Abstract
Abrupt transitions leading to algal blooms are quite well known in aquatic ecosystems and have important implications for the environment. These ecosystem shifts have been largely attributed to nutrient dynamics and food web interactions. Contamination with heavy metals such as copper can modulate such ecological interactions which in turn may impact ecosystem functioning. Motivated by this, we explored the effect of copper enrichment on such regime shifts in planktonic systems. We integrated copper contamination to a minimal phytoplankton–zooplankton model which is known to demonstrate abrupt transitions between ecosystem states. Our results suggest that both the toxic and deficient concentration of copper in water bodies can lead to regime shift to an algal-dominated alternative stable state. Further, interaction with fish density can also lead to collapse of population cycles thus leading to algal domination in the intermediate copper ranges. Environmental stochasticity may result in state transition much prior to the tipping point and there is a significant loss in the bimodality on increasing intensity and redness of noise. Finally, the impending state shifts due to contamination cannot be predicted by the generic early warning indicators unless the transition is close enough. Overall the study provides fresh impetus to explore regime shifts in ecosystems under the influence of anthropogenic changes like chemical contamination.
Similar content being viewed by others
References
Banerjee S, Sarkar RR, Chattopadhyay J (2019) Effect of copper contamination on zooplankton epidemics. J Theor Biol 469:61–74
Baudena M, Boni G, Ferraris L, Von Hardenberg J, Provenzale A (2007) Vegetation response to rainfall intermittency in drylands: Results from a simple ecohydrological box model. Adv Water Resour 30(5):1320–1328
Beisner BE, Haydon DT, Cuddington K (2003) Alternative stable states in ecology. Front Ecol Environ 1(7):376–382
Boettiger C, Hastings A (2013) No early warning signals for stochastic transitions: insights from large deviation theory. Proc Roy Soc B: Biol Sci 280(1766):20131372
Bossuyt BT, Janssen CR (2003) Acclimation of Daphnia magna to environmentally realistic copper concentrations. Comp Biochem Physiol C Toxicol Pharmacol 136:253–264
Camara BI, Yamapi R, Mokrani H (2017) How do copper contamination pulses shape the regime shifts of phytoplankton-zooplankton dynamics? Commun Nonlinear Sci Numer Simul 48:170–178
Carpenter SR (2005) Eutrophication of aquatic ecosystems: bistability and soil phosphorus. Proc Natl Acad Sci USA 102(29):10002–10005
Carpenter SR (2008) Phosphorus control is critical to mitigating eutrophication. Proc Natl Acad Sci USA 105(32):11039–11040
Carpenter SR, Cole JJ, Pace ML, Batt R, Brock W, Cline T, Coloso J, Hodgson JR, Kitchell JF, Seekell DA et al (2011) Early warnings of regime shifts: a whole-ecosystem experiment. Science 332(6033):1079–1082
Clements WH, Cherry DS, Hassel JHV (1992) Assessment of the impact of heavy metals on benthic communities at the Clinch River (Virginia): evaluation of an index of community sensitivity. Can J Fish Aquat Sci 49:1686–1694
Dakos V, Carpenter SR, Brock WA, Ellison AM, Guttal V, Ives AR, Kefi S, Livina V, Seekell DA, van Nes EH et al (2012) Methods for detecting early warnings of critical transitions in time series illustrated using simulated ecological data. PLoS One 7(7)
Dennis B (1998) Moving toward an unstable equilibrium: saddle nodes in population systems. J Anim Ecol 67(2):298–306
Dhooge A, Govaerts W, Kuznetsov YA, Meijer HGE, Sautois B (2008) New features of the software matcont for bifurcation analysis of dynamical systems. Math Comput Model Dyn Syst 14(2):147–175
Drake JM (2013) Early warning signals of stochastic switching. Proc Roy Soc B: Biol Sci 280(1766):20130686
Evans SN, Ralph PL, Schreiber SJ, Sen A (2013) Stochastic population growth in spatially heterogeneous environments. J Math Biol 66(3):423–476
Fargašová A, Bumbálová A, Havránek E (1999) Ecotoxicological effects and uptake of metals (\(Cu^+, Cu^{2+}, Mn^{2+}, Mo^{6+}, Ni^{2+}, V^{5+}\)) in freshwater alga Scenedesmus quadricauda. Chemosphere 38:1165–1173
Flemming C, Trevors J (1989) Copper toxicity and chemistry in the environment: a review. Water Air Soil Pollut 44(1–2):143–158
Folke C, Carpenter S, Walker B, Scheffer M, Elmqvist T, Gunderson L, Holling CS (2004) Regime shifts, resilience, and biodiversity in ecosystem management. Annu Rev Ecol Evol Syst 35:557–581
Garay-Narváez L, Arim M, Flores JD, Ramos-Jiliberto R (2013) The more polluted the environment, the more important biodiversity is for food web stability. Oikos 122(8):1247–1253
