prey selectivity of predators promotes biodiversity and irregularity in food webs. Ecol. Letts., 18.11 (2015), 1262-1269.
[49] M. L. Rosenzweig. Paradox of enrichment: destabilization of exploitation ecosystems in ecological time. Science, 171 (1971), 385-387.
[50] M. L. Rosenzweig, R. H. MacArthur. Graphical representation and stability conditions of predator-prey interactions. Am. Nat., 97 (1963), 209-223.
[51] S. Roy, J. Chattopadhyay. The stability of ecosystems: a brief overview of the paradox of enrichment. J. Bioscience, 32(2007), 421-428.
[52] P.A. Stephens, W.J. Sutherland. Consequences of the Allee effect for behaviour, ecology and conservation. Trends. Ecol. Evol., 14 (1999), 401-405.
[53] D.K. Stoecker, J.M. Capuzzo. Predation on Protozoa: its importance to zooplankton. J. Plankton Res., 12 (1990), 891-908
[54] W. K. Tang, and M. Taal Trophic modification of food quality by heterotrophic protists: species-specific effects on copepod egg production and egg hatching. J. Exp. Mar. Biol. Ecol., 318.1 (2005), 85-98.
[55] P. Tiselius, P.R. Jonsson. Foraging behaviour of six calanoid copepods: observations and hydrodynamic analysis. Mar. Ecol. Prog. Ser., 66(1990), 23-33
[56] S. M. Vallina, B. Ward, S. Dutkiewicz, and M. Follows. Maximal feeding with active preyswitching: A kill-the-winner functional response and its effect on global diversity and biogeography, Prog. Oceanogr., 120 (2014), 93-109.
[57] L. van Duren, J. Videler, Swimming behaviour of developmental stages of the calanoid copepod Temora longicornis at different food concentrations. Mar. Ecol. Prog. Ser., 126 (1995), 153-161.
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