Gutierrez MF, Paggi JC, Gagneten AM (2012) Microcrustaceans escape behavior as an early bioindicator of copper, chromium and endosulfan toxicity. Ecotoxicology 21:428–438
Guttal V, Jayaprakash C (2007) Impact of noise on bistable ecological systems. Ecol Model 201(3–4):420–428
Halley JM (1996) Ecology, evolution and 1f-noise. Trends Ecol Evol 11(1):33–37
Hassell M, Lawton J, Beddington J (1977) Sigmoid functional responses by invertebrate predators and parasitoids. J Anim Ecol 249–262
Hastings A (2004) Transients: the key to long-term ecological understanding? Trends Ecol Evol 19(1):39–45
Havens KE (1994) Structural and functional responses of a freshwater plankton community to acute copper stress. Environ Pollut 86:259–266
Higham DJ (2001) An algorithmic introduction to numerical simulation of stochastic differential equations. SIAM Rev 43(3):525–546
Huang Q, Parshotam L, Wang H, Bampfylde C, Lewis MA (2013) A model for the impact of contaminants on fish population dynamics. J Theor Biol 334:71–79
Huang Q, Wang H, Lewis MA (2015) The impact of environmental toxins on predator-prey dynamics. J Theor Biol 378:12–30
Ingersoll CG, Winner RW (1982) Effect on Daphnia pulex (de geer) of daily pulse exposures to copper or cadmium. Environ Toxicol Chem 1:321–327
Jorgensen E (2010) Ecotoxicology. Academic Press
Kéfi S, Dakos V, Scheffer M, Van Nes EH, Rietkerk M (2013) Early warning signals also precede non-catastrophic transitions. Oikos 122(5):641–648
Kim Y, Son J, Mo H-H, Lee Y-S, Cho K (2018) Modeling the influence of initial density and copper exposure on the interspecific competition of two algal species. Ecol Model 383:160–170
Knops M, Altenburger R, Segner H (2001) Alterations of physiological energetics, growth and reproduction of Daphnia magna under toxicant stress. Aquat Toxicol 53:79–90
Koivisto S, Ketola M, Walls M (1992) Comparison of five cladoceran species in short-and long-term copper exposure. Hydrobiologia 248:125–136
Kooi B, Bontje D, Van Voorn G, Kooijman S (2008) Sublethal toxic effects in a simple aquatic food chain. Ecol Model 212(3–4):304–318
Lebrun JD, Perret M, Geffard A, Gourlay-Francé C (2012) Modelling copper bioaccumulation in Gammarus pulex and alterations of digestive metabolism. Ecotoxicology 21:2022–2030
Luecke C, Vanni MJ, Magnuson JJ, Kitchell JF, Jacobson PT (1990) Seasonal regulation of Daphnia populations by planktivorous fish: Implications for the spring clear-water phase. Limno Oceanogr 35(8):1718–1733
Luoma SN, Rainbow PS (2005) Why is metal bioaccumulation so variable? biodynamics as a unifying concept. Environ Sci Technol 39:1921–1931
McQueen D, Post J (1988) Cascading trophic interactions: Uncoupling at the zooplankton-phytoplankton link. Hydrobiologia 159(3):277–296
Mertz W (1981) The essential trace elements. Science 213:1332–1338
Mills E, Forney J, Wagner K (1987) Fish predation and its cascading effect on the Oneida Lake food chain. In Predation: direct and indirect impacts on aquatic communities. University Press of New England, Hanover, NH 118–131
Møller JK, Carstensen J, Madsen H, Andersen T (2009) Dynamic two state stochastic models for ecological regime shifts. Environmetrics 20(8):912–927
Murdoch W, Nisbet R, McCauley E, DeRoos A, Gurney W (1998) Plankton abundance and dynamics across nutrient levels: tests of hypotheses. Ecology 79:1339–1356
O’Keefe TC, Brewer MC, Dodson SI (1998) Swimming behavior of Daphnia: its role in determining predation risk. J Plankton Res 20:973–984
Pace ML, Carpenter SR, Johnson RA, Kurtzweil JT (2013) Zooplankton provide early warnings of a regime shift in a whole lake manipulation. Limnol Oceanogr 58(2):525–532
Petrovskii S, Sekerci Y, Venturino E (2017) Regime shifts and ecological catastrophes in a model of plankton-oxygen dynamics under the climate change. J Theor Biol 424:91–109
Prosnier L, Loreau M, Hulot FD (2015) Modeling the direct and indirect effects of copper on phytoplankton zooplankton interactions. Aquat Toxicol 162:73–81
Real LA (1977) The kinetics of functional response. Am Nat 111(978):289–300
Rietkerk M, Dekker SC, De Ruiter PC, van de Koppel J (2004) Self-organized patchiness and catastrophic shifts in ecosystems. Science 305(5692):1926–1929
Rip J, McCann K (2011) Cross-ecosystem differences in stability and the principle of energy flux. Ecol Lett 14(8):733–740
Scheffer M (1997) Ecology of shallow lakes. Springer Science & Business Media vol 22
Scheffer M, Bascompte J, Brock WA, Brovkin V, Carpenter SR, Dakos V, Held H, Van Nes EH, Rietkerk M, Sugihara G (2009) Early-warning signals for critical transitions. Nature 461(7260):53–59
Scheffer M, Carpenter S, Foley JA, Folke C, Walker B (2001) Catastrophic shifts in ecosystems. Nature 413(6856):591–596
Scheffer M, Carpenter SR (2003) Catastrophic regime shifts in ecosystems: linking theory to observation. Trends Ecol Evol 18(12):648–656
Scheffer M, De Boer RJ (1995) Implications of spatial heterogeneity for the paradox of enrichment. Ecology 76(7):2270–2277
Scheffer M, Hosper S, Meijer M, Moss B, Jeppesen E (1993) Alternative equilibria in shallow lakes. Trends Ecol Evol 8(8):275–279
Scheffer M, Rinaldi S, Kuznetsov YA (2000) Effects of fish on plankton dynamics: a theoretical analysis. Can J Fish Aquat Sci 57(6):1208–1219
Sekerci Y, Petrovskii S (2015a) Mathematical modelling of plankton-oxygen dynamics under the climate change. Bull Math Biol 77(12):2325–2353
Sekerci Y, Petrovskii S (2015b) Mathematical modelling of spatiotemporal dynamics of oxygen in a plankton system. Math Model Nat Phenom 10(2):96–114
Sharma Y, Abbott KC, Dutta PS, Gupta A (2015) Stochasticity and bistability in insect outbreak dynamics. Theor Ecol 8(2):163–174
Stoyanov M, Gunzburger M, Burkardt J (2011) Pink noise, 1/f \(\alpha\) noise, and their effect on solutions of differential equations. Int J Uncertain Quan 1(3)
Sullivan B, Buskey E, Miller D, Ritacco P (1983) Effects of copper and cadmium on growth, swimming and predator avoidance in Eurytemora affinis (copepoda). Mar Biol 77:299–306
Untersteiner H, Kahapka J, Kaiser H (2003) Behavioural response of the cladoceran Daphnia magna STRAUS to sublethal copper stress-validation by image analysis. Aquat Toxicol 65:435–442
WHO (1998) Copper. Environmental health criteria 200
Wilson MA, Carpenter SR (1999) Economic valuation of freshwater ecosystem services in the united states: 1971–1997. Ecol Appl 9(3):772–783
Wright DI, O’Brien WJ (1982) Differential location of Chaoborus larvae and Daphnia by fish: the importance of motion and visible size. Am Midl Nat 108:68–73
Yan H, Pan G (2002) Toxicity and bioaccumulation of copper in three green microalgal species. Chemosphere 49:471–476
Acknowledgements
Swarnendu Banerjee acknowledges Senior Research Fellowship from Council of Scientific and Industrial Research, India. The authors would also like to thank Hil Meijer, University of Twente for confirming the MATCONT simulations for the two parameter bifurcation diagram.
Funding
No funding was received for conducting this study.
Author information
Authors and Affiliations
Contributions
SB and BS conceived the idea; SB, BS, MR, MB, and JC refined it; SB and BS designed the simulations; SB programmed the simulations and ran the experiments; SB wrote the first draft; All authors commented on the previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflicts of interest
The authors have no competing interest to declare that are relevant to the content of this article.
Appendices
Appendix
Effect of stochasticity in low copper concentrations
Deficient copper concentrations also lead to bistable system dynamics resulting in planktonic regime shifts. The effect of stochasticity on such low ranges of copper concentration is examined when carrying capacity \(K=2\). Similar to the toxic concentration case, the system switches to phytoplankton-dominated state prior to the fold bifurcation. The probability density of the observed values from the simulation is unimodal with mode around zooplankton-dominated equilibrium at copper concentration 5.1 \(\mu g L^{-1}\). Subsequent small decrease of copper results in the system demonstrating bimodality at concentration 5.095 \(\mu g L^{-1}\) and unimodal mode around phytoplankton-dominated state at concentration 5.085 \(\mu g L^{-1}\) (see Fig. 9). Increased intensity of noise leads to decreased skewness of the probability densities.
Basin of attraction for the alternative stable states
The stochastic switch between the attractors in Fig. 7 can be understood with the help of basin of attraction for the two equilibria under different carrying capacities. When \(K=2\), the boundary separating the basin of attraction is very close to both the phytoplankton and zooplankton-dominated equilibrium which facilitates multiple stochastic switching. On the other hand, the boundary is relatively farther away from the two attractor in case of higher carrying capacity, i.e., \(K=3\) resulting in very infrequent switch.
Rights and permissions
About this article
Cite this article
Banerjee, S., Saha, B., Rietkerk, M. et al. Chemical contamination-mediated regime shifts in planktonic systems. Theor Ecol 14, 559–574 (2021). https://doi.org/10.1007/s12080-021-00516-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12080-021-00516-8